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Article
Could Greater Time Spent Displaying Waking
Inactivity in the Home Environment Be a Marker for
a Depression-Like State in the Domestic Dog?
Naomi D. Harvey 1, * , Alexandra Moesta 2,†, Sarah Kappel 3, Chanakarn Wongsaengchan 1,3,
Hannah Harris 1,3, Peter J. Craigon 1,3 and Carole Fureix 3
1School of Veterinary Medicine and Science, University of Nottingham, Sutton Bonington LE12 5RD, UK
2Royal Canin Research Center, 30470 Aimargues, France
3School of Biological and Marine Sciences, University of Plymouth, Plymouth PL4 8AA, UK
*Correspondence: Naomi.Harvey@nottingham.ac.uk
†Former address: WALTHAM Centre for Pet Nutrition, Waltham-on-the-Wolds,
Melton Mowbray LE14 4 RT, UK.
Received: 30 May 2019; Accepted: 2 July 2019; Published: 5 July 2019
Simple Summary:
Stressed pet dogs, such as when deprived of their owners or after the loss of a
social companion, can become inactive and unresponsive. Dogs in this condition are commonly
referred to as being “depressed”, but this remains an untested hypothesis. One hallmark of human
clinical depression is anhedonia—a reduction in the experience of pleasure. Here we tested the
hypothesis that shelter dogs that spend greater time inactive “awake but motionless” (ABM) in
their home-pen would also show signs of anhedonia, as tested by reduced responses to a treat filled
Kong
TM
. We also explored whether dogs being rated by experts as disinterested in the Kong
TM
would
spend greater time ABM (experts did not know the dogs’ actual inactivity levels). Fifty-seven dogs
from 7 shelters were tested in total. Dogs relinquished by their owners spent more time ABM than
strays or legal cases, and one association was found between the ABM and the dogs’ response to the
filled Kong
TM
, which was in the opposite direction that expected, so does not support the hypothesis
that waking inactivity indicates a depression-like state in dogs. Dogs rated by experts as “depressed”
and “bored” when exposed to the Kong
TM
, however, spent greater time ABM; we discuss whether
ABM could tentatively indicate “boredom” in dogs.
Abstract:
Dogs exposed to aversive events can become inactive and unresponsive and are commonly
referred to as being “depressed”, but this association remains to be tested. We investigated whether
shelter dogs spending greater time inactive “awake but motionless” (ABM) in their home-pen show
anhedonia (the core reduction of pleasure reported in depression), as tested by reduced interest in,
and consumption of, palatable food (Kong
TM
test). We also explored whether dogs being qualitatively
perceived by experts as disinterested in the food would spend greater time ABM (experts blind to
actual inactivity levels). Following sample size estimations and qualitative behaviour analysis (n=14
pilot dogs), forty-three dogs (6 shelters, 22F:21M) were included in the main study. Dogs relinquished
by their owners spent more time ABM than strays or legal cases (F =8.09, p=0.032). One significant
positive association was found between the Kong
TM
measure for average length of Kong
TM
bout
and ABM, when length of stay in the shelter was accounted for as a confounder (F =3.66, p=0.035).
Time spent ABM also correlated with scores for “depressed” and “bored” in the qualitative results,
indirectly suggesting that experts associate greater waking inactivity with negative emotional states.
The hypothesis that ABM reflects a depression-like syndrome is not supported; we discuss how
results might tentatively support a “boredom-like” state and further research directions.
Keywords:
kennelled dog; depression-like state; waking inactivity; anhedonia; affective-state;
qualitative behaviour assessment
Animals 2019,9, 420; doi:10.3390/ani9070420 www.mdpi.com/journal/animals
Animals 2019,9, 420 2 of 19
1. Introduction
Pet dogs exposed to aversive events, such as when deprived of their owners or after the loss of
a social companion, can become profoundly inactive and unresponsive [
1
], as can laboratory dogs
that “give up” and develop “helplessness” (lack of reaction) in response to inescapable stressors [
2
,
3
].
Increased inactivity in dogs is also commonly referred to as indicating that a dog is “depressed” or
showing signs of “depressive-like behaviour”, both in the public domain [
4
,
5
] and peer reviewed
literature [
6
–
9
]. However, since the seminal demonstration of “helplessness” in dogs by Seligman
and colleagues [
2
,
3
], no empirical evidence has been collected to date specifically to investigate the
possibility that dogs could display other depression-like symptoms.
In humans, clinical depression (by which we mean major depressive disorder or depressive episodes
to encompass, respectively, Diagnostic and Statistical Manual of Mental Disorders 5 (DSM-V) [
10
]
and International Statistical Classification of Diseases and Related Health Problems (ICD-10) [
11
]
terminologies) is a debilitating mental illness that is commonly triggered by chronic stress, especially
in individuals with a predisposition to developing the condition due to innate genetics or aversive
early life experiences [
10
,
12
–
15
]. Various cognitive changes are hypothesised to be involved in both
its aetiology and maintenance [
16
–
19
]. One such cognitive change is pessimistic judgements bias,
where individuals experiencing a low mood make more negative judgements about ambiguous
situations [
17
,
18
]. A second is “learned helplessness”, where an individual comes to believe that
desired outcomes are improbable and aversive outcomes likely, that no action on the part of the
individual can alter this, and as such stop acting [2,16].
Diagnosis of clinical depression is based on the co-occurrence of a suite of cognitive, affective and
behavioural clinical signs, present for several weeks, and interfering with abilities to cope with everyday
life. Such signs include a persistent low, sad mood, anhedonia (a reduction in pleasure), changes in sleep
and appetite patterns, difficulty in concentrating and taking decision, and fatigue [
10
,
11
]. Importantly,
clinically depressed patients often show increased inactivity [
10
,
17
] that can take many forms, including
not partaking in activities they once enjoyed, or not doing chores that need to be done [
18
], reduced
physical activity [19,20], and difficulty taking part in or initiating social activities [10,17,21].
Whether inactive dogs, or at least those displaying certain forms of inactivity in certain contexts,
are in depression-like states remains an untested, and yet plausible hypothesis. Most of the properties
described in clinically depressed patients might indeed not be unique to humans [
22
–
24
], and
biomedical scientists have been modelling some of the illness symptoms in non-human animals for
decades [
14
,
25
–
27
]. Because the aetiology of human depression emphasizes aversive life events and
chronic stress as common triggers [
10
,
12
–
15
], increased inactivity in dogs, in tandem with chronic
stress or traumatic events, could potentially be indicative of a depression-like condition. Moreover,
learned helplessness, one of the cognitive features of clinical depression described above, has also been
shown in dogs, and is a phenomenon typically accompanied by an overall decrease in activity [
28
].
Again, because the aetiology corresponds to cognitive theories of human depression [
16
,
29
,
30
], this
inactivity is believed to be a depression-like behaviour. Furthermore, specific forms of waking inactivity
displayed in the home environment in other mammalian species have been shown to be associated
with key diagnostic features of human depression—anhedonia in riding horses [
23
] and “helpless”
responses in laboratory mice [31].
Do the above-mentioned studies demonstrate that greater level of waking inactivity in the home
environment reflect a depression-like state in the domestic dog? They do not provide sufficient
evidence. However, altogether they make testing this hypothesis very worthwhile, considering the
negative implications that depression-like states would have for dogs. Providing empirical evidence
for the existence of such a condition in domestic dogs would be the first step towards developing
evidence-based treatments for these animals, and to put these behavioural problems into focus as a
legitimate aspect of clinical animal behaviour. Such an understanding of the behaviour of companion
animals could lead to improvements in their welfare and management, and potentially even improve
the quality of the dog-human relationship for individuals whose behaviour may have gone otherwise
Animals 2019,9, 420 3 of 19
unrecognised and misunderstood. Moreover, if shown that dogs can be in a state analogous to
human depression (and methods of identifying such a state can be validated), this could help to
bring behavioural endpoints for animal research of affected dogs. Besides, whilst animals in naturally
occurring depression-like states may represent improved models of human depression, it could
potentially invalidate other research where stress and depression are not of interest [
32
,
33
]. Using dogs
in depression-like states would, therefore, invalidate the results of research projects, implying wastage
of animals and violation of the 3Rs’ Reduction [34].
Kennelled dogs, such as those housed in research facilities or rescue shelters, are exposed to an
array of chronic stressors including minimal exercise, lack of positive social interactions, disrupted
routines, high noise levels and a lack of control over their environment [
2
,
35
]. For shelter dogs in
particular, such situations could be exacerbated by the abrupt loss of their previous owners, with
whom they may have formed strong attachments [
1
]. There is ample evidence that kennelling can have
negative impacts on dogs welfare, however there are currently a lack of methods for measuring their
emotional welfare [
36
]. Because of the chronic stressors and potential traumatic events dogs in rescue
shelters are exposed to, we propose that shelter dogs are a suitable model for testing the hypothesis that
greater time spent displaying waking inactivity could reflect a depression-like condition in kennelled
domestic dogs.
We tested this hypothesis by investigating the association between greater time spent inactive
“awake but motionless” in the home-pen and a core symptom of human clinical depression—anhedonia.
Anhedonia has been successfully modelled in biomedical studies in rodents, primarily via inducing and
recording reductions in sucrose intake [
37
]. Evidence that sucrose ingestion is pleasure-driven includes
that rodents will eat sugar even when fully sated [
38
] and that it involves the same opioid-mediated
reward pathways as sexual behaviour and some recreational drugs [
38
]. Furthermore, reduced
sucrose intake by rodents is induced by chronic stressors [
37
], alleviated by anti-depressant drugs [
26
],
and co-varies with other depression-like features, including learned helplessness [
39
] and negative
judgement biases [
40
]. Dogs are equipped with sweet receptors [
41
], directly translating the paradigm
commonly used in laboratory rodents (i.e., comparing the amount of diluted sucrose solution vs. pure
water consumed), however appeared practically challenging in rescue shelters. It requires a long
exposure (usually several hours) to the solutions, as well as an adequate delivery mechanism—some
liquid might be “wasted” if the dog paws at a drinking bowl (biasing measurement of liquids
consumed)—and pure sucrose intake might be perceived as an unhealthy diet by shelter staffwhich
might reduce willingness to participate in the study. Therefore, we chose to assess interest for, and
consumption of, palatable solid “treat” foods commonly used as dog training aids (i.e., that dogs are
motivated to work to get access to) as a proxy for anhedonia. We predicted that dogs that spend greater
time awake but motionless in their home-pen would also show a reduced interest in, or consumption
of, the palatable treat food.
As mentioned at the start of this introduction, greater level of waking inactivity in dogs is
commonly referred to in the public domain and professionals working with dogs as indicating the
dog being “depressed”, although to date there is no empirical evidence supporting this interpretation.
Our second aim was, therefore, to explore, using qualitative behavioural assessment (QBA) methods,
whether dogs being perceived by a group of experts as apparently disinterested during the food test
would also spend greater time awake but motionless in their home-pen (the experts being blind to the
dogs’ actual home-pen inactivity levels).
2. Materials and Methods
The study complied with the European Communities Council Directive of 24 November 1986
(86/609/EEC) and was approved by the University of Bristol Animal Welfare Ethical Review Board in
January 2016 (UB/15/072). Permission to approach RSPCA (Royal Society for the Prevention of Cruelty
to Animals) shelters was obtained from the Head of Companion Animals Department, the Chief
Animals 2019,9, 420 4 of 19
Veterinary Officer and the Chief Scientific Officer in July 2016. Dog husbandry and care were under
the management of the shelter staff.
2.1. Subjects
This study was conducted in two parts: a pilot phase, where preliminary data were collected,
analysed and used to conduct a sample size estimation (see Supplementary Material Pilot Study
section) as well as qualitative behavioural analysis (QBA) and a full study on an independent sample
to meet the sample size requirement. The inclusion criteria for selecting dogs that could participate
in both parts of this study were four-fold. First, dogs must not have an existing health condition
(as diagnosed by a qualified veterinarian based on physical examination). Second, dogs must be aged
between 12 months and 10 years of age. Third, dogs must not be on a reduced calorie diet (which
could invalidate anhedonia food consumption testing through confounding impacts upon motivation
to eat). Fourth, dogs must have been housed in the shelter for a minimum of 1 week at the time of
video observation (behaviour of shelter dogs has been shown to become repeatable or stable after
1 week in the shelter [42]).
We recruited a total of seven shelters in the United Kingdom (either RSPCA or private shelters),
in which observations were carried from March 2016 to December 2017 (shelter 1: March, June,
September 2016 and January 2017; shelter 2: August 2016; shelter 3: October 2016, February 2017;
shelter 4: February 2017; shelter 5: October 2017; shelter 6: November 2017; shelter 7: December 2017).
Ninety dogs originally met the inclusion criteria, of which 33 had to be excluded from analyses due
to being rehomed, developing health problems over the course of the study, or due to recording
equipment failures. In all shelters, the dogs were individually housed in two-compartment kennels,
entirely cleaned once a day. All dogs were fed twice a day (approximately 08:30 and 16:00–17:00), but
two animals were fed an extra meal around lunchtime. Water was provided ad libitum. In all shelters,
the dogs were provided daily with a Kong
TM
either around lunch time or around 16:30–17:00 as part
of their normal management routine. In all shelters, all dogs were walked twice a day (once for 10 and
once for 20 min) by shelter staffor volunteers.
2.1.1. Quantitative Analyses Subject Demographics (N =43)
Complete datasets were successfully collected for 43 dogs in the full study (22 female, 21 male),
from across six shelters (shelter 1: 8 dogs; shelter 3: 7 dogs; shelter 4: 5 dogs; shelter 5: 10 dogs; shelter
6: 9 dogs; shelter 7: 4 dogs; see Table 1). Fifty-eight percent (25 dogs) of these were neutered, and
44% (19 dogs) were classified according to the American Kennel Club groupings as being from a
working/herding/sporting breed; this binary classification allowed us to include crossbred dogs in the
analysis; where parent breeds were stated they were assigned a 1 or 0 accordingly, or when no breed
was stated (mixed) dogs were assigned a 0 as they could not be classified into this breed group. In total,
49% (21 dogs) were voluntarily relinquished, 16% (7 dogs) were found as strays, and 33% (14 dogs)
were seized as part of legal cases (plus one dog missing origin data). The mean age of the dogs was
4.01 years (SD
±
2.17), with the youngest being 1 year and the oldest being 10 years of age. Excluding
an outlying long-stay dog who had spent 210 weeks in the shelter, the mean number of weeks spent in
the shelter was 8.1 (SD
±
8.0), with the minimum number being 1.4 weeks and the maximum being
45.4 weeks.
2.1.2. Qualitative Behaviour Analyses (QBA) Subject Demographics (N =14)
A total of 14 dogs (7F: 7M) from three shelters, recruited during the pilot study, were utilised here
(shelter 1: 7 dogs; shelter 2: 2 dogs; shelter 3: 5 dogs) (see Table 1). QBA analyses were performed on the
dogs from the pilot sample, as the complete datasets from the 43 other dogs described above were
not available at the time we could organise the QBA assessment. Dogs were aged 1–9 years (average
3.02
±
2.26 years), and 43% (6 dogs) were classified according to the American Kennel Club groupings
as being from a working/herding/sporting breed. In total, 36% (5 dogs) were voluntarily relinquished,
Animals 2019,9, 420 5 of 19
21% (3 dogs) were found as strays, and 29% (4 dogs) were seized as part of legal cases (plus two dogs
with missing origin data). The mean number of weeks spent in the shelter was 8.4 weeks (SD
±
7.7),
from 3.4 weeks to 15.6 weeks.
Table 1.
Individual characteristics of the 14 pilot study dogs included in the qualitative behaviour
analysis (QBA) and the 43 dogs from the main study for which complete data sets were obtained.
ID Shelter Sex Intact Age (years) Breed W/H/S breed Origin Study
10 1 M MD 1 Labrador cross Yes Rel. QBA
12 1 F MD 1 Husky Yes Rel. QBA
14 1 F MD 2 German shepherd Yes Rel. QBA
15 1 M MD 2 Mixed No Rel. QBA
18 1 M MD 1 Lurcher No Stray QBA
19 1 M MD 2.5 Jack Russell Terrier No Stray QBA
20 1 F MD 5 ABD x Mastiffx DDB Yes Stray QBA
24 2 F MD 4.5 SBT No Rel. QBA
26 2 M MD 2 Boxer cross Yes MD QBA
33 3 F Yes 5 Springer Spaniel Yes Case QBA
34 3 M Yes 2 Beagle cross No Case QBA
37 3 M Yes 1.25 Bichon frise x Toy poodle No Case QBA
39 3 F Yes 9 SBT No Case QBA
40 3 F Yes 4 Jack Russell Terrier x SBT No MD QBA
42 1 M No 6 Border Collie Yes Rel. Main
43 1 M No 5 Boxer Yes Rel. Main
44 1 F Yes 6 SBT cross No Rel. Main
45 1 F No 8 Yorkshire terrier No MD Main
46 1 M No 2 SBT No Rel. Main
47 1 M No 3 Husky Hound Yes Rel. Main
48 1 F No 3 Parson Jack Russel cross No Rel. Main
49 1 M No 4 Husky Hound (small) Yes Rel. Main
50 3 M Yes 1 French Bulldog No Case Main
51 3 M Yes 2 French Bulldog No Case Main
52 3 F No 2 Rottweiler x GSD x Collie Yes Rel. Main
53 3 M No 6 SBT x Boxer x Labrador Yes Rel. Main
54 3 F No 6 Bull Lurcher No Rel. Main
55 3 F Yes 1 French Bulldog No Case Main
56 3 F Yes 3 Mixed No Case Main
58 4 F No 3 Alaskan Malamute cross Yes Rel. Main
59 4 F No 4 Border collie Yes Rel. Main
60 4 M No 2 Saluki No Rel. Main
61 4 F No 4 Lurcher No Rel. Main
62 4 F No 7 SBT cross No Rel. Main
64 5 M No 2 GSD x Akita Yes Stray Main
65 5 M No 5 Mixed No Rel. Main
66 5 M No 7 SBT No Stray Main
67 5 F No 2 Mixed No Rel. Main
68 5 M No 2 Akita Yes Stray Main
69 5 F Yes 4 Akita Yes Stray Main
70 5 F No 4 Border collie Yes Stray Main
71 5 M No 2 Bichon frise No Rel. Main
72 5 F No 5 SBT No Stray Main
73 5 M Yes 6 GSD Yes Stray Main
74 6 F Yes 2 Yorkshire terrier No Case Main
75 6 F Yes 7 Yorkshire terrier No Case Main
76 6 F Yes 1 Pug x Bichon frise No Case Main
77 6 F Yes 4 Chihuahua No Case Main
78 6 M Yes 10 Bichon fries cross No Case Main
79 6 F No 6 SBT No Rel. Main
80 6 F Yes 4 SBT No Rel. Main
81 6 M Yes 5 Labrador Yes Case Main
Animals 2019,9, 420 6 of 19
Table 1. Cont.
ID Shelter Sex Intact Age (years) Breed W/H/S breed Origin Study
82 6 F Yes 3 Shizu cross No Case Main
83 7 M Yes MD Newfoundland Yes Case Main
84 7 M No 2 SBT No Rel. Main
86 7 M Yes MD Newfoundland Yes Case Main
87 7 M Yes MD Newfoundland Yes Case Main
MD =Missing data; M =male, F =Female; GSD =German Shepherd Dog; ABD =American Bulldog; DDB =Dogue
de Bordeaux; SBT =Staffordshire Bull Terrier; Rel. =Relinquished. Breed information was obtained from pedigrees
(when available) or visual inspection (which for the latter might involve some overestimation of Staffordshire Bull
Terrier crosses [
43
]). W/H/S breed indicates whether the breed stated or the parent breeds (if stated) were in a
working/herding/sporting breed group according to American Kennel Club classifications. ‘x’ indicates a cross
between breeds.
2.2. Home-Pen Activity Budget
Dogs were video recorded in their home-pens for a total of 6 h, blocked over three days and three
2-h time periods. The three 2-h recording periods were classified as: AM, between 09:00 and 11:00,
early PM (EPM), between 11:30 and 13:30, and late PM (LPM), between 14:00 and 16:00. Each dog
(maximum 9 dogs studied simultaneously in a 3-day recording block due to camera availability) was
recorded for one 2-h period each day following a day and period blocked design, so that each dog had
2-h of footage from each period.
Two GoPro Hero 3 (white edition) cameras were used per dog, positioned outside (therefore
not reachable to the dog) at either end of the kennels using specially made wooden mounts and
GorillaPod
®
for mesh kennel walls, and GoPro glass mounts for kennels with solid walls and glass
door panels. The cameras were placed at the height of the dog’s head and angled inwards to capture
the maximum range of the kennel floor space. The mounts were left in place for the full three-day
period, whilst the cameras were removed after each observation period to be recharged and for video
file extraction.
An ethogram (Table 2) was developed based upon previous published work [
23
,
31
,
35
,
44
–
47
] to
record the dog’s behaviour in the home-pen. Behaviour was sampled via instantaneous sampling [
48
].
“Not visible” was selected if the dog was entirely not visible in the camera shot (i.e., was not in the
kennel) or if the view was so obscured that identifying its behaviour became ambiguous. For the
behaviours being characterised by either a lack of movement (e.g., awake but motionless, sleeping) or
repetition (abnormal repetitive behaviours), 10 s of footage was watched continuously 5 s either side
of the scan point in order to best determine the correct following action [
31
,
49
]. The behaviour we
hypothesised to reflect a depression-like condition in dogs, being awake but motionless (ABM) was
defined as follows (adapted from previous studies [
23
,
31
]): “The dog is completely motionless (no head,
body or ear movements) with eyes open apparently staring (anywhere). Dog may be lying, sitting or standing
but not vocalizing. If sitting, head may be in a “drooped” position with head lower than or level with their spine.
State must last for at least 5 s”.
Videos were scored using the Behavioural Observation Research Interactive Software (BORIS) [
50
]
by trained observers (C.F., C.W., H.H., P.J.C., and an intern, Miss S. Vuillermet). Observers were all blind
to the dogs’ results in the anhedonia test at the time they were scoring home-pen behaviour. Training of
observers consisted first of watching videos together with C.F. or N.D.H. to identify examples of each
item from the ethogram. Following this, C.F. and the observers worked independently to scan 15 min of
footage each (scanning each minute), from four dogs gathered during the refinement stage of the pilot.
The scans were visually checked for agreement, with any non-matching scans reviewed and discussed
until the observers agreed on the code to be assigned. This was repeated with a series of random
15-min samples for each dog until raters assigned the same code for all scans on two consecutive
occasions. Agreement was re-checked once (approximately around mid-term data extraction) for
the pilot study and it remained excellent (only one scan differed, therefore we did not evaluate the
difference statistically), or at any time requested by any of the observers on specific data point.
Animals 2019,9, 420 7 of 19
Table 2.
Ethogram for determination of activity budgets of dogs in their home pen (adapted from
previous studies [
23
,
31
,
35
,
44
–
47
]). Note that eye invisibility when the dog is scored “Eyes out of sight”
does not allow for determination of the correct action (e.g., sleeping, or awake but motionless), which
would impair any interpretations of the results; consequently, no subsequent analyses were performed
on this variable.
Category Description
Not visible Dog is out of the kennel, or out of sight and no options can be confidently
selected.
Awake but motionless (ABM)
Dog is completely motionless (no head, body or ear movements) with eyes
open apparently staring (anywhere). Dog may be lying, sitting or standing but
not vocalizing. If sitting, head may be in a “drooped” position with head lower
than or level with their spine. State must last for at least 5 s.
Sleeping Dog is lying down, motionless with eyes closed. State must last for at least 5 s.
Eyes out of sight Could be sleeping or ABM but eyes are out of sight.
Observing
Dog is located at the boundary of the kennel, standing or sitting and attention is
focused outside of the kennel (i.e., the head or the head and the body are
oriented out of “aperture”, mesh or glass door).
Lying down head or ears mobile
Dog is lying down eyes open, no body movement but may be moving ears
and/or head, including any short, subtle movements. Dog should not be
vocalising.
Walking Forward motion of the dog with all four legs in motion [includes trotting,
fast-paced walking or running.
Jumping The dogs front two paws, or all four paws, are offthe ground; may occur in
bouts, or may be still with front two paws on a wall or door.
Sniffing
Nose angled downwards and in close proximity to the floor. Often the head will
make sharp side-to-side movements. Can be done while the dog is in motion or
stationary.
Urinating/Excreting Release of urine or faeces onto floor.
Grooming Licking or chewing of self.
Eating Dog swallows an item it has in its mouth. Results in sequence of characteristic
movements of the mandibular.
Drinking
Series of movements where the dog’s tongue touches the liquid up to the
swallow. A dog may often stop in between drinking to breathe. The head
performs a bobbing motion.
Interact with Object
Can include: chewing of an object that is not food; touching an object with their
front paws repeatedly (pawing); tossing an object in the air; rolling on an object.
Interact with Person
Can include: licking; touching with paws, snout or body; jumping on; sitting on;
lying on; or being petted (dog may be lying, standing or sitting).
Abnormal Behaviour
Including: pacing, walking in a repetitive pattern (at least 3 repeats) usually
along a boundary; flank sucking (taking skin in mouth and sucking); wall
bouncing (dog jumps towards wall and contacts with limbs repeatedly
(>3 times); tail chasing (repeated (>3 times) chasing of tail).
Barking
Vocalisation of loud sounds. Head is often elevated and thrown forwards at the
moment of the bark. Often in bouts of multiple barks.
Whining Prolonged high-pitched sound. Mouth may be open or closed.
Howl Raise muzzle perpendicular to ground and emit a long, drawl out sound
through semi-closed jaws.
None of the above For example, postural transitions (the dog is standing up, or lying down,
exactly at the time of scan), yawning
In order to be time efficient, but not lose accuracy of the data, it was necessary to identify the
maximum sample interval we could use that would produce a representative activity budget. Shorter
sample intervals form more accurate representations of behaviour but are less time and cost effective
than longer intervals [
51
]. For the first seven dogs from Shelter A scans were taken every 30 s over 4 h
Animals 2019,9, 420 8 of 19
(480 scans) in total. An activity budget was calculated for each dog comprising the proportion of scans
seen exhibiting each point event from the ethogram. This was done iteratively for all seven dogs for the
original 30-s interval scans, then utilising every second scan (representing 1-min intervals), every third
scan (representing 1.5-min intervals) and every fourth scan (representing 2-min intervals), creating
4 different datasets. The mean proportion of scans spent in each behavioural state was calculated
for each dataset, followed by the difference in the mean between the 30-s reference data and each
of the second, third and fourth scan data (the Error Proportion; EP). If the EP for the larger interval
datasets for any behavioural state was less than 10% different from of the 30-s mean estimate then it
was considered to have retained accuracy [
51
]. In this way, the longest interval that produced mean
behavioural estimates most similar to the 30-s reference sample, for the greatest number of behavioural
states, was selected for subsequent video analysis (see Supplementary Material Pilot Study for a full
description of this process). Intervals of 1.5-min were deemed to produce acceptably accurate time
budget estimates and were utilised for all subsequent home-pen video analyses.
2.3. Anhedonia Test
A stuffed KongTM toy (KONG Company, Golden, CO, USA) was placed on the floor of the dogs
pen (small, medium, large or extra-large Kong
TM
assigned according to dog size as outlined here [
52
].
The toy was stuffed with a mix of the dog’s own standard dried biscuits, soaked dried chicken pieces
(a common dog training aid) with KONG Stuff’n Paste to bind and the large hole was sealed with a
3-cm long piece of hot dog sausage. Ingredients were mixed following the ratio of 2:3 for biscuits
to soaked dried chicken pieces, for each 2 “squirts” of Stuff’n Paste, in order to keep the Kong
TM
effectively filled the same. All dogs were already habituated to the Kong
TM
toys (provided daily
in each of the recruited shelters) and it has been shown that dogs habituated to Kong
TM
treat filled
Kong’s as feeding devices (i.e., dogs behave in a way demonstrating that they expect to get food from
it) as opposed to a rubber toy [
53
], which could have confounded the results. To prevent potential
neophobic reactions to the Kong
TM
contents, dogs were offered a small amount of the foods used on
the day prior to the test to ensure willingness to eat all of them. To limit the impact of appetite, dogs
were given the Kong
TM
between 15 to 30 min after they had consumed their normal ration of dog food,
as hedonically motivated behaviours seem more driven by opportunism and external stimuli (i.e.,
eliciting cues such as odours) than by states of deprivation [
23
,
54
]. To control further for motivation for
food, the dogs’ latency to approach their normal ration of dog food (less palatable than treat food used
to stuffthe Kong
TM
) was recorded once for each dog on the day previous to the Kong
TM
consumption
test. The dog’s behaviour was video recorded using the same setup as for the home pen recordings
but was conducted on the day after the home pen recordings were completed. Following 30 min of
exposure, the Kong
TM
toys were removed from the pen. The filled toys were weighed before being
given to each dog and weighed again after to enable calculation of how much food mix was consumed.
N.D.H. and two research assistants (H.H. and Dr G. Miguel-Pacheco), blind to the dogs’ activity
budgets, used the video footage of the consumption test to subsequently score: the total time the dog
spent interacting with the food toy (defined as paw or muzzle in contact with, or sniffing the Kong
TM
,
including time stood chewing the food mix but not in physical contact), expressed as a proportion of
the total test duration (Kong_Prop_Time); the number of bouts of interaction with the Kong
TM
(a bout
was considered to have ended when a dog ceased to physically contact the Kong
TM
and ceased to
chew food retrieved from the Kong
TM
, and began again when the dog re-initiated contact with the
Kong
TM
;Kong_Bout_N), and the duration of each bout (averaged for each dog; Kong_Av_Bout_Time).
Data regarding the percentage of the food mix eaten by the end of the 30 min test (% of Kong Eaten) was
included as a fourth test variable.
2.4. Qualitative Behaviour Assessment
QBA focuses on assessing observers’ interpretations of an animal’s behaviour (how does the dog
appear to feel) rather than the observers quantifying individual behaviours themselves. Following
Animals 2019,9, 420 9 of 19
developed methodologies, a QBA term list was utilised from a previously validated list designed to
assess shelter dog behaviour [
55
]. The original 20 term list was reduced to 17 terms for our purposes,
as three terms were not relevant to the footage we had as they related to social behaviour (aggressive,
attention-seeking and sociable) and all dogs were housed alone. Data collection was conducted by N.D.H.
and A.M. and took place at Waltham on September 1, 2017. A total of 6 participants, all experienced in
working with dogs, were recruited (including A.M.). Participants were briefed on the project and trained
in QBA using training clips (of dogs not in the study) by N.D.H., prior to scoring. The QBA terms were
discussed and the definitions clarified as a group until a consensus was reached on how each term
would be defined. A total of 5 clips were scored per dog, for 14 dogs (see Table 1and Section 2.1.2), with
each clip being 30 s long and selected to be evenly spread across the KongTM test period. Ten minutes
were allotted to score each dog (2 min per clip in total), scoring three dogs each time before a break to
help prevent people becoming mentally fatigued and keep scoring quality high. All participants were
blind to the home-pen conditions and the quantitative KongTM data extraction results.
2.5. Statistical Analysis
2.5.1. Quantitative Analysis
Statistical analysis was conducted using SPSS
®
v. 22 (SPSS Inc., Chicago, IL, USA). Descriptive
statistics were calculated to summarise the behavioural variables observed during the home-pen
and anhedonia tests. Time spent ABM and model residuals were not normally distributed, so ABM
was transformed into a logarithmic scale (after adding 1 to remove zeros); the logarithmically
transformed variable is indicated with “lgABM”. Breed could not be included individually in the
models, so dogs were classified according to the American Kennel Club groupings as being from a
working/herding/sporting breed or not, which allowed for crossbreeds to be included. Univariate
linear regression models were utilised to investigate potential associations between time spent ABM
(dependent variable) and each independent variable: sex; neuter status; shelter; age; origin; video
observer; American Kennel Club working/herding/sporting breed (yes/no); and each anhedonia
Kong
TM
test variable. The main outcome variable for this study was the dog’s response to the Kong
TM
,
therefore effects of all other variables were investigated as potential confounding variables. These
variables (age, weeks in shelter, neuter status, female, weight, and working/herding/sporting breed
group) were tested for associations amongst each other using Kendall’s tau-b correlations (in case
of ties) and were included in multivariate models together where associations were found. Model
residuals were visually assessed for normality, and collinearity in multivariate models was checked for
and ruled out using variance inflation factor (VIF) statistics.
2.5.2. QBA Analysis
Data was analysed according to accepted QBA methodology alongside original data on ABM and
Kong
TM
interactions [
56
]. Principal components analysis (PCA) (unrotated and based on a correlation
matrix) was used to analyse the data using QBA scores from each of the 5 clips initially to test for an
effect of clip on reliability. The Kendall Correlation Coefficient (Kendall’s W) was used to evaluate
inter-rater reliability of the resulting PCA scores. Kendall’s W varies from 0, indicating no agreement,
to 1, indicating perfect agreement, and values greater than 0.5 were considered acceptable. Following
this, the QBA data for all clips and all raters were combined into a final PCA along with the home-pen
ABM, and anhedonia test data for each dog.
3. Results
3.1. Quantitative Results
Overall, dogs were most frequently recorded observing (median time: 37.0%), walking (10.5%),
lying down with head or ears mobile (9.9%) and in behavioural or postural transition (8.6%) in their
Animals 2019,9, 420 10 of 19
home pen (Table 3). Crucially, the dogs did display the behaviour we hypothesised to reflect a
depression-like condition (being awake but motionless “ABM”), for a median time of 3.1% of the scans
(first quartile 1.2%, third quartile 6.8%) with clear variation between individual dogs (from 0 to 20.4%
of scans). This ranks similarly to the pilot group of dogs, for whom ABM was the sixth most common
behavioural category exhibited and spent a median time of 2.5% and a maximum of 16.1% of time in
this state (see Supplementary Material Pilot Study section).
Table 3.
Median percentage of scans, first (Q1) and third (Q3) quartiles and minimum (min) and
maximum (max) values for behaviour in the home-pen (n =43 dogs). The behaviour are ordered from
the longest to the shortest median times spent displaying them, and the behaviour we hypothesise to
specifically reflect depression is highlighted in bold.
Behaviour Median Q1 Q3 Min Max
Observing 37.0% 21.6% 49.7% 0.0% 68.5%
Walking 10.5% 5.5% 16.7% 1.2% 30.2%
Lying down head or ears mobile 9.9% 3.4% 14.2% 0.0% 48.1%
None of the above 8.6% 4.9% 15.4% 0.0% 42.0%
Eyes out of sight (could be ABM or sleeping) 4.9% 1.2% 12.4% 0.0% 30.2%
Awake but motionless (ABM) 3.1% 1.2% 6.8% 0.0% 20.4%
Sniffing 1.2% 0.6% 2.5% 0.0% 8.0%
Interacting with object 0.6% 0.0% 1.9% 0.0% 4.9%
Sleeping 0.6% 0.0% 2.8% 0.0% 13.6%
Barking 0.6% 0.0% 4.0% 0.0% 16.7%
Jumping 0.6% 0.0% 2.5% 0.0% 21.0%
Eating 0.6% 0.0% 1.2% 0.0% 3.1%
Grooming 0.6% 0.0% 1.2% 0.0% 4.3%
Interacting with person 0.6% 0.0% 0.6% 0.0% 2.5%
Whining 0.0% 0.0% 0.6% 0.0% 17.9%
Anormal behaviour 0.0% 0.0% 0.9% 0.0% 17.9%
Howl 0.0% 0.0% 0.0% 0.0% 8.6%
Drinking 0.0% 0.0% 0.0% 0.0% 2.5%
Urinating-excreting 0.0% 0.0% 0.6% 0.0% 1.2%
There were no significant differences in (lg)ABM between videos coded by the four different
observers (ANOVA (analysis of variance) with Tukey post-hoc: F =0.62, p=0.605) nor between the
shelters (ANOVA with Tukey post-hoc: F =0.41, p=0.801) or age (linear regression: t =0.199, p=0.843).
Further, no significant differences were found in (lg)ABM according to sex or neuter status (ANOVA
with Tukey post-hoc: F =0.776, p=0.514), nor between dogs’ breed type (American Kennel Club
groupings) (ANOVA with Tukey post-hoc: F =2.07, p=0.158). However, dogs that were relinquished
to the shelter by their owners spent significantly more time ABM than dogs that were seized as part of
welfare cases (controlling for time spent in the shelter, Figure 1; ANOVA with Tukey post-hoc: F =8.09,
p=0.032).
With regards to the anhedonia test, individuals varied in the time they spent interacting with the
Kong
TM
, spending a median time of 29.0% of the test interacting with the Kong
TM
(first quartile 14%,
third quartile 48%, range from 0% to 95%). The manner in which dogs interacted with the Kong
TM
also differed in terms of how many bouts of interaction they engaged in—dogs engaged for a median
number of 8 bouts of interaction, with a minimum of 1 and maximum of 28 bouts (first quartile 3, third
quartile 12). Inter-individual variation was also observed in the proportion of the mix the dogs ate
from the KongTM, from 0 (none) to 100% (median 96.4%, first quartile 38.3, third quartile 100.0).
The variables latency to eat the mix in the Kong
TM
(a control for potential neophobia), and latency
to start eating their regular meal (a control for general interest in food) showed very little variation,
with most dogs (93% and 88%, respectively) starting to eat within a few seconds (on average 1.87s SD
±
2.3 for trying the new mix, and 1.88 s SD
±
1.4 for regular meal). For this reason, these two variables
were not included in these analyses. Although origin was associated with ABM, it was not considered
Animals 2019,9, 420 11 of 19
to be something that should be “controlled” for, as it could be a factor associated with the likelihood
for developing a negative affective response to being in a shelter.
Origin of Dog
CaseStrayRelinquished
log10ABM
1.25
1.00
.75
.50
.25
.00
Page 1
*
0
0
0
0
Figure 1.
Boxplot showing the distribution (median and interquartile ranges) of time spent awake but
motionless (ABM; logarithmically transformed) between dogs that were relinquished by their owners
(n=21), found as strays (n=7) or seized as part of animal welfare legal cases (n=14). ANOVA with
Tukey post-hoc: F =8.09, * p=0.032.
Significant correlations were found between the factors female, weight, and working/herding/
sporting breed group (Table S3), so these were included together in any multi-variate models, with
collinearity checked for using VIF diagnostics. Each Kong
TM
test variable was tested against (lg)ABM
in its own regression model with potential confounders (age, weeks in shelter, neuter status and female,
weight, and working/herding/sporting breed group) checked sequentially for stratifying interactions.
Only one model was found to be significantly associated with ABM. A model including average bout
length of interaction with the Kong
TM
(in seconds) with the number of weeks spent in the shelter was
significant at the p<0.05 level (Table 4). Both variables were positively associated with (lg)ABM, with
longer average bout lengths tending to be associated with greater time spent ABM with increasing
time spent in the shelter. This association is in the opposite direction than would be predicted if time
spent ABM was an indicator that some of these dogs were in a depression-like state.
Table 4.
Results of univariate general linear regression models comparing variables from the Kong
TM
anhedonia test to time spent awake but motionless in the home kennel (logarithmically transformed).
N=43 dogs. Average bout length is mean duration of bouts of interaction with the Kong
TM
. The overall
model was significant at the p<0.05 level: F =3.66, df =2, p=0.035, R
2
=15.8%. See Table S4 for model
statistics from all tests. The 95% CI Bounds indicate the upper and lower 2.5% confidence intervals
around the beta (B) estimate.
B t p95% CI Bounds
Constant 0.441 4.60 <0.001 0.247 to 0.635
Average bout length 0.001 1.98 0.055 0.000 to 0.002
Weeks in shelter 0.015 2.04 0.048 0.000 to 0.029
Animals 2019,9, 420 12 of 19
3.2. QBA Results
Two dimensions were formed from a PCA of the QBA scores: Component
1—Stressed/Anxious to Comfortable/Relaxed, which explained 25.3% of total variance; and Component
2—Interested/Explorative to Bored/Depressed, which explained 15.5% of all variance. Kendall’s W was
applied to the PCA scores for each of the 5 clips (to check whether clip order affected the reliability)
and averages to evaluate inter-rater reliability. There was no effect of clip and both component scores
were deemed suitably reliable, achieving average W-statistics of 0.63 (p<0.001) for Component 1 and
0.53 (p=0.003) for Component 2.
The data for all clips and all raters were then combined in a PCA with the ethogram data ABM,
proportion of test interacting with Kong, the number of Kong
TM
bouts and the average duration of these
bouts to place these measures within the QBA component structure (Figure 2, Table S2). The home-pen
score, ABM and the average bout length of Kong
TM
interaction loaded with the QBA scores “Depressed”
and “Bored”, along the axis for Component 1 (meaning that dogs rated as “depressed” or “bored”
during the Kong
TM
test were displaying greater time awake but motionless in their home-pen), whilst
the Kong
TM
scores for proportion of test time spent interacting with Kong
TM
and the total number of
Kong
TM
bouts loaded towards the Interested/Explorative end of Component 1 (meaning that dogs
rated as Interested/Explorative were spending more time and more bouts interacting with the Kong
TM
).
Animals 2019, 9, x 13 of 20
Figure 2. QBA scores overlaid with KongTM test variables and home-pen awake but motionless ABM
behaviour. The axis for Component 1 (25.3% of variance) reflects Stressed/Anxious to
Comfortable/Relaxed, whilst the axis for Component 2 (15.5% of variance) reflects scores for
Interested/Explorative to Bored/Depressed. When interpreting Figure 2 and Table S2, it is important
to note that all QBA participants (n = 6) were blinded to the dogs’ prior ethogram home-pen and
KongTM test scores.
4. Discussion
The goal of the study was to test the hypothesis that greater time spent displaying waking
inactivity in the home environment could reflect a depression-like condition in kennelled domestic
dogs. We tested this hypothesis in rescue shelter dogs by quantitatively investigating the association
between greater time spent inactive “awake but motionless” in the home-pen and anhedonia (a core
symptom of human clinical depression), using reduced interest in, and consumption of, palatable
food as a proxy for anhedonia. Because greater levels of waking inactivity in dogs is commonly
referred to in the public domain and amongst professionals working with dogs as the dog being
“depressed”, we also aimed to explore whether dogs being qualitatively rated as less interested in
the palatable food test would also spend greater time awake but motionless in their home-pen (with
the raters being blind to the dogs’ actual home-pen inactivity levels and food test quantitative results).
Our quantitative results do not support the study hypothesis. One of the measures showed a
positive association with time spent ABM, with longer average bout lengths interacting with the food
dispenser associated with greater time spent inactive in the home pen with increasing time spent in
the shelter, which is in the opposite direction than would be predicted if greater time spent ABM was
an indicator that dogs were in a depression-like state. Interestingly however, the results from the
QBA study have shown that the time spent awake but motionless in the home-pen correlated with
scores for “depressed” and “bored” (which overlapped with each other) in the QBA of the KongTM
test videos, despite the data being completely independent and scored blindly. This result shows that
people experienced with dogs observed something in the dogs’ demeanour during the anhedonia
test that they associated with a negative emotional state (in this case “depressed” and “bored”), which
in turn was associated with waking inactivity independent of the anhedonia test. This implies that
waking inactivity is not a “normal” healthy behaviour, but instead is associated with a negative
Figure 2.
QBA scores overlaid with Kong
TM
test variables and home-pen awake but motionless
ABM behaviour. The axis for Component 1 (25.3% of variance) reflects Stressed/Anxious to
Comfortable/Relaxed, whilst the axis for Component 2 (15.5% of variance) reflects scores for
Interested/Explorative to Bored/Depressed. When interpreting Figure 2and Table S2, it is important to
note that all QBA participants (n =6) were blinded to the dogs’ prior ethogram home-pen and Kong
TM
test scores.
4. Discussion
The goal of the study was to test the hypothesis that greater time spent displaying waking
inactivity in the home environment could reflect a depression-like condition in kennelled domestic
dogs. We tested this hypothesis in rescue shelter dogs by quantitatively investigating the association
Animals 2019,9, 420 13 of 19
between greater time spent inactive “awake but motionless” in the home-pen and anhedonia (a core
symptom of human clinical depression), using reduced interest in, and consumption of, palatable food
as a proxy for anhedonia. Because greater levels of waking inactivity in dogs is commonly referred to
in the public domain and amongst professionals working with dogs as the dog being “depressed”,
we also aimed to explore whether dogs being qualitatively rated as less interested in the palatable
food test would also spend greater time awake but motionless in their home-pen (with the raters being
blind to the dogs’ actual home-pen inactivity levels and food test quantitative results).
Our quantitative results do not support the study hypothesis. One of the measures showed a
positive association with time spent ABM, with longer average bout lengths interacting with the food
dispenser associated with greater time spent inactive in the home pen with increasing time spent in the
shelter, which is in the opposite direction than would be predicted if greater time spent ABM was an
indicator that dogs were in a depression-like state. Interestingly however, the results from the QBA
study have shown that the time spent awake but motionless in the home-pen correlated with scores for
“depressed” and “bored” (which overlapped with each other) in the QBA of the Kong
TM
test videos,
despite the data being completely independent and scored blindly. This result shows that people
experienced with dogs observed something in the dogs’ demeanour during the anhedonia test that
they associated with a negative emotional state (in this case “depressed” and “bored”), which in turn
was associated with waking inactivity independent of the anhedonia test. This implies that waking
inactivity is not a “normal” healthy behaviour, but instead is associated with a negative emotional
state. That the dogs displaying greater time ABM are “depressed” is not supported by our quantitative
observations; however, our results might tentatively support a “boredom” hypothesis.
In humans, boredom is a negative affective state induced by a lack of desired stimulation or
behavioural opportunities [
57
]. While the use of the term “boredom” in animals and its relationship
to inactivity still needs validation [
57
–
59
], Meagher and Mason [
60
] have proposed an operational
definition of such a state based on motivation to obtain stimulation. According to this definition, a
“bored” animal would display increased willingness to interact not only with positive (appealing)
stimuli, but also with neutral and even slightly aversive situations, as a result of an overall elevated
motivation to obtain stimulation; of any kind. That the dogs spending greater time ABM tended
to display an increased interest in the filled Kong
TM
toy (as shown by longer bout average lengths
interacting with it) would match with the boredom-like state prediction. Furthermore, Meagher and
collaborators have tentatively identified in minks a link between apparent boredom and a specific
subtype of inactivity that might (partly) resemble the waking inactivity observed in the dogs here:
lying down with the eyes open when undisturbed in the home cage [
61
] (although another study [
62
]
failed to replicate this result).
That dogs that were relinquished to the shelter by their owners spent significantly more time
ABM than legal case dogs might also tentatively support an association between waking inactivity
in the home kennel and a boredom-like state. It is indeed possible that being kennelled represents
for these dogs an even more impoverished environment than it does for dogs from a different origin,
as relinquished dogs may have been used to getting various stimulation and positive human contact in
the home. Such a loss of enrichment, where stimulation is lacking but individuals remains generally
motivated to be stimulated, can trigger boredom [
59
]. One may, thus, hypothesize that greater
levels of waking inactivity in dogs relinquished by their owners, and as such putatively exposed
to greater environmental enrichment loss compared to dogs from a different origin; might reflect a
boredom-like reaction.
Such a tentative relationship between waking inactivity in the home environment and boredom-like
states in dogs remains to be investigated further however, as direct positive association between greater
time spent ABM and the positive stimulus was observed only for one measure from the Kong
TM
test. However, “average bout length” is the most discerning of all the Kong
TM
variables, as dogs
with the same overall time could have very different patterns of interaction in terms of bout numbers,
and vice versa, which may be why it was the only significant variable. Crucially however, the dogs’
Animals 2019,9, 420 14 of 19
reactions to neutral and slightly aversive stimuli were not tested here, which are part of the operational
definition of boredom-like states in non-humans [
60
]. Although the current results do not support
the depression-like condition hypothesis, we also believe that further research should be conducted
into the relationship between waking inactivity in the home environment and depression-like state
in dogs, as methodological refinements and complementary investigations are required before it is
possible to safely reject this hypothesis. As such, we will discuss further research directions into
depression-like hypotheses, which do not mutually exclude conducting more in-depth investigation
into boredom hypotheses.
In regards to the assessment of anhedonia, we chose here to assess this phenomenon via reduced
interest in, and consumption of, palatable “treat” foods as a proxy, because reduced sucrose-ingestion
has been validated in laboratory rodents as a proxy of anhedonia [
37
]. This approach has several
drawbacks, however. First, anhedonia in clinical depression refers to a “markedly diminished pleasure
in all, or almost all, activities” [
10
], and reduced interest in palatable food (that dogs are motivated
to work to get access to) does not demonstrate generalised anhedonia. A broader range of activity
motivated by positive affect should, thus, be investigated. For instance, our original research plan
also included assessing reduced interest and eagerness to play, both self-play interacting with toys
and with a person [
63
]. Within this study context, however, implementation of the play protocols
in situ proved challenging for practical reasons, which included difficulties in finding testing areas
that were relatively similar across shelters to perform the play with a person protocol, as well as large
variation in the dogs’ exposure to toys and play (which could have induced neophobic reactions had
we suddenly added toys to the kennels, or conversely increased salience and interest in those dogs
not provided with toys, therefore acting as potential confounds when interpreting the self-play with
toys in the kennel results). A second drawback is that using solid “treat” palatable food does not
directly translate the paradigm used in laboratory rodents (i.e., comparing the amount of diluted
sucrose solution vs. pure water consumed [
37
]. Moreover, as discussed in a previous study [
64
],
low concentrations of sucrose (such as with a strongly diluted solution) might be more sensitive
when measuring anhedonia, while solutions or food with significantly more concentrated palatable
compounds might be more consumed by stressed individuals, including depressed people, as comfort
food intake and carbohydrate “craving” responses. As mentioned in the introduction, our choice of
using reduced interest in, and consumption of, palatable “treat” foods as a proxy of anhedonia was
motivated by feasibility reasons within the available time frame of this study. Longer stays in shelters
for future research or involvement of laboratory dogs from research centres environments should allow
tackling these practical concerns, e.g., allowing for more direct translation of validated paradigms
(longer measurements, with adapted drinking apparatus) and assessment of a broader range of activity
motivated by positive affect. Further research would also include assessing the co-variation of ABM
not only with anhedonia but also with other key symptoms of depression, as discussed in previous
studies [
22
,
23
], as well as into inter-individual variations in susceptibility to developing depression-like
states, such as breed differences and active and passive responder styles.
Along with assessing anhedonia and the existence of other symptoms of depression more fully,
further research (including ours) would benefit from refined definitions or measurement of inactive
behaviour(s) relevant to hypothesis(es) under evaluation. Indeed, while inactive behaviour in shelter
dogs is mentioned in published papers, to date we could not identify with confidence reports of ABM
in the scientific literature. For instance, dogs have been reported as “resting” when “lying down with
eyes open or closed” [
45
] (our emphasis in italic), or with “abdomen touching the ground with its
dorsal, caudal or lateral side, whilst legs are extended forwards, curled close to the body or laid to one
side; eyes are open” [
65
], which compared with ABM does not appear to exclude the possibility of
head or ear movement. Perhaps the closest behavioural description we found comes from a study [
66
]
describing “passive gazing” as the dog being “still and its eyes are open, but its attention does not
appear to be focused on anything in particular”. That study, however, investigated how kennel sizes
influences the dogs’ behaviour (finding no effect on this particular behaviour) and did not study the
Animals 2019,9, 420 15 of 19
possibility that this behaviour could reflect a depression-like condition. This diversity in the way forms
of inactivity are defined highlights a broader issue within the field of inactivity-related investigations,
i.e., that inactivity is often considered simply a default state, or not associated with specific hypothesis,
rather than a true “behaviour” [
58
] and is differentially defined between studies, therefore limiting
cross-study comparisons.
Lastly, we built our hypothesis and chose to define here the specific form of inactivity ABM
following previous works showing that being awake with eyes open, motionless in the home
environment was associated with key diagnostic features of human depression in several other
mammalian species: horses, laboratory mice and non-human primates [
23
,
31
,
67
]. In the current study,
we defined waking inactivity as follows: “Dog is completely motionless (no head, body or ear movements)
with eyes open apparently staring (anywhere). Dog may be lying, sitting or standing but not vocalizing. If sitting,
head may be in a “drooped” position with head lower than or level with their spine. State must last for at least
5 s”. Despite general similarity, there were variations from above-mentioned studies in the way we
defined the inactive state of interest. First, postural criteria included in our dog definition were less
specific than for instance the flat head or back alignment included in the criteria for being “withdrawn”
in horses [
23
] or the “crumpled” body posture of “depressed” monkeys [
24
,
67
]. The “drooped” posture
was an optional part of the definition in the dog and was not commonly (if at all) observed. Moreover,
we did not have the scope to quantify the (lack of) reactivity of the dogs as we did in horses, for
example, in which we measured the animals’ reactivity to a range of visual and tactile stimuli [
68
].
Lastly, the behavioural method we used for recording the inactive behaviour in the dogs (instantaneous
scan sampling with a 5 s interval around the scanning point) was chosen as a compromise between
measuring the exact durations of each bout length (that would allow more precise quantification of
inter-individual variations) and the time required to extract data from the videos (scan sampling being
relatively fast). Continuous recording of the behaviour could have, thus, been more appropriate; its
downside being nevertheless that the time required to extract behaviour from the 400 +hours of video
recording would have conflicted with the budget available for research assistants to extract the data.
For these reasons, it is, therefore, possible that the form of waking inactivity we measured in the
current study partly differs from the above-mentioned forms (e.g., is less “profound”), and that greater
times displaying that behaviour are either associated with a different affective state (e.g., boredom) or
even simply part of the normal behavioural repertoire of kennelled dogs. Further investigations using
continuous recording of the behaviour, refining postural aspects of the definition, and comparing times
spent displaying ABM in more diverse and enriched environments, including at home, would help in
addressing this question.
5. Conclusions
Through this study we showed that shelter dogs spend an average (median) of 3.1% of their time
“awake but motionless”. Distinct inter-individual variation in this behaviour was present, with some
dogs not spending any time “awake but motionless” and others spending 20.4% of their time in this state.
Being relinquished to the shelter by the dogs’ owner (as opposed to being seized as part of a welfare
case) was associated with greater time spent awake but motionless in the home-kennel. We could
not conclude that the most inactive dogs in our study displayed signs of being in a depression-like
state, although methodological refinements and complementary investigations are required before it is
possible to safely reject this hypothesis. However, our results highlight a potential association between
being awake but motionless (apparently doing nothing) in the home-kennel and a boredom-like state
in shelter dogs. Boredom is reported to feel highly aversive in humans, and this result opens the
door to further investigations of this important concept, taking the first steps towards validating a
non-invasive behavioural indicator of “boredom” in the dog. Identifying measures of a boredom-like
state will be required if we are to better understand the impact of housing, management and research
procedures on kennelled and laboratory animals to maximize their welfare, and ultimately develop
treatments for affected individuals.
Animals 2019,9, 420 16 of 19
Supplementary Materials:
The following are available online at http://www.mdpi.com/2076-2615/9/7/420/s1,
supplementary text describing pilot study. Table S1: Median percentage of scans, first and third quartiles and
minimum and maximum values for behaviour in the pilot study based upon scans using 1.5 min. Table S2:
PCA component loading table for QBA scores overlaid with Kong
TM
test variables and home-pen “awake but
motionless” behaviour. Table S3: Kendall’s tau-b correlations comparing all potential confounding variables. Table
S4: Statistics from multi-variate general linear regressions comparing variables from the Kong
TM
test to time spent
awake but motionless in the home kennel (logarithmically transformed) alongside potential confounding factors.
Author Contributions:
Conceptualization, N.D.H., A.M., and C.F.; data curation, N.D.H. and C.F.; formal analysis,
N.D.H.; funding acquisition, N.D.H., A.M., and C.F.; investigation, N.D.H., A.M., S.K., C.W., H.H., P.J.C. and
C.F.; methodology, N.D.H., A.M., and C.F.; project administration, N.D.H. and C.F.; resources, N.D.H. and C.F.;
supervision, N.D.H. and C.F.; visualization, N.D.H.; writing—original draft, N.D.H. and C.F.; writing—review
and editing, N.D.H., A.M., S.K., C.W., H.H., P.J.C., and C.F.
Funding:
This project was funded by a Waltham Collaborative Behaviour and Welfare Award to Carole Fureix
and Naomi D. Harvey. Carole Fureix was supported by a European Marie Curie FP7 IEF Fellowship (fellowship
no. 626732) and internal funding from the University of Plymouth School of Biological and Marine Sciences
during the project period and Naomi D. Harvey was supported by funding from Guide Dogs, a Dogs Trust Canine
Welfare grant and The University of Nottingham HERMES Fellowship through the period of the study. The APC
fees were met by internal funding from the University of Plymouth School of Biological and Marine Sciences and
The University of Nottingham.
Acknowledgments:
The authors are grateful to Sandra Vuillermet (and her invaluable patience) and Giuliana
Miguel-Pacheco for their help in extracting the data from footage; to Ilana Kelland for her help with data collection
during the pilot study; to the five participants who volunteered for participating in the QBA study; to Olivier
Friard and Marco Gamba for their free, open-source BORIS software; and two anonymous reviewers for their
comments on the manuscript.
Conflicts of Interest:
The authors declare no conflict of interest. The European Commission, University of
Plymouth, The University of Nottingham, Guide Dogs and Dogs Trust had no role in the study design, data
collection and analyses, decision to publish or preparation of the manuscript. The Waltham Centre for Pet
Nutrition contributed to the choice of research project, design of the study, in the writing of the manuscript,
interpretation of data and in the decision to publish.
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