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Four groups of dogs, which had been subjected to housing conditions of varying quality for years, were assumed to experience different levels of stress. The groups were compared for behavioural and hormonal parameters in order to identify measures that indicate chronic stress in the dog and which may help to identify poor welfare in this species. As a standard for comparison, one of the four groups was composed of privately owned dogs; we assumed that chronic stress levels were relatively low in this group (GI). The three remaining groups of dogs (GII, GIII and GIV) were kept under conditions of low to relatively high austerity, and had basal urinary ratios of cortisol to creatinine, adrenaline to creatinine and, to a lesser extent, noradrenaline to creatinine, that varied from low to high, respectively. Significant differences (P < 0.05) were found in cortisol to creatinine ratios when comparing GI to GII, GIII and GIV and when GII was compared to GIV. Statistical analyses indicated that the mean adrenaline to creatinine ratio in GI differed from that in the remaining groups and that the ratio in GII differed from that in GIII. Noradrenaline to creatinine ratios differed significantly only between GI and GIII. Dopamine to creatinine ratios and noradrenaline to adrenaline ratios did not differ significantly between groups. When dogs were not disturbed, those that were kept under the most austere conditions typically had high levels of locomotor activity, nosing, urinating and paw lifting. After mild disturbance by a slamming door or in the presence of a researcher these animals reacted actively, with increased locomotor activity, circling and nosing, and they showed high levels of behaviours that have previously been associated with acute stress: body shaking, yawning, ambivalent postures and displacement behaviours. Chronic stress in dogs may be identified by increased paw lifting when animals are not disturbed and by ample behavioural expressions of arousal when they are mildly stimulated. Since some behaviours may occur in contexts not related to stress, behavioural data are easily misinterpreted with regard to chronic stress. Interpretation will only be meaningful when physiological measures such as urinary adrenaline to creatinine ratios and, especially, urinary cortisol to creatinine ratios are also determined.
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BEHAVIOURAL AND HORMONAL INDICATORS OF
ENDURING ENVIRONMENTAL STRESS IN DOGS
B Beerda
l,2,
M B H Schilder
t2,
JAR A M van Hooff
2,
H W de Vries
l
andJ
A
Moll
Department of Clinical Sciences of Companion Animals, Utrecht University, The Netherlands
2Department of Ethology and Socio-Ecology, Utrecht University, Padualaan 14, PO Box 14,3508
TB, Utrecht, The Netherlands
t
Contact for correspondence and requests for reprints
Final Acceptance: 7 April 1999
Abstract Animal Welfare 2000,
9:
49-62
Four groups of dogs, which had been subjected to housing conditions of varying quality for
years, were assumed to experience different levels of stress. The groups were compared for
behavioural and hormonal parameters in order to identifYmeasures that indicate chronic stress
in the dog and which may help to identifY poor welfare in this species. As a standard for
comparison, one of thefour groups was composed of privately owned dogs; we assumed that
chronic stress levels were relatively low in this group (GI). The three remaining groups of dogs
(GIl, GIIl and GIV) were kept under conditions of low to relatively high austerity, and had basal
urinary ratios of cortisol to creatinine, adrenaline to creatinine and, to a lesser extent,
noradrenaline to creatinine, that varied from low to high, respectively. Significant differences
(P
<
0.05) werefound in cortisol to creatinine ratios when comparing GI to GIl, GIll and GIV
and when GIl was compared to GIV. Statistical analyses indicated that the mean adrenaline to
creatinine ratio in GI differed from that in the remaining groups and that the ratio in GIl
differedfrom that in GIll Noradrenaline to creatinine ratios differed significantly only between
GI and GIll Dopamine to creatinine ratios and noradrenaline to adrenaline ratios did not differ
significantly between groups. When dogs were not disturbed, those that were kept under the
most austere conditions typically had high levels of locomotor activity, nosing, urinating and
paw lifting. After mild disturbance by a slamming door or in the presence of a researcher these
animals reacted actively, with increased locomotor activity, circling and nosing, and they
showed high levels of behaviours that have previously been associated with acute stress: body
shaking, yawning, ambivalent postures and displacement behaviours. Chronic stress in dogs
may be identified by increased paw lifting when animals are not disturbed and by ample
behavioural expressions of arousal when they are mildly stimulated. Since some behaviours may
occur in contexts not related to stress, behavioural data are easily misinterpreted with regard
to chronic stress. Interpretation will only be meaningful when physiological measures such as
urinary adrenaline to creatinine ratios and, especially, urinary cortisol to creatinine ratios are
also determined.
Keywords: animal welfare, behaviour, chronic stress, dog, urinary catecholamines, urinary
cortisol
© 2000, UFAW, The Old School, Brewhouse Hill, Wheathampstead, Herts AL4 8AN, UK
Animal Welfare2000,9: 49-62
49
Beerda et al
Introduction
Animal shelters, breeding stations, animal boarding houses and laboratories are examples of
situations where living conditions may be austere and stressful to dogs. The assessmel1t of
welfare problems in dogs requires tools that measure poor welfare in this species. Humans who
experience reduced welfare show signs of stress (Silver & Wortman 1980; Hilton 1989; Kathol
et a11989; J0rgensen et a11990; Herbert &Cohen 1993). Following similar reasoning (for a
discussion see Stafleu et al [1992]), it can be argued that dogs also show expressions of stress
when they experience poor welfare. Thus, the measurement of stress parameters constitutes a
way of identifying welfare problems in dogs. Stressful situations that endure, say for several
days, may induce different stress responses, and will be more detrimental to a dog's state of
welfare, than when such situations are relatively short-lasting. Since welfare is most seriously
compromised in situations of enduring stress, parameters that indicate chronic stress are more
useful for detecting welfare problems than parameters that change only temporarily at the onset
of the stressor (ie acute stress parameters).
Previously, we have studied behavioural and physiological indicators of chronic stress in
socially and spatially restricted Beagles (Beerda et a11999a, b). It is unclear whether or not our
findings also apply to other, non-experimental, settings. The experimental animals that we used
in that study were socially and spatially restricted for only 6 weeks and they were homogenous
with regards to breed, age and life history. In any non-experimental setting, the dogs under study
are likely to differ from the animals that we studied. Moreover, the stressor to which they are
exposed may not resemble the treatment that we applied and it may last considerably longer than
6 weeks. As a result, dogs that are exposed to stressful situations may show responses that
deviate from the ones that we have reported. The present study aims to establish the practical
use of behavioural and physiological measurements for the assessment of chronic stress under
minimally controlled conditions.
Four groups of dogs that had been living for years under relatively enriched conditions or in
conditions of three degrees of austerity were assumed to have experienced levels of stress that
varied accordingly. The groups were compared with regards to behavioural parameters, urinary
cortisol and urinary catecho1amines. We aimed to identify behavioural and physiological
characteristics that typically manifest themselves under rather austere living conditions and that
indicate chronic stress in dogs. Behavioural parameters, urinary cortisol and urinary
catecholamines were measured because they indicate the activity of biological systems that are
known to respond in acutely stressed dogs, namely behaviour (Solomon
&
Wynne 1953; Corson
1971; Schwizgebel1982; Engeland et aI1990), the hypothalamic-pituitary-adrenal (HPA) axis
(Clower et a11979; Dess et a11983; Palazzolo & Quadri 1987; Assia et a11989; Bueno et al
1989; Gue et a11989; Engeland et a11990) and the sympathetic-adrenal-medullary (SAM)
system (Anderson & Brady 1972; Lown et a11973; Gaebelein et aI1977; Galosy et a11979;
Pagani et aI1991). Moreover, we have previously found that behaviour and cortisol levels may
also respond in chronically stressed dogs (Beerda et a11999a, b).
The groups of dogs that we studied were not balanced for factors like breed, gender and age.
However, intra-group comparisons were made to fmd out how variation in breed, gender and
age may have biased the measurement of chronic stress.
In summary, we wanted to know which behavioural and hormonal parameters distinguish
dogs which are kept poorly from those which are kept well, and, as such, have practical use as
indicators of poor welfare. For the same reason, we investigated correlations between cortisol
secretion, as an established indicator of stress, and the remainder of the parameters.
50
Animal Welfare 2000, 9: 49-62
Enduring stress in dogs
Methods
Animals
Data were obtained from 72 dogs that were categorized in accordance with the conditions under
which they were maintained. Preceding the collection of data, the dogs' housing conditions had
been unchanged for 1year or longer. Group sizes and statistics with regards to gender, breed and
age are summarized in Table I. Dogs in group GI were privately owned. On working days, from
0800h to 1700h, these dogs were maintained in outdoor kennels of 4.3m2. Between 1200h and
1400h the dogs were taken outside for a walk. GIl individuals were housed individually in
kennels that included an indoor section (2. 1m2) and an outdoor section (5.6m2). GIl dogs were
walked outside the premises on a regular basis between 1200h and 1330h. The dogs in GIll (all
female) were maintained in pairs in kennels measuring 2.4m2. From 0800h to 1400h these dogs
resided pairwise in outdoor kennels (3.6m2). GIV individuals were maintained individually in
kennels that measured 1.7m2. From 0800h to 1400h these dogs stayed individually in outdoor
kennels that were sized 3.6m2. GIV individuals were unique in that, over the years, they had
been subjected to a number of different, sometimes stressful, experiments. The animals in Gil,
GIll and GIV were fed once a day (brand DOKO, Trouw, Purten) between 0800h and llOOh.
The privately owned GI dogs were fed at around 0800h and around 1800h. Different owners
supplied different brands of food. All animals had free access to water.
Table 1
Gender
Breed
Mean
±
SEM age
Composition of the groups and the number of animals measured.
GI GIl GIII GIV
12 <Jand 12 ~ 9 <Jand6 ~ 20 ~ 7 <Jand 6 ~
Various breeds Various breeds Beagles Beagles
5.3
±
0.8 years 7.2
±
0.6 years 3.3
±
0.5 6.2
±
0.7
years years
Behavioural recordings (no. of
animals) when dogs were:
-
undisturbed (6 observation
sessions of lOmin) 8 12 18 11
- startled by a slamming door (6
observation sessions of 5min) 8 12 18 11
- approached (6min) 8 12 18 11
Hormonal measurements:
Urinary cortisol 21 15 17 11
Urinary catecholamines 13 15 16 11
We assumed that the levels of chronic stress increased progressively from GI to GIV in
accordance with increasingly austere conditions of maintenance.
Data collection
The dogs were alternating and/or limitedly available for experimental use. As a result,
measurements were performed with variable sets of animals. The numbers of animals used for
the different types of measurements are given in Table 1. The nature and diversity of the factors
that caused animals to be unavailable for testing makes it unlikely that any sort of unintended
selection of the experimental animals biased assessment of stress.
The undisturbed behaviour which the dogs displayed inside their home kennel was recorded
on video, using a Panasonic M7 video recorder (van Hulskamp, Nieuwegein) for IOmin on 6
different days between 1430h and 1700h. After a dog had been recorded for lOmin, it was
startled by slamming the entrance door of the housing facility. The dog's response to this
Animal Welfare 2000, 9: 49-62 51
Beerda et al
stimulus was recorded for 5min. On one of the 6 days the dogs were observed in the presence
of a female researcher. Having been in sight for 1min (t
=
1), the researcher moved towards the
door of a home kennel (t
=
2min), from where she tried to establish physical contact with the
animal (t
=
3min). Next, the researcher went inside the kennel (t
=
4min), tried to attract the
subject (t
=
5min) and, [mally, retreated to the starting position (t
=
6min). The female researcher
was familiar to the dogs in that she had frequently visited their housing facilities. On such
occasions she was in sight of the animals, sometimes handled them but did not purposely pet
them.
Behaviour was analysed in terms of the frequency or duration of occurrence using the
Observer software package version 3 (Noldus Information Technology, 6702 EA Wageningen,
The Netherlands). Behavioural observations were conducted by one person according to the
following protocol:
Behaviours scored in terms of the frequency of occurrence
Autogrooming, body shaking, changes from one posture to another, changes from one state of
locomotion to another, circling, crouching, defecating, digging, drinking, eating faeces, floor
licking, intentions to change from one state of locomotion to another (scored when dogs
performed only the first motions of the normal repertoire that they performed when changing
from, for example, a standing position to a sitting position, thus maintaining the starting, in this
example standing, position), manipulating the environment, open mouth, oral behaviours, paw
lifting, sighing, stretching, urinating, vocalizing and yawning (see Beerda
et al
[1998] for
descriptions).
Behaviours scored in terms of the duration of occurrence
Nosing, panting, tail wagging, trembling, states of locomotion and postures were scored as
described previously (Beerda et aI1998). Postures were only recorded when the positioning of
a dog's ears, tail and legs could be readily assessed, ie when a dog stood or walked. Other
behaviours that we recorded in terms of their duration of occurrence were:
Ambivalent postures: a crouched body posture accompanied by a position of the tail that is
higher than the breed-specific position; or a high body posture accompanied by a position of the
tail that is below normal.
Contact: dog within a radius of approximately 30cm of the researcher.
Gnawing at the rest basket.
Latency to first contact.
Raising of the hairs on the withers.
Repetitive behaviour: motions that were repeated with minimal interruptions and that were
stereotyped in character.
Naturally voided urine samples were collected in the morning and stored, within 3h of being
voided, at -20°C until their creatinine and cortisol concentrations could be analysed. Half of each
6ml urine sample was adjusted to pH 3-4 using methanoic acid, stored at -20°C and analysed
for catecholamines.
Determinations
Urinary cortisol and creatinine concentrations were determined following the procedures
described by Rijnberk et al (1988). Inter-assay variation was 9.5 per cent. Urinary catecholamine
concentrations were measured after solid-phase extraction by HPLC followed by radiochemical
detection, as validated for the dog (Beerda et aI1996). A commercially available kit was used
for urine extraction (Pharmacia LKB, Woerden). The HPLC system consisted of a model 112
52 Animal Welfare 2000, 9: 49-62
Enduring stress in dogs
solvent delivery system (Beckmann, Mijdrecht) and a model 460 electrochemical detector
(Waters, Milford, MA). The electrochemical detector data were analysed using a model 3396
integrator (Hewlett Packard, Amsterdam).
Data processing and statistical analysis
The data were normalized by means of logarithmic transformation and analysed by an analysis
of variance (one-way ANOV A). Pairwise comparisons between groups were conducted for
those parameters that showed a significant group effect as indicated by the F-statistic.
Differences between groups were tested for significance following the Tukey method when
group sizes were equal, and by the Tukey/Kramer approach when group sizes differed (for
details on the Tukey method and Tukey/Kramer approach see Stoline [1981]).
Statistical tests on locomotor activity and postures were performed with ratios in order to
achieve mutual independence between the different states of locomotion or postures. First, a
reference state of locomotion (or posture) was selected on the basis of it being performed by all
animals, under a given test condition, with relatively small differences between groups. Next,
the remaining states of locomotion (or postures) were expressed as a ratio to the selected
reference state oflocomotion (or posture). Lying with head rested and half-low were used as the
reference state of locomotion and posture, respectively, for the conditions when dogs were
startled by a slamming door or not disturbed. For the condition involving approach by a female
researcher, standing and neutral posture were used as references.
Per test condition, only the scores on the behaviours that significantly discriminated between
any two groups are presented. However, two exceptions are made. Firstly, in the case of
significant group effects in any of the locomotor states (or postures), the scores for the reference
locomotor state (or reference posture) are also shown. Secondly, scores on the behaviours that
significantly discriminated groups during the time that the dogs were startled by a slamming
door are also presented for the undisturbed condition. Thus, the extent to which the dogs
responded to the slamming door could be assessed.
Urinary levels of cortisol and catecholamines were expressed as ratios to creatinine.
Pooled Pearson's product-moment correlations (Morrison 1976) were calculated between
urinary cortisol to creatinine ratios and behaviours that significantly discriminated between
groups. By calculating pooled correlations, group effects, which are likely to inflate the
correlations, were taken into consideration.
The effects of gender were investigated by means of setting sex as an independent variable
when running ANOVAs with data from GI, GIl and GIV (GIll included only females). The
behaviour of 12 GIl individuals (six Beagles and six dogs from different breeds) was analysed
in an ANOV A for behaviours specific to Beagles. Age effects were investigated by means of
calculating Pearson's product-moment correlations (not pooled) between age and behavioural
or hormonal parameters. Gender, breed and age effects were only tested for the parameters that
differed significantly between the groups. Results are presented as mean values
±
standard errors
of the means (SEM). The level of significance was set at P
<
0.05. Our analytical techniques
corrected error rates for multiple between-group comparisons, but not for the number of
parameters studied.
Results
Urinary cortisol and catecholamines
The urinary cortisol and catecholamine levels for each group are presented in Table 2. Urinary
cortisol to creatinine (CC) ratios were higher in GIV than in GIl or GI. CC ratios in GIll were
Animal Welfare 2000, 9: 49-62 53
Beerda et al
elevated in comparison to those in GI. Similarly, mean adrenaline to creatinine (AC) ratios
tended to decline from GIV to GI (see Table 2). Urinary noradrenaline to creatinine (NC) ratios
were significantly higher in GIII than in GI. Ratios of noradrenaline to adrenaline (NA) and
dopamine to creatinine (DC) were similar for all groups.
Table 2
Ratio
Mean
±
SEM cortisol and catecholamine levels
1
in urine voided by dogs
that were maintained under different housin2 conditions.
Group
GI GIl GIll GIV
CC
DC
NC
AC
NA
4.8 ± OS 7.4 ± 0.6b8.7 ± 0.6ab 14.4 ± 3.4a
9.4 ± 3.7 2.3 ± 0.6 8.3 ±4.0 10.4 ± 3.5
6.5 ± LIb 8.7 ± 1.4ab 20.5 ± 4.4a16.6 ± 4.8ab
1.4 ± 0.6c2.2 ± 0.6b8.5 ± 2.3a11.5 ± 4.8ab
15.8 ± 5.7 7.9 ± 2.0 3.6 ± 0.8 6.9 ± 3.7
I
Urinary levels of cortisol (CC), dopamine (DC), noradrenaline (NC) and adrenaline (AC) are expressed as
ratios to creatinine concentrations x 10-6.Noradrenaline to adrenaline ratios are indicated by NA. Differences
between lettered superscripts within a row indicate significant (P
<
0.05) differences between groups.
Unit
instances h·1
GIV
0.6 ± 0.4
3.3
±
1.6
50.9:... 12.3bc 55.2 ± 12.3c90.0 ± 9.6a92.7 ± 16.6ab
"
71.3 ± 5.1 59.9 ± 7.2 50.5 ± 4.5 49.2±5.1 % obs. time
1.6 ± 1.2b13.2 ±4.4a17.3 ± 3.3' 20.1±5.7"
4.1 ± 2.0c5.2 ± 1.7bc 19.6 ± 3.4a12.6 ± 2.6ab
"
0.9±0.6b2.2 ± 0.8a5.3 ± 0.9" 5.0 ± 1.8a
"
21.9 ± 6.0 26.3 ± 8.2 28.5 ± 5.3 48.1 ± 9.0 instances h·1
1.0 ± O.4b2.4 ± 0.6b6.8 ± 1.0" 6.3 ± LIa % obs. time
0.3 ± 0.3b0.6 ± 0.2ab 2.0 ± 0.8ab 3.5 ± 1.3ainstances h·1
64.8 ± 13.2 64.7 ± 11.3 69.9 ± 6.7 70.6 ± 8.5 % obs. time
1.5 ± 1.0" 1.4 ± 0.7ab 2.5 ± 0.9ab 0.3 ± 0.3b
"
0.9 ± 0.5b2.9 ± 0.6" 0.2±0.lb0.1 ± O.lbinstances h·
1
1.6 ± 1.5ab 0.1 ± 0.8b1.3 ± O.4a1.5 ± 0.7ab % obs. time
Ob Ob O.I±O.lb0.8 ± O.3ainstances h-
I
1.3 ± 0.7 1.8 ± 0.4 2.4 ± 0.4 2.6 ± 0.6
Differences in the undisturbed behaviour of dogs that were maintained
under different hoUSin2conditions.
Behaviour
&
score GI GIl GIll
body shaking 0.4 ± 0.3 0.4 ± 0.2 0.8 ± 0.2
circling 0 1.3 ± 0.8 1.6 ± 0.6
locomotion:
c.s.!.
I
lying head rested
sitting
standing
walking
oral behaviours
nosing
paw lifting
posture:
half-low
high
sighing
tail wagging
urinating
yawning
Table 3
Mean behavioural scores (± SEM) are expressed as frequencies or percentages of the observation time.
Differences between lettered superscripts within a row indicate significant (P
<
0.05) differences between
groups.
I
changes from one state of locomotion to another.
2
changes from one posture to another.
Behaviour
Tables 3,4 and 5 sunnnarize the dogs' behaviour as recorded under three different conditions.
Locomotor activities and levels of nosing were higher in GIV and GIII than in GIl and GI. This
turned out to be consistent for the situations in which the dogs were not disturbed, when they
were startled by the slannning of a door and when they were approached by a familiar person.
GIV individuals stood out, especially in comparison to GI individuals, in that they showed high
54 Animal Welfare 2000, 9: 49-62
Enduring stress in dogs
levels of paw lifting and urinating when they were not disturbed (Table 3), and high levels of
circling, body shaking, yawning, urinating, tail wagging and oral behaviours when they were
startled (Table 4). Also, GlV individuals rarely showed a high posture. Only in GIV did the
slamming of a door induce increases in circling, body shaking and oral behaviours. Increased
nosing occurred in GlV and in GIll. When GlV individuals were approached by a familiar
person they typically showed ambivalent postures, changed often from one posture to another
and, together with GIll individuals, were the only dogs that drank: (Table 5). GI individuals that
were approached by a familiar person showed fewer oral behaviours and more growling than
the remainder of animals. At the same time, they appeared reluctant to contact the researcher and
Unit
instances 30min·1
1.2
±
0.3'
4.9± 3.0'
GIV
GIll
0.8 ± 0.2ab
0.5 ± 0.2b
27.3 ± 5.5b29.2 ± 6.0b51.5 ± 6.]' 75.2 ± 11.0'
"
55.] ± 9.6 57.7 ± 7.5 46.0± 4.9 29.9 ± 3.8 % obs. time
6.] ± 4.5b5.6 ± 1.7b20.4±3.1' 24.2± 4.1"
1.4 ± O.4bc 2.0
±
0.6c5.2 ± 0.9ab 7.3
±
1.7'
"
6.3 ± 2.2b14.5 ± 4.7b12.3
±
3.5b48.4 ± 10.2' instances 30min·
1
1.5 ± 0.5b2.1 ± 0.6b10.6 ± 1.2' 14.8 ± 2.4' % obs. time
46.4± 14.8 ]5.2 ± 13.6 75.3 ± 6.] 67.9 ± 9.0
9.4 ± 7.]- 2.6 ± 1.8- 1.9 ± LOb 0.9 ± 0.7b
"
0.5 ± 0.2b1.7 ± 0.3- 0.2 ± O.1b0.2 ± O.1binstances 30min·
1
1.7 ± 1.1ab 0.2±0.lb2.0 ± 0.8ab 3.6 ± 1.1- % obs. time
Ob O.]±O.lb0.1 ± O.lb0.9 ± 0.3- instances 3Omin·
1
0.3 ± 0.2ab 0.3 ± 0.2b1.3 ± 0.3- 2.] ± 0.8-
Differences in the response behaviour of dogs that were maintained under
different housing conditions and disturbed by slamming a door. For notes
and legend see Table 3.
Behaviour
&
score GI GIl
body shaking 0.] ± 0.] b 0.3 ± O.2b
circling Ob 0.4 ± 0.3b
locomotion:
c.s.l.
I
lying head rested
standing
walking
oral behaviours
nosing
posture:
half-low
high
sighing
tail wagging
urinating
yawning
Table 4
s
Unit
% obs. time
instances 6min·1
instances 6min·1
% obs. time
"
instances 6min·
1
%obs. time
1.8±0.9-
6.8
±
2.2-
0.2
±
O.]ab
Ob
18.3 ± 7.4ab
GIV
16.]±3.9b28.6 ± 5.3b55.3 ± 3.9- 30.1 ± 5.4ab
29.5 ± 9.7' 11.2 ± 8.6ab Ob 1.3 ± 0.9b
27.0 ± 12.0- Ob Ob 2.1±I.4b
4.2 ± 2.0ab 26.5 ± 7.3- 6.7 ± 1.6b22.8 ± 7.6ab
32.9 ± 14.1 24.6 ± 5.7 44.9 ± 3.4 45.5 ± 10.6
2.9 ± 2.6ab 26.4 ± 8.3" 29.1 ± 3.7' 13.8±7.1b
5.9 ± 2.3b27.8 ± 5.8- 16.5±3.1- 29.1 ± 7.9'
4.1 ± 1.9b12.7 ± 2.5- 25.4 ± 2.5- 22.4 ±4.3'
26.0 ± 6.1b44.7 ± 3.8- 49.3 ± 2.6- 37.8 ± 4.7ab
23.7 ± 13.7b45.4 ± 7.6- 57.3 ± 6.0- 37.2 ± 6.3-
Differences in the response behaviour of dogs that were maintained under
different housing conditions and approached by a familiar person. For
notes and legend see Table 3.
Behaviour
&
score GI GIl GIll
ambivalent posture Ob 0.2 ± 0.2bOb
C.p.2
1.9 ± 1.2bc 1.8 ± 0.8c4.7 ± 0.8ab
drinking Ob Ob 0.6 ± 0.1"
growling 3.6 ± 2.7- Ob Ob
latency to contact 51.4 ± 11.9' 16.2 ± 6.4' 1.4 ± 0.4b
locomotion:
c.s.l.
I
lying
lying head rested
sitting
standing
standing raised
oral behaviours
nosing
contact
tail wagging
Table 5
Animal Welfare 2000, 9: 49-62
55
Beerda
etal
they showed relatively little tail wagging. In situations where the dogs were startled by a
slamming door or left alone, GIl individuals sighed relatively often and rarely wagged their tails
(Tables 3 and 4).
Correlations between urinary cortisol and behavioural or urinary catecholamine parameters
We investigated correlations of urinary cortisol levels with the remainder of parameters that are
listed in Tables 2 and 3-5. With regard to correlations between the basal urinary CC ratio and
behavioural parameters (see Table 6), we found positive correlations with changes from one
state of locomotion to another and walking when dogs were not disturbed. After being startled
by a slamming door, the CC ratios correlated with these same behaviours plus circling, tail
wagging and urinating. Basal urinary CC ratios and the behaviour of the dogs in the presence
of a female researcher were not correlated. With regard to catecholamine measures, the urinary
CC ratio was positively correlated with the basal urinary AC ratio (r
=
0.53, n
=
55,
P
<
0.001).
Table 6 Correlation coefficients between urinary CC ratios and behavioural
parameters (n
=
46 in all instances).
Pearson's correlation and significance
0.33 ns
0.53 P< 0.001
0.57 P< 0.001
0.86 P< 0.001
0.34 ns
0.38 P< 0.014
0.67 P< 0.001
(b) after disturbance by a slamming door;
changes from one state of locomotion to another
circling
tail wagging
urinating
walking
Behaviours
(a) when dogs were undisturbed;
changes from one state of locomotion to another
walking
Pooled Pearson's correlation coefficients between basal urinary CC ratios and behavioural parameters when
dogs were (a) undisturbed and (b) startled by a slamming door.
Effects of gender, breed and age
Gender effects were studied in GI, GIl and GIV (GIll consisted only of females). Male dogs
showed more ambivalent postures than females when they were approached by a familiar
person. Ambivalent postures were shown during a (mean
±
SEM) of 1.6
±
0.8 per cent and 0
±
o
per cent of the observation time by males and females, respectively. Undisturbed females
wagged their tail during 1.5
±
0.8 per cent of the observation time, which was longer than the
0.3
±
0.3 per cent of the observation time that we recorded for male dogs.
With regard to stress hormone excretion, Beagles in GIl did not differ from group members
that were of other breeds, but they did deviate in their behaviour. GIl Beagles typically showed
high levels (mean
±
SEM) of oral behaviours after they were startled by a slamming door: 25.7
±
6.6 instances 30min-
1
vs 3.3
±
2.4 instances 3Omin-
1
in GIl individuals that were not Beagles.
When not disturbed, Beagles sighed more than dogs of other breeds: 4.2
±
0.9 instances h-
I
vs
1.7
±
0.4 instances h-l.
Effects of age occurred in behavioural parameters only. In the situation that animals were not
disturbed, age correlated with sighing
(r
=
0.30, n
=
48, P
=
0.04) and urinating
(r
=
0.37, n
=
48, P
=
0.0 I). When animals were startled by a slamming door, age correlated with urinating
(r
=
0.36, n
=
48, P
=
0.01), oral behaviours
(r
=
0.42, n
=
48, P
=
0.003) and lying
(r
=
0.38, n
=
48, P
=
0.007). Finally, when dogs were approached by a familiar person, relationships existed
56
Animal Welfare 2000, 9: 49-62
Enduring stress in dogs
between age and the performance of oral behaviours
(r
=
0.34, n
=
48, P
=
0.02), drinking
(r
=
-0.32, n
=
48,
P
=
0.03), sitting
(r
=
0.41, n
=
48,
P
=
0.004) and changes from one state of
locomotion to another
(r
=
-0.43, n
=
48,
P
=
0.003).
Discussion
The present study aims to identify behavioural and hormonal parameters that measure chronic
stress in dogs and that have practical use in the assessment of poor welfare in this species. Dogs
maintained under relatively enriched (GI) or increasingly austere conditions (GIl, GIll and GIV)
for several years were assumed to experience higher levels of chronic stress, and were compared
for behavioural and hormonal parameters. The fmdings with regard to urinary cortisol indicated
that our experimental set-up was usable for the investigation of chronic stress parameters in dogs
and that, conforming to our assumptions, chronic stress levels increased progressively from
groups I to IV. There is ample evidence of increased glucocorticoid levels in acutely stressed
dogs (Clower
et a11979;
Dess
et a11983;
Palazzolo & Quadri 1987; Assia
et a11989;
Bueno
et a11989;
Gue
et a11989;
Engeland
et aI1990).
As in a number of other species (Sassenrath
1970; Craig
et a11986;
Gamallo
et a11986;
von Holst 1986; Roger
et aI1989),
it would appear
that increased glucocorticoid secretion also indicates dogs that experience enduring stress
(Beerda
et aI1999a).
This leads us to assume that elevated cortisol levels are a strong indication
of chronic stress, although normal cortisol levels do not exclude chronic stress, since
physiological adaptations and stressor-specific responses cannot be ruled out. Our present data
show that dogs which are housed under rather austere conditions for several years show elevated
CC ratios and that these values become progressively higher as living conditions worsen. The
present investigations also show that adaptation of the HPA axis in chronically stressed dogs
probably does not imply a normalization of cortisol levels. This makes cortisol levels a very
useful measure of chronic stress.
Although the present findings on urinary cortisol indicate otherwise, we may have ranked the
groups incorrectly in terms of the austerity of their housing conditions. Differences in the way
GIl and GIll individuals were housed suggested to us that the former were 'better off than the
latter, but the opposite may have been true. Dogs in GIll, but not GIl, had the permanent
companionship of aconspecific. Dogs in GIl were privileged, in comparison to those in GIll,
in that they were kept in a more spacious and enriched home kennel and they were regularly
walked outside. The latter implies regular exposure to novel stimuli, contact with conspecifics
and interactions with humans. The importance of human companionship for dogs has been
highlighted by the work of Tuber et al (1996). Based on the way GI individuals were kept, we
assumed that these dogs had the lowest chronic stress levels. It carmot be excluded that, for
reasons unknown to us, some of the dogs in GI experienced chronic stress, although these
privately owned animals lived in a social, spacious and enriched environment. In contrast, from
all the dogs that we studied, those in GIV were subjected to the highest degree of social and
spatial restriction.
An important aspect of the present study is that we measured a large number of parameters
simultaneously. This complicated the statistical analysis of the results. A correction for the
number of parameters that were measured would have practically ruled out the possibility of
significant group effects. In our opinion, this would not have reflected the actual situation.
Instead, we chose to evaluate the results less conservatively and we adopted a comparison-wise
error rate of
P
<
0.05 as the level of significance. This necessitates a critical discussion of the
results since there is a fair chance that some of the significant results were accidental. Only with
great caution may the behavioural and hormonal differences between GIII dogs and the
remainder of the animals be interpreted in terms of signs of different levels of chronic stress.
Animal Welfare 2000, 9: 49-62 57
Beerda etal
Dogs in GIII were the only ones that were kept in pairs and direct influences of a cage
companion on a dog's behaviour may have obscured the effects of chronic stress. Also, these
dogs were relatively young and were all female. We investigated, and discuss hereafter, if
differences in the dogs' age and gender biased our assessment of stress: we cannot rule out that,
at least in part, the behavioural and hormonal differences between GIll and the other groups
were caused by differences in age and gender.
Hormonal measures
In accordance with our assumption that chronic stress levels increased from GI to GIV, we
found that basal urinary CC ratios were highest in GIV and declined progressively to the lowest
values in GI. Differences between groups were significant except when GIV was compared to
GIll, or GIII to GIl. Mean basal urinary CC ratios were comparable to those reported by others.
Van Vonderen et al
(1997)
measured a mean ratio of
2.9
x
10-<i
in morning urine samples of
88
pet dogs, which is somewhat lower than the 4.8 x
10-
6
that we found for the privately owned GI
dogs. A mean basal urinary CC ratio of
9.4
x
1O-<i
has been reported for dogs that, like our GIV
dogs, were housed individually but unlike our GIV dogs were sometimes taken outside for a
walk (Jones et aI1990). This ratio suggests that at the time that Jones et ai's dogs were tested
these animals had stress levels that ranged between those experienced by our GIll dogs (a mean
ratio of
8.7
x
1O-<i)
and our GIV dogs (a mean ratio of
14.4
x
10
-6).
Increased catecholamine
levels have been found in the plasma of acutely stressed dogs (Mekhedova & Ghadirian
1979;
Engeland et a11990; Parrilla et aI1990), but there is little evidence that increased catecholamine
levels occur in the urine of chronically stressed dogs. We found that basal urinary AC ratios
were highest in GIV and declined progressively to lowest values in GI. Differences were not
significant between GIl and GIV, or between GIII and GIV. NC ratios only discriminated GIll
individuals from GI individuals, the latter having the lowest ratios.
Our fmdings indicate that chronically stressed dogs have increased catecholamine secretion
and that this is reflected in urinary adrenaline levels and, to a lesser extent, urinary noradrenaline
levels, but not in basal urinary DC or NA ratios. Hormonal measures were not significantly
affected by gender, breed or age. The impression that arises when hormonal data from GIII
(pair-wise housing) and GIV (solitary housing) are compared is that housing dogs pair-wise in
a small kennel only moderately improves the situation for the dogs.
Behavioural measures in undisturbed dogs
The behavioural scores on undisturbed dogs confirm the findings on urinary cortisol and
catecholamines, in that behavioural differences were most pronounced between GI and GIV,
with GIl and GIII resembling GI and GIV, respectively. The dogs that we assumed were
experiencing the highest level of chronic stress, namely the GIV individuals, typically showed
increased locomotor activity, nosing, paw lifting and urinating, and they rarely exhibited high
postures. Past and present data indicate that increased paw lifting in dogs may indicate both
chronic (Beerda et a11999a) and acute stress (Beerda et aI1998). Measures of activity are
difficult to interpret with regard to chronic stress. Both inactivity (Hubrecht et a11992) and
increased movement (Hetts
et al
1992)
have been connected with chronic stress induced by
social isolation. In the present experiment, the relative inactivity of dogs in GI and GIl may have
been directly related to the fact that these animals were regularly walked out. The latter factor
may also explain why GIV individuals urinated more often than dogs in the other groups.
Contrary to the dogs in GI and GIl, those in GIV were never walked outside and, perforce, they
may have acquired a reduced inhibition to urinate inside their home kennel. Like GIV
individuals, those in GIII were not walked out. However, GIII included only bitches, which
58 Animal Welfare 2000, 9: 49-62
Enduring stress in dogs
urinate less often than male dogs (Beerda et aI1999a). We found positive correlations of age
with urinating and sighing, and a negative correlation with activity. Bitches wagged their tails
more often than male dogs. These effects of age and gender did not obscure the assessment of
chronic stress behaviour.
High incidences of repetitive locomotor behaviour (Hubrecht et aI1992), manipulations of
the environment, grooming, vocalizing (Hetts et al 1992; Beerda et al 1999a), bizarre
movements (Hetts et al 1992), coprophagy and a low posture (Beerda et al 1999a), have
previously been associated with chronic housing stress, but not in the present study. Differences
in the duration of the stress period, which spanned years in the present experiment but only 3
months or 6 weeks in the studies by Hetts et al and Beerda et ai, respectively (Hubrecht et aI's
study included variable periods of restricted housing), may have been a major cause of
discrepancies between the studies. Stereotyped behaviour rarely occurred in any of the groups
that we studied. Mertens and Unshelm (1996) reported stereotyped behaviour in 10 per cent of
109 dogs which were housed individually in an animal shelter. Perhaps the housing conditions
in the present study were not so austere that they induced stereotypies. Or perhaps we did not
observe the dogs at the moments that stereotypies are typically performed. Pigs, for example,
stereotype most abundantly around feeding time (Rushen 1985). It may be that dogs develop
stereotyped behaviour under conditions of social and spatial restriction (Mertens &Unshelm
1996; Beerda et aI1999a), but that such behaviour dissipates over the years. Dynamics in
abnormal behaviour have been reported by Clark
et al
(1997), who reported increasing
incidences of abnormal behaviour over a 3 month period in young, poorly kept Beagles. The
data that are currently available do not portray clearly how abnormal behaviour in dogs develops
over time.
Behavioural measures in dogs that were startled by a slamming door or approached by a
familiar person
Dogs that were mildly stimulated reacted differently according to the austerity of their living
conditions. High levels oflocomotor activity, changes from one posture (or state oflocomotion)
to another, circling, nosing, body shaking, oral behaviours, yawning, ambivalent postures and
displacement behaviour may characterize the responses of chronically stressed dogs. Reactions
to the sound of a slamming door typically involved a high activity (locomotor activity, circling
and nosing), and the expression of behaviours that we previously associated with acute stress
(body shaking, oral behaviours and yawning [Beerda et aI1998]), when dogs were maintained
under poor conditions. It can be argued that differences in response behaviour between GI dogs
and the remainder of animals merely indicate that dogs in the different groups learned different
associations with the sound of a slamming door. If so, one would expect relatively high, and not
low, levels of activity in GI dogs since they may have associated the sound of a slamming door
with being picked up by their owner and going home. Privately owned GI individuals typically
reacted minimally to an approaching female researcher. They sometimes growled, performed
a few oral behaviours or spent a little time nosing and tail wagging, but spent much time lying
and appeared reluctant to contact the researcher. In contrast, GIll and GIV individuals showed
relatively high levels of ambivalent postures, changes from one posture (or state of locomotion)
to another or drinking. The drinking of GIll and GIV individuals during the time that they were
approached by a person may be interpreted as displacement behaviour. The performance of oral
behaviours in stimulated dogs was positively correlated with age and appeared breed (Beagle)
specific. GIV individuals were, on average, 0.9 years older than GI individuals and were all
Beagles, contrary to GI individuals. This implies that in the present experiment, during mild
Animal Welfare 2000, 9: 49-62 59
Beerda et al
stimulation, high levels of oral behaviours may have been falsely interpreted as an indication of
chronic stress.
Correlations of urinary cortisol with behavioural and urinary catecholamine parameters
In the preceding discussion we compared dogs kept in four different housing conditions, in order
to identify parameters that indicate chronic stress. Chronic stress parameters may also be
identified by a positive correlation with an established sign of chronic and acute stress, namely
high cortisol secretion. The present correlations of behavioural and hormonal parameters with
basal urinary CC ratios suggest that chronically stressed dogs have increased basal urinary AC
ratios. Also, they respond actively to mild stimulation, as indicated by positive correlations of
the CC ratio with: i) changes from one state of locomotion to another and walking when dogs
were not disturbed; and ii) changes from one state of locomotion to another, walking, circling,
tail wagging and urinating when dogs were startled by a slamming door. This implies that the
increased activity we associated with chronic stress occurred both when dogs were and were not
disturbed. We do not believe that the increased activity in dogs kept under austere conditions
was the predominant cause of increased cortisol excretion because the groups that were most
intensely exercised (GI and GIl) showed the lowest CC ratios. Also, it has been reported that
exercise programmes in Beagles do not significantly affect the levels of plasma cortisol (Hughes
& Campbell 1990).
In summary, the present results substantiate the measurement of urinary cortisol, adrenaline,
and to a lesser extent noradrenaline, as a valid and non~invasive way to detect chronic stress in
dogs. Behaviourally, chronically stressed dogs may show increased paw lifting, locomotor
activity and nosing when they are not disturbed. During mild stimulation, such dogs may be
identified by relatively high levels of arousal as indicated by increased locomotor activity,
changes from one posture (or state oflocomotion) to another, circling, nosing, body shaking,
yawning, ambivalent postures and displacement behaviour. Because stress behaviour is rather
variable and often nonspecific to stress, it is readily misinterpreted. In many situations, where
pronounced behavioural aberrations are absent, behavioural observations may be of limited use
in the assessment of chronic stress and it may only help to interpret physiological measures like
urinary cortisol and adrenaline levels. The reported indications of chronic stress were associated
with rather austere keeping conditions and the results must be applied with some caution when
a completely different source of stress is involved.
Acknowledgements
We thank students Sandra Menting and Josefien C von Frijtag Drabbe Kunzel, who helped in
performing the experiments. The technical assistance of Elpetra A P Sprang and Ank van Wees
(Department of Clinical Sciences of Companion Animals, Utrecht University) was highly
appreciated. This work was supported by funds from the Ministry of Agriculture Nature
Management and Fisheries, the Sophia Vereeniging ter Bescherming van Dieren and the Bond
tot Bescherming van Honden.
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... Some are present in a variety of mammalian species and are therefore interesting to investigate in the light of future comparative studies. For example, depending on the severity of the stressor eliciting a response, self-scratching (hereafter scratching), yawning, vacuum behavior [sensu (34)], and head/body shaking or trembling, can be associated with chronic and/or acute anxiety in both human and non-human primates (4,(35)(36)(37)(38)(39), and in other mammals, including domestic animals (40)(41)(42)(43)(44). From the physiological perspective, such behaviors appear to be linked to the hormonal cascade that underlies the stress response, mediated by cortisol and whose intensity depends on the stressor (40,(45)(46)(47). ...
... Some are present in a variety of mammalian species and are therefore interesting to investigate in the light of future comparative studies. For example, depending on the severity of the stressor eliciting a response, self-scratching (hereafter scratching), yawning, vacuum behavior [sensu (34)], and head/body shaking or trembling, can be associated with chronic and/or acute anxiety in both human and non-human primates (4,(35)(36)(37)(38)(39), and in other mammals, including domestic animals (40)(41)(42)(43)(44). From the physiological perspective, such behaviors appear to be linked to the hormonal cascade that underlies the stress response, mediated by cortisol and whose intensity depends on the stressor (40,(45)(46)(47). Scratching, in particular, is performed in response to the itch sensation mediated by cortisol (48,49) and can lead to the itch-scratch cycle (50). ...
... In particular, such studies have shown the link between the stress response mediated by glucocorticoids and scratching in mammals [dogs (89); primates (4,49,50,87)]. An analogous link has been demonstrated in pigs for stereotypic vacuum chewing (47), indirectly suggested in dogs for body shaking (40), and described in rats (45) and hypothesized in humans for yawning (46,98). Our results suggest that a similar association might be present in domestic pigs for the anxiety related behaviors considered in this study. ...
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... In order to evaluate the possible presence of anxiety-related behaviours in the players, we coded the following behavioural items: nose/ mouth self-licking, self-scratching, yawning in dogs (Beerda et al., 2000;Mariti et al., 2012;Kis et al., 2019)and vacuum chewing and snapping in horses (Waring, 2002;Scopa et al., 2018). ...
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Social play is a window on cognitive and communicative abilities of species. Inter-specific play, in particular, is a fertile venue to explore the capacity to correctly perceive and interpret signals emitted by partners. Up to now, most studies have focussed on dog-human play due to the important implications such studies have in understanding the peculiar relationship we establish with our pets. Here, we focussed on social play between dogs and horses. By using a set of specific keywords (dog, horse, play, friend) we selected 20 videos of dog-horse social play (with each session lasting >30 secs) from the open video-sharing website YouTube. We described the behavioural patterns composing each session by defining analogous and species-specific patterns shown by dogs and horses. The rates of self-handicapping and variability in playful actions did not differ between the two interacting subjects thus suggesting well-balanced playful tactics. The Relaxed Open Mouth (ROM, a widespread playful facial expression in mammals) was also similarly performed by dogs and horses. The Rapid Facial Mimicry (RFM) is an automatic, fast response in which individuals mimic others’ expressions (less than 1 sec) that seems to have a role in mood sharing during social interactions. The dogs and horses under study showed a stronger and rapid mimicry response (less than 1 s) after perceiving ROM than after perceiving an attempt to bite (a play pattern resembling ROM in its motor performance). Taken together, our results suggest that, despite the difference in size, the phylogenetic distance, and differences in the behavioural repertoire, dogs and horses are able to fine-tune their actions thus reducing the probability of misunderstanding and escalating into aggression. One of the future challenges is to explore the role of ontogenetic pathways and familiarity in shaping inter-specific communicative ability of animals that can be at the basis of a universal language of play.
... Dogs that are subjected to stressors such as social or spatial restriction are known to perform specific behaviors more often than relaxed dogs. Examples of such behaviors include yawning without other signs of drowsiness, paw lifting, body shaking without a waterlogged fur, and walking around erratically [30,31]. The performance of these behaviors has further been linked to a state of either conflict, confusion, or fear in dogs [32], which can, in turn, be used to determine if an individual dog is either physically or mentally able to cope with the situation it is currently in. ...
... Although cortisol can be found in various bodily fluids [36][37][38], one of the less invasive, yet accurate, ways in which to detect it is through a salivary swab [39,40]. Because of this reduced invasiveness, salivary cortisol has become a widely used method to determine both acute [23] and chronic stress [24,30] in dogs. It has additionally given insight into dogs' recovery process from acute stressors, as demonstrated by Beerda et al. in their study from 1998 [23]. ...
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Only a few studies have investigated the welfare of animals participating in animal-assisted interventions (AAIs). Most of these studies focus on dogs in therapeutic settings. There are, however, also dogs—service dogs—that are employed to continuously support a single human. Because the welfare of these service dogs is important for the sustainability of their role, the aim of this study was to investigate their stress response to service dog training sessions. To do this, we took repeated salivary cortisol samples from dogs who participated in a training session (n = 19). Samples were taken just after arrival at the training ground, before training, after training, and after a period of free play. Our results showed that mean cortisol levels in all samples were relatively low (between 1.55 ± 1.10 and 2.73 ± 1.47 nmol/L) compared to similar studies. Analysis further showed that samples taken before and after participation in the training’s session did not differ from one another. Mean cortisol levels in both situations were additionally lower than those upon arrival at the training site and after a period of free play. This led to the conclusion that the dogs in our study did not seem to experience training as stressful.
... This situation could be worse in kennelled dogs, particularly in those housed for longer periods of time, where they usually live under suboptimal conditions and their environment is often restricted in space and complexity and can limit the socialisation with other conspecifics and humans [21,22]. Previous studies have shown through physiological and behavioural measures that dogs experience acute stress after admission to kennels, and some suffer chronic stress when kennelled for long periods [17,23]. This in turn could alter their preferences for palatable foods. ...
... In our study, dogs were on average 5 years under these conditions, where they were: a) spatially restrained; b) socially isolated and kept for more than 20 h per day without the possibility of tactile or visual interactions with conspecifics or humans; c) limited in their feeding frequency, being fed once a day; and d) housed in a sensory deprived environment without any type of environmental enrichment. Although in the present study no indicators were used to evaluate stress or welfare, due to their kennelling managements previously described, they were considered to be at least at risk of suffering chronic stress, according to previous studies performed in kennelled dogs in similar environments [23,51,52], which could trigger anhedonia in certain individuals. ...
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Kennelled dogs are at risk of suffering chronic stress due to long-term spatial, social and feeding restrictions. Chronic stress may decrease the dogs’ capacity to feel pleasure when facing hedonic experiences, modifying their perception for palatable ingredients. However, different abilities to cope with environmental stressors could prevent the onset of anhedonia. Fourteen kennelled Beagle dogs were used to study the acceptability and preference for different dilute sucrose and monosodium glutamate (MSG) solutions. Coping style of animals was previously evaluated through a human approach test (HAT) and classified as close dogs (CD; proactive) or distant dogs (DD; reactive) according to whether or not they approached an unfamiliar human when a feeding opportunity was presented. Consumption results were analysed taking into account the sucrose/MSG concentrations, HAT (CD or DD), age, and weight of the animals. DD presented a lower intake of sucrose (p = 0.041) and MSG (p = 0.069) solutions compared with CD. However, DD exhibited a higher consumption of MSG than CD at its highest concentrations, supporting that their intake depends on solution palatability. Finally, DD did not prefer sucrose or MSG solutions over water at any dilute solution offered. Together, these results suggest that dogs that are categorized as reactive animals could diminish their ability to perceive dilute palatable solutions, reflecting depressive-like behaviours as anhedonia.
... Positive-emotional states associated with an animal's well-being are usually much more subtle, often less expressive, and often difficult to reliably assess and distinguish from negative emotional states (Boissy et al., 2007). Even though dog wellbeing and welfare 2 topics have received increased attention in recent years, most of the studies have focused on indicators of compromised dogs' welfare (e.g., Beerda et al., 2000;Rooney et al., 2007;Mariti et al., 2015) or indicators related to the improvement of dogs' already compromised welfare (Hennessy et al., 1998(Hennessy et al., , 2006Coppola et al., 2006;Bergamasco et al., 2010;Shiverdecker et al., 2013;Csoltova et al., 2017). ...
... Increased activity was shown as a sign of positive excitement in dogs when reunited with the owner after separation or when the dogs were solving a cognitive task (McGowan et al., 2014). On the other hand, this behavioral indicator is also context specific, since excitation was also documented as an indicator of moderate stress in a social setting (Beerda et al., 1998(Beerda et al., , 2000 and shelter environment (Part et al., 2014;Cozzi et al., 2016). ...
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Although there have been a growing number of studies focusing on dog welfare, the research field concerning dog positive-emotion assessment remains mostly unexplored. This paper aims to provide a state-of-the-art review and summary of the scattered and disperse research on dog positive-emotion assessment. The review notably details the current advancement in dog positive-emotion research, what approaches, measures, methods, and techniques have been implemented so far in emotion perception, processing, and response assessment. Moreover, we propose possible future research directions for short-term emotion as well as longer-term emotional states assessment in dogs. The review ends by identifying and addressing some methodological limitations and by pointing out further methodological research needs.
... This overstimulating environment can lead to high arousal levels and stress in shelter animals. The stress response is multifactorial and includes activation of the hypothalamic-pituitaryadrenal (HPA) axis and the sympathetic branch of the autonomic nervous system (ANS), with behavioural [3] and physiological changes [4] produced. Behavioural responses to stress consist of increased arousal [5,6], which in turn results in heightened sensory sensitivity and alertness, the production of corticosteroids and increased heart rate (HR) [7]. ...
... As mentioned above, shelters can be challenging places for dogs and it is important to try to mitigate stress and arousal levels to avoid chronic stress that may impact welfare [33]. Moreover, stress and high arousal levels can increase the development of undesirable behaviours [3,[34][35][36]. These reduce the likelihood of adoption [37], increase the risk of being returned to the shelter after adoption [38,39] and elevate the risk of euthanasia [2]. ...
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Animal shelters can be stressful environments and time in care may affect individual dogs in negative ways, so it is important to try to reduce stress and arousal levels to improve welfare and chance of adoption. A key element of the stress response is the activation of the autonomic nervous system (ANS), and a non-invasive tool to measure this activity is heart rate variability (HRV). Physiologically, stress and arousal result in the production of corticosteroids, increased heart rate and decreased HRV. Environmental enrichment can help to reduce arousal related behaviours in dogs and this study focused on sensory environmental enrichment using olfactory and auditory stimuli with shelter dogs. The aim was to determine if these stimuli have a physiological effect on dogs and if this could be detected through HRV. Sixty dogs were allocated to one of three stimuli groups: lavender, dog appeasing pheromone and music or a control group, and usable heart rate variability data were obtained from 34 dogs. Stimuli were applied for 3 h a day on five consecutive days, with HRV recorded for 4 h (treatment period + 1 h post-treatment) on the 5th and last day of exposure to the stimuli by a Polar® heart rate monitor attached to the dog’s chest. HRV results suggest that music activates both branches of the ANS, which may be useful to relieve both the stress and boredom in shelter environments.
... It could also be related to the higher activity levels, or physiological responses to arousal increasing body temperature [51], with the dogs panting as a cooling mechanism [78]. Control dogs also excreted more than those exposed to Music; it has been reported that dogs kept under austere conditions and presumably experiencing higher stress levels show increased excretion [75,79]. ...
... Dogs from all treatments reacted to this external stimulus, but these behaviours were exacerbated in the Control group. In Beerda et al.'s study [79], dogs in the most austere conditions reacted more actively to disturbances such as slamming doors. It is possible that some beneficial effects could be achieved in a shelter just by limiting the external stimulation that the dogs experience. ...
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Shelter environments are stressful for dogs, as they must cope with many stimuli over which they have little control. This can lead to behavioural changes, negatively affect their welfare and downgrade the human‐animal bond, affecting re-homing success. Arousal is evident in their behaviour, particularly increased activity and frequent vocalisation. Environmental enrichment plays an important role in reducing arousal behaviour, either through direct physiological effects or by masking stressful stimuli. The present study focused on sensory environmental enrichment, using olfactory and auditory stimuli under shelter conditions. Sixty dogs were allocated to one of four treatments: three types of enrichment, Lavender, Dog appeasing pheromone (DAP) and Music, and a Control group. Stimuli were applied for 3 h/d on five consecutive days. Dogs exposed to DAP lay down more, and those exposed to Music lay down more with their head down, compared to the Control. Those in the Control stood more on their hind legs with their front legs on the exit door, compared to those exposed to Music and DAP, particularly if they had only been in the shelter for a short time. They also panted and vocalised much more than dogs in the three enrichment treatments, which tended to persist during the 4 h period post treatment, and in the case of vocalisation into the subsequent night. The study suggests that all three enrichments had some positive benefits for dogs in shelters, as well as being non-invasive and easy to apply in the shelter environment.
... In the 2014 study, the reported behaviors were lip licks, yawning, paw lifting, body shake, tail wagging, and panting. In previous studies, lip licks and yawning have been associated with social conflict situations in dogs (33), and panting and tail wagging were associated with chronic stress (34). Additionally, lip licks and wet dog shake were correlated with higher cortisol concentrations during therapy dog visits (12). ...
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Therapy dogs provide health benefits for individuals who suffer from illnesses, such as dementia, depression, loneliness, and aggression. Therapy dogs' impact on human health has been thoroughly studied; however, studies on dog welfare have been limited. Additionally, as dogs have evolved with humans, they have learned to read non-verbal social cues. Dogs can read humans' non-verbal body language and can react to their emotions. However, the body language of dogs is poorly understood and can lead to dog owner-directed aggression. Communication plays a vital role to be a cohesive therapy team. The purpose of this study was to assess perceived stress and cortisol concentrations in therapy dogs and their handlers during the first three visits in a hospital setting. Moreover, the study aimed to investigate whether, while in an overstimulating environment, a therapy dog handler can observe his or her dog's body language and correlate such observations to the dog's stress. Nine therapy dog teams from Mayo Clinic's Caring Canine Program participated in this study. A baseline salivary cortisol was collected from the handler and therapy dog each day of the visits. Once the team arrived, a pre-visit salivary cortisol was collected from the handler and therapy dog and, afterward, a post-visit salivary cortisol. Handlers were also asked to fill out a perceived stress survey on their own stress and that of their therapy dogs'. Behavior was documented by a staff member and the handler. For each visit, the therapy dogs were at the hospital on average 47 min and visited with nine people. There was significant correlation (P = 0.02) between the owner's perceived stress of his or her therapy dog and the dog's salivary cortisol concentrations. The handlers noted medium to high stress, and those dogs had higher cortisol concentrations post-visit. There was no significant difference in salivary cortisol for the handler and therapy dog over the course of the three visits and comparing pre-and post-visit. Overall, the dogs displayed mixed behaviors, with the three most reported being panting, lip licking, and yawning. However, salivary cortisol results suggest that the handlers and therapy dogs maintained their welfare state throughout the visits.
... The decrement in lying time reported here is supported by the study of Kiddie et al. (2017) who reported that treatment with coconuts, cardboard bed or cardboard partition decreased yawning frequencies, lying and sitting down time without difference between them, which could indicate the active engagement of dogs with the enrichment objects, so support the hypothesis stating that the used objects were enriching. The grooming frequency decrease through the enrichment phase may be attributed to this behavior association with chronic stress in dogs and so it increases postenrichment (Beerda et al., 2000) as a displacement activity in contexts of conflict (Hennessy et al., 2006). Previous studies on ACTH-induced behavioral syndromes, suggested, inclusion of displacement behaviors as grooming and yawning (Bertolini, etal.,1998). ...
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Key words: behavior, feeding enrichment, cortisol, dog, welfare, kennel Environmental enrichment used in captive animals with goals of increasing the activity, behavioral diversity, utilization of the environment and reducing abnormal behaviors. The present study was designed to determine the springing feeding bottles toy ameliorative effect on behaviors and cortisol level of kenneled Caucasian dogs. Sixteen healthy kenneled Caucasian shepherd dogs were utilized under four phases: 1) habituation period, 2) baseline period (pre-enrichment phase), 3) treatment period (enrichment phase)-and 4) post-exposure period (post-enrichment phase). Each phase last for 3 days during which dogs were video recorded for state and event behaviors except the first one. Hair was collected during the three phases (pre, during and post enrichment) for cortisol analysis. The provision of the feeding enrichment shorter the lying time and stereotypies frequencies, while increased the activity level. These behaviors persisted after withdrawal of enrichment with improvement in feeding time. Hair cortisol levels also was lower during and after enrichment with a marked reduction after withdrawal. Therefore, it appears that the provision of feeding enrichment toy could improve the behavioral repertoire and decrease cortisol level in kennelled dogs, and thus enhance its welfare.
... Direct behavioral assessment through scales or measurement of defined behaviors has been proven to be a reliable marker of stress in dogs. Behavior that is associated with stress includes low posture, vocalization, mouth opening, oral behaviors, shaking, and others (Beerda et al., 1997(Beerda et al., , 1998(Beerda et al., , 2000. ...
Article
Visiting veterinary clinics has been demonstrated to be a stressful experience for the majority of dogs and is a common reason that owners delay treatment for their pets. The use of dexmedetomidine oromucosal gel has been shown to reduce stress during minor procedures at the veterinary clinic as well as alleviate acute anxiety and fear associated with noise in dogs. The objective of this study was to assess the efficacy of dexmedetomidine oromucosal gel in alleviating acute stress during standardized veterinary visits for physical examinations when administered by owners in the hospital. This study was a randomized, crossover, double-blinded, placebo–controlled trial. Forty client-owned healthy dogs with a history of anxiety and/or fear during veterinary visits presented for two visits and were randomized into two treatment groups. One treatment group received placebo at the first visit then dexmedetomidine oromucosal gel at the second visit and the other group received it in the reverse order. We video-recorded the dogs’ behavior during the duration of the physical examination and the video was analyzed by a blinded investigator, using an ethogram with predetermined stress-related behaviors. Mixed effect logistic regression was used to study the effect of dexmedetomidine oromucosal gel on the behavior categories during the physical examination. Age, sex, weight, noise level, and sedation scores were considered confounding factors. The random-effects were set on the level of the individual animal. Statistical significance was assumed for a value of p<0.05. Results showed that dexmedetomidine oromucosal gel significantly decreased the likelihood of dogs exhibiting the behavior categories of Stress/Fear Vocalization (whining, yelping, grumbling) (p<0.01), Avoidance Behaviors (oriented towards the door, attempting to exit the room, trying to jump from the table) (p<0.01), and Other Stress-related Activities (panting, trembling, urinating, defecating) (p=0.016) during the physical examination. Stress/Fear Vocalization occurred less frequently during the second visit compared to the first visit and was more likely to occur in dogs that were young and male. Dexmedetomidine oromucosal gel reduces signs of stress (vocalizations, avoidance behaviors, panting, trembling, urination, defecation) in dogs during veterinary examinations. By decreasing stress in dogs during physical examinations, we can diagnose more accurately and improve welfare for our patients.
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The dog (Canis familiaris) has been domesticated for thousands of years but the effects of different housing regimens on canine behaviour are poorly understood. This study presents behavioural data collected from solitary and group-housed dogs housed in animal shelters and laboratories. The dogs differed greatly in their behaviour under the different housing regimens. Solitary dogs were more inactive (72-85% of observed time compared with group-housed dogs 54-62% of observed time), and spent more time in non-social repetitive locomotory behaviour categories (4-5% compared with group-housed 0.9-2% of observed time). Group-housed dogs were not only able to interact socially, but also spent more time investigating the floor of their pens, presumably because of the increased olfactory stimuli. Group-housed laboratory dogs provided with kennels used them for: rest, play and the control of social interactions. Single-housed dogs, which were housed in smaller pens, had low overall activity and tended towards stereotyped circling rather than pacing. At all the sites the opportunities for interactions with humans were limited (0.24-2.52% of the time observed). The results are discussed in terms of cage design and animal husbandry.
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Six weeks of social and spatial restriction were used as a model to induce chronic stress in Beagles. Behavioral and physiological measurements were performed during a period of enriched spacious outdoor housing in groups (GH) and during a subsequent period of solitary housing in small indoor kennels (IH). Behavioral parameters that may indicate chronic stress in dogs are reported. During IH, the dogs showed significantly (comparison-wise error rate <0.05) lower postures than during GH. IH induced enduring increments in frequencies of autogrooming, paw lifting, and vocalizing, and was associated with incidents of coprophagy and repetitive behavior. So far, we interpret the behavioral changes as signs of chronic stress. Relatively low levels of walking, digging, intentions to change from one state of locomotion to another, and increments in circling are conceived as obvious adaptations to the specific features of the IH system. By challenging the dogs outside their home kennel we tested whether the dogs’ coping abilities were affected by IH. Dogs that were challenged were introduced into a novel environment, given the opportunity to escape from their home kennel, restrained, walked down an unfamiliar corridor, presented a novel object, exposed to loud noise, given food, or confronted with a conspecific. During IH, challenged dogs exhibited higher postures, showed more tail wagging, nosing, circling, urinating, and defecating, and changed more often from one state of locomotion (or posture) to another than during GH. These behavioral changes were observed across the different types of challenges, with the exception of the noise administration test. In the presence of conspecifics, the socially and spatially restricted male dogs behaved more dominantly and aggressive than during the time that they were kept in groups. Such behavior manifested as increased performances of raised hairs, growling, paw laying, and standing over. Both sexes showed increases in paw lifting, body shaking, ambivalent postures, intentions to change from one state of locomotion to another, and trembling in any of the challenges, excluding the walking down the corridor test. In short, during a variety of challenges, socially and spatially restricted dogs exhibited a heightened state of aggression, excitement, and uncertainty. Behavioral differences between dogs that had experienced pleasant and bad weather conditions during GH, suggested that “pleasant-weather individuals” had experienced early stress during the control period, and, as a result, responded to the subsequent period of IH differently. Regardless of the housing conditions, challenged bitches showed stronger indications of acute stress than male dogs. Gender did not affect the chronic stress responses to social and spatial restriction. A low posture and increased autogrooming, paw lifting, vocalizing, repetitive behavior, and coprophagy may indicate chronic stress in dogs, and as such, can help to identify poor welfare. When challenged, chronically stressed dogs may show increased excitement, aggression, and uncertainty, but the nonspecificity of such emotional behavior will complicate its practical use with regard to the assessment of stress.
Article
Thirty tethered sows were observed for 5 min every half-hour for 9 h spanning the two feeding periods. Activity, consisting largely of food searching behaviour and drinking, was largely restricted to two 2-h periods following each feed. Three categories of stereotyped behaviour were observed and these were closely tied to the feeding periods. Short-duration bouts of rubbing, head-waving and bar-biting occurred during food delivery, while long-duration bouts of highly stereotyped and idiosyncratic sequences of rubbing and drinking were shown by older sows immediately after feeding. Vaccuum chewing tended to occur slightly later. I suggest that frustration of feeding motivation rather than under-stimulation underlies stereotypies in pigs, and that the different forms may represent stereotype of the appetitive and consummatory phases. Aggression was rare and was not closely related to the feeding periods or to stereotypies.
Article
The effects of different spatial areas and different social conditions on behaviours of beagles maintained in a laboratory were evaluated. Eighteen female purpose-bred beagles were divided into six groups of three, and housed individually for 3 months each in six different housing conditions: (A) a 6.1 m × 9.1 m outdoor pen; (B) a 1.8 m × 6.1 m outdoor run; (C) a 1.2 m × 3.66 m indoor run; (D) a 0.9 m × 1.2 m × 0.84 m cage; (E) a 0.9 m × 1.2 m × 0.84 m cage with 30 min of forced treadmill exercise, 5 days week-1; (F) a 0.71 m × 0.86 m × 0.69 m cage. Behaviours of six dogs housed in pairs in Conditions A and C were also compared. Behaviours studied were movement, vocalisation, lying down, sleep, object manipulation, barrier manipulation, barrier jumping, fence running, agonistic and affiliative activities, and proximity. Behavioural effects were compared among housing conditions, order of rotation through each housing condition, and behavioural changes over time during each 3 month rotation. Dogs spent more time moving in pens and runs than in cages. Dogs housed in the greatest degree of social isolation spent the most time moving, exhibited the greatest number of bizarre movements, and vocalised the most. Dogs housed in the smallest cages spent more time grooming and in manipulation of enclosure barriers than those housed in any other conditions. Forced treadmill exercise did not significantly alter behaviours. When housed in pairs, dogs spent more time sleeping and showed a tendency to spend less time vocalising than when housed singly. The results indicate that spatial area and activity are not likely to be the most important factors to be considered when evaluating psychosocial well-being of dogs. In assessing the psychosocial well-being of dogs, social isolation may be as harmful or more harmful than spatial restriction.
Article
To emphasize the effects of group- and single housing of kennelled dogs, the behavior of 211 dogs in two German animal shelters was tested and observed. After being placed, 197 of the dogs' new owners were interviewed. Although 51% of the German animal shelters already keep dogs in groups, there is strong prejudice against group housing because of the fear of fights. This study demonstrates that this apprehension is unfounded. Ninety-one percent of the social confrontations between dogs housed together were settled by the use of behavioral rituals. Keeping dogs in groups, furthermore, leads to a significant reduction in noise emission (p<.001). Group housing fulfills the dog's need for social interaction and the need to move. Dogs that were housed in groups displayed a closer human-animal relationship (80%) than those that had been kept individually (43%). A high percentage of individually housed dogs suffered from behavioral problems (31%) and 10% developed stereotypes. The percentage of behaviorally disturbed dogs observed in group housing was 11%, and stereotyped forms of behavior did not occur. Dogs who had been kept in groups were, on average, placed within 10 days, and were returned to the animal shelter less often (9%) compared to those housed individually (25%). Dogs that were housed separately needed an average of 17 days to be placed. Even after being placed, there is a correlation between the animal shelter's type of housing and the dog's behavior. Within four weeks after picking up their pet, 88% of the owners of dogs that had been housed individually complained of problems compared to the owners of the dogs that had been kept in groups, 53% of whom were completely satisfied with the adoption. Despite the fact that these results might be influenced by the small number of shelters examined, the study leads to the conclusion that keeping dogs in groups is a suitable alternative for dog housing in animal shelters and, for the animals' welfare, is preferable to individual housing.
Article
Two mixed-sex groups of subadult M. mulatta, maintained under chronic crowding stress, were characterized re adrenal responsiveness to ACTH (via urinary 17-hydroxycorticosteroids) and intragroup social behavior over a 2-year period which included a series of changes in social environment.Under conditions of unchanging dominance structure, ACTH-response levels of individual cagemates remained relatively constant, with 3- to 10-fold differences between the lowest (dominant male) and the highest (most subordinate female cagemate). Elevated response levels of subordinate cagemates were lowered by changes which reduced social stress, such as transfer to individual caging, removal of the dominant male, or consort pair formation involving the dominant male. Conversely, removal of the most subordinate cagemate resulted in elevation of ACTH-response levels of some remaining subordinates. Covariance was demonstrated between ACTH-response levels, aggressive stimulation received, and fear-anxiety behavior for two female subordinate cagemates.The data suggest that the prime determinant of ACTH-response levels is the fear- or anxiety-evoking aspects of group interaction. Elevated adrenal responsiveness is assumed to be a function of chronically elevated ACTH output reflecting the characteristic level of fear-evoking or “stressful” stimulation sustained by each member of the social group.
The physiologic contribution of the limbic brain to emotionally induced stress is still poorly understood. The present study is designed to more specifically evaluate the role of the hippocampus in stress induced plasma 17-OHCS elevations. The conditional reflex to a sequential presentation of tone and shock was used as the stress agent in adult mongrel dogs. Plasma 17-OHCS levels were determined by the Porter-Silber method. Control and stress levels of 17-OHCS were determined before and after unilateral (left) hippocampectomy, and subsequent contralateral (right) hippocampectomy. A unilateral posterior hippocampal lesion partially attenuated (20%) the normal 17-OHCS stress response. In contrast to unilateral lesions, equivalent bilateral posterior hippocampal lesions abolished the normal 17-OHCS stress response. These observations support the thesis that the elevated 17-OHCS levels in response to the conditioning paradigm is dependent on the hippocampus. Furthermore, it is dependent upon the continuity of the hippocampal circuit and not upon the volumetric steroid binding capacity of the hippocampus. These studies also suggest that a unilaterally functioning hippocampus may be adequate to meet the physiologic needs of stress, as reflected by the 17-OHCS response. Presented at the 1978 meeting of the Pavlovian Society, St. Petersburg, Florida.
Article
In this study, we used spectral analysis of short-term R-R and systolic arterial pressure (SAP) variabilities to estimate the changes in neural control of the circulation produced by psychological stress. The 0.1 Hz low-frequency (LF) component of R-R and SAP variabilities provided a quantitative index of the sympathetic activity controlling heart rate and vasomotion. Conversely the high-frequency (HF) respiratory component of R-R variability provided an index of vagal tone. In conscious dogs we used the seemingly stressful situation of being accompanied for the first time to the experimental laboratory as a stimulus. In human subjects we used mental arithmetic. In both cases LF of R-R and SAP variabilities increased significantly suggesting enhanced sympathetic activity both to the SA node and the vasculature. In man, the index α, a measure of the overall gain of baroreceptor mechanisms, was found to be reduced during mental arithmetic. Spectral analysis of cardiovascular variabilities thus suggests that in man and in conscious dogs psychological challenges induce a profound re-arrangement of neural control of the circulation, which appears to be characterised by sympathetic predominance and which can be monitored by this technique.
Article
Stress parameters that can be measured noninvasively may help to identify poor welfare in dogs that live in private homes and institutions. Behavioural parameters are potentially useful to identify stress, but require further investigation to establish which behaviours are appropriate. In the present study, behaviours were recorded and analysed for signs of acute stress in dogs. Simultaneously, saliva cortisol and heart rate were measured to support the interpretation of the behavioural data with regard to stress. Ten dogs of either sex, different ages and various breeds were each subjected to six different stimuli: sound blasts, short electric shocks, a falling bag, an opening umbrella and two forms of restraint. Each type of stimulus had been selected for its assumed aversive properties and was administered intermittently for 1 min. The stimuli that could not be anticipated by the dogs, sound blasts, shocks and a falling bag, tended to induce saliva cortisol responses and a very low posture. The remainder of the stimuli, which were administered by the experimenter visibly to the dog, did not change the cortisol levels but did induce restlessness, a moderate lowering of the posture, body shaking, oral behaviours, and to a lesser extent, yawning and open mouth. Pronounced increases in the heart rate were nonspecifically induced by each type of stimulus. Heart rate levels normalized within 8 min after stressor administration had stopped. Saliva cortisol levels decreased to normal within the hour. Correlations between behavioural and physiological stress parameters were not significant. From the present results, we conclude that in dogs a very low posture may indicate intense acute stress since dogs show a very low posture concomitant with saliva cortisol responses. Dogs may typically show increased restlessness, oral behaviours, yawning, open mouth and a moderate lowering of the posture when they experienced moderate stress in a social setting. The nonspecific character of canine heart rate responses complicates its interpretation with regard to acute stress.