Content uploaded by Jan Mol
Author content
All content in this area was uploaded by Jan Mol on Nov 16, 2016
Content may be subject to copyright.
Physiology & Behavior, Vol. 66, No. 2, pp. 233–242, 1999
© 1999 Elsevier Science Inc.
Printed in the USA. All rights reserved
0031-9384/99/$–see front matter
PII S0031-9384(98)00289-3
233
Chronic Stress in Dogs Subjected to Social and
Spatial Restriction. I. Behavioral Responses
BONNE BEERDA,*† MATTHIJS B. H. SCHILDER,†
1
JAN A. R. A. M. VAN HOOFF,†
HANS W. DE VRIES* AND JAN A. MOL*
*
Department of Clinical Sciences of Companion Animals and the
†
Department of Ethology and Socio-Ecology,
Utrecht University, PO Box 80.086, 3508TB, The Netherlands
Received 9 January 1997; Accepted 2 October 1998
BEERDA, B., M. B. H. SCHILDER, J. A. R. A. M. VAN HOOFF, H. W. DE VRIES AND J. A. MOL.
Chroni
c stress in dogs subjected to social and spatial restriction.
I:
Behavioral responses.
PHYSIOL BEHAV
66
(2) 233–242, 1999.—
Six weeks of social and spatial restriction were used as a model to induce chronic stress in Beagles. Behavioral and physiolog-
ical measurements were performed during a period of enriched spacious outdoor housing in groups (GH) and during a subse-
quent 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 inci-
dents 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 en-
vironment, given the opportunity to escape from their home kennel, restrained, walked down an unfamiliar corridor, pre-
sented a novel object, exposed to loud noise, given food, or confronted with a conspecific. During IH, challenged dogs exhib-
ited 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 spa-
tially 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, so-
cially and spatially restricted dogs exhibited a heightened state of aggression, excitement, and uncertainty. Behavioral differ-
ences 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 auto-
grooming, 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. © 1999 Elsevier Science Inc.
Chronic stress Dogs Behavior Social and spatial restriction
1
To whom requests for reprints should be addressed. E-mail: m.b.h.schilder@bio.uu.nl
CHRONIC stress is probably a major contributor to poor
welfare in dogs, and therefore, reliable methods are needed
for measuring it. This means that we need to know how
chronic stress is manifested in the dog. Studies towards
chronic stress are problematic in that, for ethical reasons, it is
not acceptable to apply stress regimes that dramatically im-
pair the welfare of experimental animals. Previously, we have
attempted to induce chronic stress by means of exposing dogs,
intermittently, to loud noise (2). Whereas the subjects re-
sponded minimally to acoustic stimulation, they clearly re-
234 BEERDA ET AL.
sponded to an unfamiliar experimental room and a changed
daily routine. Changes in the way the dogs were maintained
caused enduring increments in the excretion of the stress hor-
mone cortisol. Other studies have shown that (poor) housing
conditions may induce increased passiveness, grooming, ma-
nipulations of the environment, and repetitive movements
(6,9), but not the type of fear behavior that has been associ-
ated with, for example, electric shock (13). To us, this sug-
gests that changes in a dog’s housing conditions can be stress-
ful, without necessarily compromising the subject’s well-being
to an extreme. Therefore, in the present experiment social
and spatial restriction was used to induce chronic stress in
Beagles. An array of behavioral and physiological parameters
were measured to investigate whether these parameters indi-
cate chronic stress. The physiological results will be presented
in a separate article, and here we report on the behavioral
findings. Similar to the deviant behavior of genetically ner-
vous Pointer dogs (10), stress behavior may only be displayed
when subjects are behaviorally challenged. For this reason,
behavioral challenges were included in this study.
METHODS
Animals and Treatments
Fifteen Beagles (age 1.6
6
0.2 year) were obtained from a
spacious group housing facility. The first group (2
C
, 6
F
) was
transported into the research facilities, placed in a social
group housing (GH) system of two or three individuals and
kept outdoors for 7 weeks on lawns of 36 m
2
. The dogs could
observe other dogs and, during the daytime, people. Shelters
were available for protection against bad weather. After this
period, the dogs were individually housed (IH) for 6 weeks in
indoor kennels of 1.7 m
2
, without any visual or physical contact
between individuals. At this time the second group (3
C
, 4
F
)
was put into the GH system, undergoing the same protocol.
Food was provided at 0730 h and water was available ad lib.
Behavioral Observations
Computer-aided behavioral observations were conducted in
a continuous fashion for bouts of 10 min. Six bouts per individ-
ual per week were obtained during weeks 4 and 5 of GH, and
during the first 5 weeks of IH. Behaviors were recorded on line
by using the Observer software package (Noldus Information
Technology, 6702 EA Wageningen, The Netherlands), and
were recorded in terms of the frequency of occurrence or in
terms of the duration of occurrence. Behavioral observations
were conducted according to the following protocol.
Behaviors scored in terms of the frequency of occurrence.
Autogrooming, body shaking, changes from one posture to an-
other, changes from one state of locomotion to another, cir-
cling, crouching, defecating, digging, drinking, eating feces,
floor licking, intentions to change from one state of locomotion
to another, manipulations of the environment, open mouth,
oral behaviors, paw lifting, sighing, stretching, urinating, vocal-
izing, and yawning, we described earlier (1). Also, we recorded
behaviors that dogs directed towards a conspecific—eliciting
play: a variety of behaviors that are performed to elicit play be-
havior in other individuals; exposure of the teeth: the retraction
of the upper lips; licking the corner of the mouth of a conspe-
cific; lying on back: in the near presence of a conspecific the
dog rolls onto its back; paw laying: the forepaw is placed on the
back of a second animal; snout “biting”: a dog puts its jaws over
the snout of another animal; and standing over: the dog posi-
tions its head and chest above the body of a second individual.
Behaviors scored in terms of the duration of occurrence.
Nosing, panting, tail wagging, trembling, locomotive states, and
postures were scored as described previously (1). Postures were
only recorded when the positioning of a dog’s ears, tail, and
legs could be readily assessed, i.e., when a dog stood or walked.
Other behaviors that we recorded in terms of their duration of
occurrence were—ambivalent postures: a crouched body pos-
ture is accompanied by a position of the tail that is higher than
the breed specific position; or in the other way around, a high
body posture is accompanied by a position of the tail that is be-
low normal; and raising of the hairs on the withers.
Behaviors that we scored in terms of the frequency of oc-
currence were scored once every 5 s when dogs displayed it in
a continuous fashion. The interobserver reliability for the be-
havioral protocol was 94%. Interactions between the observer
and the dogs were minimized by using a one-way screen.
In addition to the undisturbed behavior we measured be-
havioral responses to eight different challenges. When chal-
lenged, the dogs were subjected to one of the following proce-
dures—open field: the dog is introduced into a spacious novel
environment. Six different environments are available and are
used in a randomized order; escape: by means of opening the
kennel door, the subject is allowed to escape. Outside, the dog
is free to explore the area in front of the kennels and, to a cer-
tain extent, interact with its confined conspecifics; restraint:
the experimental animal is forced to the floor and kept in a
prostrate lying position for 20 s. Next, the subject is released
and, with an interval of 20 s, restrained for another 20 s; walk-
ing down the corridor: the dog is walked down an unfamiliar
corridor. Six different corridors are used in a randomized or-
der; novelty presentation: through the manipulation of strings,
a novel object is slowly lowered into the experimental kennel.
Clothes, shoes, bottles, and dolls are the items that, in a random
order, are presented to the dog. One test consists of the presen-
tation of one novel object; noise administration: the subject is
exposed to an unexpected sound blast. Sound blasts are 110–120
dB in intensity and 1–2 s in duration; food presentation: a bowl
with food is lowered from the ceiling into the experimental ken-
nel. Similar to the novel objects, the food bowl is manipulated
through strings that are handled from behind a one-way screen;
and confrontation: two male dogs, no (former) cage consorts,
are put together in the experimental kennel; one test includes
two separate confrontations with two different individuals.
The performances of the tests were concentrated in three
test periods that each lasted for 2 weeks. Test period I (pI)
started in the fifth week of GH. Test period II (pII) and III
(pIII) started in the second and fifth week of IH, respectively.
In this way, the dog’s coping abilities were tested before, half-
way, and at the end of the period of restricted housing. The
open field, escape, restraint, walking down the corridor, and
novelty presentation tests were performed twice during each
test period. The remainder of the tests were performed once
during pI and once during pIII. Behavioral observations were
conducted during the first 5 min from the onset of a test. Only
when dogs were walked down a corridor, was the observation
time reduced to 2 min. Prior to the presentations of novelties
and sound blasts, the undisturbed behavior was registered
(for 5 min). This allowed the assessment of novelty-induced
and noise-induced behavioral responses. Novelties, sound
blasts, food, and conspecifics were presented in a test environ-
ment (an indoor kennel sized 5.3 m
2
) to which the animals
were previously accustomed. The dogs were observed from
behind a one-way screen during the novelty presentation,
noise administration, food presentation, and confrontation
test, and recorded on video during the remainder of the tests.
CHRONIC STRESS IN THE DOG 235
Data Processing and Statistical Analysis
Per week, 6
3
10 min of undisturbed behavioral observa-
tions were pooled. The behavior that was recorded during the
5 subsequent weeks of IH was compared both separately and
in combination against mean behavior that was recorded dur-
ing weeks 4 and 5 of GH. Behavioral responses were tested
for differences between pI and pII, for differences between pI
and pIII, and, in the cases of open field, escape, restraint,
walking down the corridor, and novelty presentation tests, for
effects of repeated challenging within a 2-week period. Be-
havioral data were analyzed using an analysis of variance
(ANOVA) for repeated measurements. Contrasts between
GH and IH were tested by the Helmert method, contrasts be-
tween GH and the separate weeks of IH were tested by using
the
F
-statistic. Gender was treated as an independent variable
when running ANOVAs. During the last month of GH, indi-
viduals in the first experimental group experienced relatively
pleasant weather conditions: a mean temperature of 20.6
8
C,
an average 9.6 h of sun per day, a mean wind velocity of 2.9 m/
s, and a mean daily rainfall of 0.6 mm (data provided by the
KNMI, De Bilt, The Netherlands). Individuals in the second
experimental group were subjected to 15.4
8
C, 4.1 h of sun, 3.6
m/s, and 3.8 mm daily rainfall. The first and second group
were, therefore, considered as a pleasant weather (PW) and
bad weather (BW) group, respectively, and weather conditions
were treated as a second independent variable. To achieve
normality, behavioral data were transformed to a logarithmic
scale. Univariate
F
-statistics were corrected with the Huynh–
Feldt epsilon adjusted degrees of freedom, when data sets de-
viated from the sphericity assumption. The level of signifi-
cance was set at a comparison wise error rate
,
0.05. Error
rates were corrected using the Bonferroni correction for mul-
tiple testing, except when behavioral responses were investi-
gated for effects of repeated testing, but not for the number of
parameters that were studied. The results are presented as
mean values
6
SEM.
RESULTS
Spontaneous Behavior
Under outdoor group housing (GH) conditions, the behav-
ior of the dogs was significantly affected by the prevailing
weather conditions. In comparison to the group that experi-
enced pleasant weather (PW) conditions, the group that was
exposed to bad weather (BW) showed behavioral characteris-
tics that were later associated with spatial and social restric-
tion (the IH condition). During GH, BW individuals showed
increased circling, paw lifting and sighing, decreased digging,
and a lower posture in comparison to PW individuals (Table
1). Differences between the PW and BW group in floor lick-
ing, manipulations of the environment, oral behaviors, and
stretching were reflected in the behavioral responses to IH.
TABLE 1
THE BEHAVIOR OF DOGS DURING GROUP HOUSING AND SUBSEQUENT INDIVIDUAL HOUSING
Behavior Group Housing Individual Housing Unit
Circling 0.7
6
0.3
(
p
5
0.006)
3.3
6
1.4
5
times/h
Digging 3.7
6
1.1
(
p
5
0.0008)
0.9
6
0.6
1 3 4 5
times/h
Eating feces 0
(
p
5
0.01)
0.8
6
0.3 times/h
Intentions to change* 1.3
6
0.3
(
p
5
0.03)
0.7
6
0.3
4 5
times/h
Low posture 0.0
6
0.0
(
p
5
0.05)
0.8
6
1.1 % obs. time
Panting 21.3
6
5.2
(
p
5
0.0004)
4.0
6
1.5
1 2 3 4 5
% obs. time
Sighing 2.3
6
0.6
(
p
5
0.02)
3.7
6
0.6
1 2
times/h
Sitting 2.5
6
0.7
(
p
5
0.002)
9.1
6
2.1
1 5
% obs. time
Vocalizations 0.2
6
0.1
(
p
5
0.04)
5.4
6
2.6 times/h
Walking 4.6
6
0.8
(
p
5
0.0001)
1.9
6
0.6
1 2 3 4 5
% obs. time
PW BW PW BW
Circling 0.2
6
0.1 1.3
6
0.5† 3.4
6
2.0 3.1
6
1.3 times/h
Digging 5.4
6
0.8 1.7
6
1.1† 1.4
6
0.6 0.3
6
0.1 times/h
Floor licking 13.5
6
6.7 0.1
6
0.1† 2.0
6
1.0 1.8
6
0.9 times/h
Manipulations of the
environment 0.1
6
0.2 6.8
6
4.5† 18.8
6
9.0 1.9
6
1.2 times/h
Neutral posture 41.6
6
7.1 37.7
6
7.7† 22.7
6
7.8 27.1
6
7.1 % obs. time
Oral behaviors 62.7
6
8.6 42.5
6
7.6† 54.6
6
10.0 88.6
6
18.9 times/h
Panting 36.8
6
5.1 3.5
6
1.5† 7.4
6
2.2 0 % obs. time
Paw lifting 0.3
6
0.1 1.0
6
0.3† 2.1
6
0.8 3.2
6
0.5 times/h
Sighing 1.3
6
0.3 3.4
6
0.6† 3.4
6
0.4 4.1
6
0.4† times/h
Stretching 0 6.0
6
1.2† 2.4
6
0.7 4.1
6
1.4 times/h
The mean behavior (
6
SEM) of 15 Beagles during the periods that they were kept in a spacious enriched out-
door group housing (GH) system and in a restricted indoor individual housing (IH) system. In the upper part of
the table, the
p
-values relate to the differences between GH and the overall period of 5 subsequent weeks of IH.
Significant (
p
,
0.05) contrasts between GH and specific weeks of IH are indicated by superscripts. In the lower
part of the table, behavioral results are presented separately for dogs that experienced nice (PW) and bad
weather (BW) during GH.
Significant differences between the PW and the BW group are indicated by †.
*Intentions to change from one state of locomotion to another.
236 BEERDA ET AL.
After the transfer from GH to IH, the PW group showed sig-
nificant increases in stretching and manipulations of the envi-
ronment, and a significant reduction in floor licking. The BW
group displayed significant increases in floor licking and oral
behaviors, and a significant reduction in manipulations of the
environment. Manipulations of the environment that were
performed by PW individuals during IH were often rigid and
repetitive in character, and included gnawing at the lying bas-
ket. Direct effects of the weather conditions on the dogs’ be-
havior are illustrated by the results on panting. The BW group
panted minimally during GH (a mean 3.5
6
1.5% of the ob-
servation time), and not during IH. Under warmer conditions,
group-housed PW individuals panted during 36.8
6
5.1% of
the observation time (% obs. time), and they showed a de-
cline to 17.2
6
3.8, 19.4
6
6.4, 0.6
6
0.6, 0 and 0% of the obs.
time during the 5 subsequent weeks of IH, respectively.
In response to IH, the dogs showed a number of behavioral
changes that were independent of the weather conditions dur-
ing GH (see Table 1). When socially and spatially restricted,
the dogs showed increased frequencies of autogrooming (Fig.
1), circling, eating feces, paw lifting (Fig. 2), sighing, and vo-
calizing. They showed a lower posture (Fig. 3), sat more, and
walked less. Decreased occurrences were recorded with re-
gard to digging, panting, and intentions to change the state of
locomotion (Table 1).
Significant differences between the undisburbed behavior
of bitches and male dogs were only detected for urinating.
Throughout the periods of GH and IH, urinating was ob-
served 35 times and involved a female dog on only three occa-
sions.
Behavior During and After Behavioral Challenges; Differences
Between GH and IH
To assess a dog’s behavioral responsiveness an animal was in-
troduced into a novel environment, given the opportunity to es-
cape their home kennel, restrained, walked down an unfamiliar
corridor, presented a novel object, exposed to loud noise, given
food, or confronted with a conspecific. Changes in the behavioral
responsiveness that occurred after the transfer from GH to IH
are presented in Table 2. In this section we will indicate a num-
ber of behavioral changes that we recorded across different types
of challenges. For the precise changes in the behavioral respon-
siveness such as they occurred for one specific challenge we refer
to Table 2. Only significant effects are mentioned.
FIG. 1. The effects of the transfer of dogs from spacious outdoor
group housing (GH) to restricted individual indoor housing (IH) on
the performance of autogrooming. Presented are the mean frequen-
cies per hour 6 SEM for 15 dogs. Significant (p ,0.05) differences
from the mean level of autogrooming during GH are indicated by *.
FIG. 2. The effects of the transfer of dogs from spacious outdoor
group housing (GH) to restricted individual indoor housing (IH) on
the performance of paw lifting. Presented are the mean frequencies
per hour 6 SEM for 15 dogs. Significant (p ,0.05) differences from
the mean level of paw lifting during GH are indicated by *.
FIG. 3. The effects of the transfer of dogs from spacious outdoor
group housing (GH) to restricted individual indoor housing (IH) on
the dog’s posture. Presented are the mean percentages of the obser-
vation time (6 SEM, n 5 15) during which the dogs showed of a neu-
tral posture. Significant (p ,0.05) differences from the mean
performance a neutral posture during GH are indicated by *.
CHRONIC STRESS IN THE DOG 237
The dogs showed lower postures when they were chal-
lenged during GH (pI) than during weeks 2–3 (pII) and 5–6
(pIII) of IH. A relatively high posture during IH was accom-
panied by increased nosing and tail wagging. Increments in
tail wagging were in part the effect of repeated testing. Dogs
wagged their tails for respectively 3.3 6 1.2 and 5.7 6 2.0% of
the obs. time (mean values for periods I, II, and III) after the
first and second time that they were restrained within 2
weeks.
IH induced changes in the locomotor responses to differ-
ent types of stimuli. Noise-induced reductions in the time the
dogs walked increased from 23.9 6 4.1 (pI) to 27.1 6 3.0%
of the obs. time (pIII). Dogs walked less during food presen-
tation; pI: 32.5 6 3.9, pIII: 22.0 6 3.0% of the obs. time. In the
confrontation test the dogs sat less; pI: 15.3 6 5.5, pIII: 6.9 6
2.9% of the obs. time. In response to loud noise the dogs
changed less often from one state of locomotion to another,
and such responses were enhanced during IH (Table 2).
Changes from one state of locomotion or posture to another
were increased during the escape and restraint test. IH-induced
increments were attenuated by repeated testing. The number
of changes from one state of locomotion to another decreased
from 61.0 6 2.3 to 55.2 6 2.2 times/5 min during a first and sec-
ond escape test, respectively. Concomitantly, the number of
changes of the posture diminished from 17.7 6 1.2 to 14.1 6 1.4
times/5 min. Repetition of the restraint test was associated
with a decrease in changes from one posture to another; from
an initial 12.0 6 1.3 to 6.7 6 0.9 times/5 min.
Opposite to the effects of repeated testing, paw lifting was
increased during IH in comparison to GH (Table 2). Within
the 2-week test periods, paw lifting decreased from 6.8 6 0.8
to 5.0 6 0.7 times/5 min when the restraint test was repeated.
Similarly, a decrement from 5.8 6 0.8 to 3.4 6 0.7 times/5 min
was found for the escape test.
Circling, as performed during walking down the corridor,
escape, and restraint tests, was increased after the dogs had
TABLE 2
THE BEHAVIOR OF DOGS THAT WERE CHALLENGED DURING GROUP HOUSING AND SUBSEQUENT INDIVIDUAL HOUSING
Behavior Challenge pI (GH) pII(IH2–3) pIII(IH5–6) unit
High posture confrontation 26.3 6 10.3 71.2 6 8.4‡ % obs. time
Neutral posture open field 38.7 6 10.3 43.0 6 8.1† 59.7 6 8.1‡ % obs. time
Neutral posture walking (corridor) 4.1 6 2.2 19.6 6 9.1† % obs. time
Neutral posture restraint 18.3 6 6.2 51.4 6 8.6‡ 55.368.1‡ % obs. time
Half-low posture restraint 74.1 6 6.5 37.2 6 7.0† % obs. time
Half-low posture controntation 23.4 6 6.9 0.8 6 0.4† % obs. time
Low posture food 2.4 6 2.2 0† % obs. time
Very low posture walking (corridor) 2.8 6 1.1 1.9 6 1.2† % obs. time
Tail wagging open field 3.5 6 2.2 7.8 6 2.2‡ % obs. time
Tail wagging waking (corridor) 1.8 6 1.7 12.4 6 7.0† % obs. time
Tail wagging escape 29.3 6 6.3 48.4 6 6.4† 47.0 6 5.1‡ % obs. time
Tail wagging restraint 1.7 6 0.7 7.1 6 2.4† 4.7 6 1.7† % obs. time
Nosing walking (corridor) 32.1 6 7.5 55.8 6 5.4‡ % obs. time
Nosing escape 63.4 6 5.4 85.2 6 2.8‡ % obs. time
Nosing restraint 26.5 6 4.2 72.2 6 5.5‡ 72.2 6 4.7‡ % obs. time
Nosing novelty (before) 13.0 6 2.1 24.3 6 4.5‡ 26.6 6 4.1‡ % obs. time
Nosing food 23.5
6
5.8 31.4 6 4.5† % obs. time
Paw lifting escape 1.6 6 0.3 4.6 6 0.8‡ 7.6 6 1.3‡ times/5 min
Paw lifting restraint 3.1 6 0.7 6.1 6 0.8† 8.6 6 1.1‡ times/5 min
Paw lifting noise (before) 1.3 6 0.7 2.9 6 0.7† times/5 min
Urinating open field 2.9 6 0.8 4.6 6 0.8‡ 5.0 6 0.9‡ times/5 min
Urinating restraint 0.6 6 0.2 2.8 6 0.6‡ 2.8 6 0.5‡ times/5 min
Urinating food 0.9 6 0.3 2.5 6 0.7‡ times/5 min
Urinating confrontation 2.2 6 0.4 3.9 6 0.6‡ times/5 min
Defecating open field 0.9 6 0.4 2.7 6 0.4‡ times/5 min
Defecating restraint 0.4 6 0.2 3.0 6 0.7‡ 2.2 6 0.6† times/5 min
Defecating confrontation 0.3 6 0.3 1.4 6 0.5† times/5 min
Changes of the
locomotive state escape 54.0 6 1.9 60.4 6 2.5† times/5 min
Changes of the
locomotive state restraint 39.5 6 1.9
50.1 6 1.7‡
54.6 6 2.6‡ times/5 min
Changes of the
locomotive state noise (after)* 22.1 6 2.6 27.5 6 3.9‡ times/5 min
Posture escape 11.0 6 1.3 21.5 6 2.5‡ 15.3 6 1.3† times/5 min
Posture restraint 8.7 6 1.2 10.5 6 1.1† times/5 min
The behavior (mean 6 SEM, n = 15) of dogs that were challenged during a period of spacious enriched group housing (pI), during the second
and third week of social and spatial restriction (pII), and during the fifth and sixth week of social and spatial restriction (pIII). Presented are the
behaviors that changed significantly († p , 0.05, ‡ p , 0.01) after the transfer from spacious group to restricted housing.
*Behavioral responses are expressed as the scores that were obtained after noise administration minus the scores from before the sound
blast.
238 BEERDA ET AL.
been transferred from GH to IH; a rise from 0.7 6 0.4 (pI) to
1.5 6 0.4 times/5 min (pIII). IH-induced increments after re-
straint were largely due to repeated testing, which caused an
increase from 0.7 6 0.3 to 1.5 6 0.3 times/5 min.
Ambivalent postures and intentions to change from one
state of locomotion to another occurred during the restraint
and escape test, and were performed more during pIII than
during pI. Increments from 0 (pI) to 2 6 0.9% of the obs. time
(pIII) and from 0.1 6 0.1 (pI) to 0.4 6 0.1 times/5 min (pIII),
were recorded for ambivalent postures and intentions to change
from one state of locomotion to another, respectively. Repeti-
tion of the escape test caused a reduction of ambivalent pos-
tures from 3.1 6 1.1% to 0.9 6 0.4% of the obs. time.
Behaviors that were typically observed in a social context
were increased during pIII in comparison to pI. In the escape
test, when dogs were free to contact their confined conspecif-
ics, or in the confrontation test, the dogs raised their neck hairs
more often; an increment from 1.7 6 0.8 (pI) to 13.6 6 4.3% of
the obs. time (pIII). In the confrontation test they also showed
more growling (pI: 0.4 6 0.2, pIII: 3.0 6 1.3 times/5 min), paw
laying (pI: 0.4 6 0.2, pIII: 2.5 6 0.7 times/5 min) and standing
over (pI: 1.1 6 0.3, pIII: 3.2 6 1.2 times/5 min).
IH-induced changes in the performances of oral behaviors,
open mouth, and yawning were small and inconsistent for the
different types of challenges, or for the periods II and III.
Levels of body shaking were increased from 0.3 6 0.1 times/5
min during pI (mean results from the confrontation, open
field, and restraint test) to 0.7 6 0.2 times/5 min during pIII.
Behavior During and After Behavioral Challenges; Differences
Between the PW and BW Group
A number of differences occurred in the stimulated behav-
ior of PW and BW individuals (Table 3). The pooled data
from the various challenges showed that, similar to the spon-
taneous behavior, panting decreased from 37.2 6 8.3% of the
obs. time during pI to 10.8 6 4.1 and 6.5 6 4.8 % of the obs.
time during pII and pIII, respectively, and that panting was
predominantly shown by the PW group (Table 3). Dogs defe-
cated and urinated more when they were challenged in the IH
period than in the GH period (Table 2), and these increments
were more pronounced in the PW group than in the BW
group. Trembling was virtually restricted to the BW group.
During food presentation, BW individuals trembled 0 and
28.4 6 12.8% of the obs. time during pI and pIII, respectively.
When BW individuals were introduced in the test environ-
ment where novelties were presented, a room that the dogs
had visited many times before, they trembled during 16.2 6
6.4% of the obs. time (pI). After a novel object had actually
been presented, the dogs trembled during an extra 7.9 6 5.8%
of the obs. time. During pIII, BW individuals that were in the
same test environment trembled during 50.3 6 9.8% of the
obs. time. The latter percentage was 18.5 6 7.4% lower after a
novel object had been presented to the dogs. In general, chal-
lenged BW individuals showed more paw lifting, tail wagging,
and nosing than PW individuals. Differences between the PW
and BW group were inconsistent for the various challenges
with regard to the posture and the changes from one state of
locomotion or posture to another (Table 3).
Behavior During and After Behavioral Challenges; Differences
between Bitches and Male Dogs
Response differences between bitches and male dogs are
presented in Table 4. Regardless if challenges were per-
formed during GH or IH, paw lifting was predominantly
shown by bitches. Defecating and especially urinating was
typically observed in male dogs. Also, male dogs showed a
higher posture, wagged their tail more often, and changed less
often from one state of locomotion to another.
DISCUSSION
Social and spatial restriction induced an array of changes
in the spontaneous and stimulated behavior of our dogs. Re-
duced locomotor activity, digging, and intentions to change
from one state of locomotion to another, together with more
circling, we interpreted as obvious adaptations to the re-
stricted housing facilities. As such, these changes may not
have indicated stress. A low posture, eating feces, signs of re-
petitive behavior, and increased autogrooming, paw lifting,
and vocalizing were changes that occurred during social and
spatial restriction, and that have been associated with stress be-
fore (1,4,6,8,12,13). This suggests that they indicated chronic
stress. Social and spatial restriction changed the behavioral re-
sponsiveness of the dogs in that they showed stronger indica-
tions of excitement (higher levels of tail wagging, nosing, cir-
cling, urinating, and defecating, more changes from one state of
locomotion or posture to another, and higher posture), aggres-
sion (higher levels of raised hairs, growling, paw laying, and
standing over), and uncertainty (increased paw lifting, ambiva-
lent postures, intentions to change from one state of locomo-
tion to another, and trembling). Behavioral responses to re-
stricted indoor housing were modulated by meteorological
factors during the control period of spacious outdoor group
housing. The results suggested that the dogs appreciated the re-
stricted housing conditions less negatively when they had expe-
rienced bad weather during the control period.
Bitches may show an increased stress responsiveness in
comparison to male dogs (1,5). In the present experiment, be-
havioral differences between bitches and male dogs did occur
during the challenges, but gender did not affect the chronic
stress behavior.
An important and unique aspect of the present study is
that we measured a large number of parameters simulta-
neously. However, this complicated the statistical analysis of
the results. A correction for the number of parameters that
were measured would have practically ruled out the possibil-
ity of significant treatment 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 ,0.05 as the level of significance.
This necessitates a critical discussion of the results because
there is a fair chance that some of the significant results were
accidental.
Spontaneous Behavior
Dogs that were accustomed to spacious group housing
showed a sustained lowering of the posture during social and
spatial restriction. Dogs show a low posture not only during
poor housing, but also in response to acute aversive events
(1,12). Therefore, it is likely to indicate stress. The possibility
exists that in the present experiment factors other than stress
influenced the posture. Dogs use their posture to establish
and maintain dominance relationships, and low postures in
socially and spatially restricted dogs may have been directly
related to the absence of conspecifics. In this case, the most
pronounced changes should have occurred in those individu-
als that exhibited relatively high postures during the control
period of group housing. There was nothing that suggested
this (data not shown).
CHRONIC STRESS IN THE DOG 239
TABLE 3
BEHAVIORAL DIFFERENCES BETWEEN STIMULATED DOGS THAT HAD EXPERIENCED PLEASANT OR
BAD WEATHER DURING A CONTROL PERIOD OF OUTDOOR HOUSING
Behavior Challenge Period PW BW Unit
High posture escape I 17.3 6 7.9 25.4 6 8.4 % obs. time
High posture escape III‡ 24.1 6 5.5 6.0 6 2.2 % obs. time
High posture restraint I 0 0 % obs. time
High posture restraint III† 0.1 6 0.1 0.4 6 0.2 % obs. time
Low posture restraint I 1.9 6 0.9 13.4 6 4.5 % obs. time
Low posture restraint III‡ 4.1 6 1.3 3.2 6 1.6 % obs. time
Nosing walking (corridor) I 13.4 6 2.7 53.4 6 11.2 % obs. time
Nosing walking (corridor) II† 38.0 6 8.9 62.6 6 10.1 % obs. time
Nosing walking (corridor) III‡ 62.6 6 8.9 48.0 6 4.5 % obs. time
Nosing escape over all‡ 64.5 6 4.7 87.1 6 3.5 % obs. time
Nosing restraint over all† 50.3 6 6.0 64.7 6 6.1 % obs. time
Nosing noise (after)* over all† 219.5 6 8.6 213.7 6 3.4 % obs. time
Tail wagging escape overall‡ 29.3 6 5.5 55.6 6 7.4 % obs. time
Tail wagging escape I 10.4 6 2.7 50.9 6 6.4 % obs. time
Tail wagging escape III† 38.4 6 5.3 56.8 6 5.1 % obs. time
Tail wagging novelty (before) I 0.4 6 0.3 1.9 6 1.9 % obs. time
Tail wagging novelty (before) III† 0.8 6 0.4 0 % obs. time
Tail wagging novelty (after)* over all† 2.4 6 1.5 20.6 6 0.7 % obs. time
Paw lifting escape over all‡ 3.0 6 0.7 6.4 6 1.2 times/5 min
Paw lifting restraint over all† 4.9 6 1.1 7.1 6 1.2 times/5 min
Paw lifting noise (before) over all‡ 0.6 6 0.3 3.8 6 1.2 times/5 min
Panting pooled data over all‡ 29.2 6 7.8 7.1 6 3.6 % obs. time
Urinating open field I 1.5 6 0.5 4.6 6 1.4 times/5 min
Urinating open field II‡ 4.4 6 0.6 4.8 6 1.5 times/5 min
Urinating open field III‡ 5.4 6 0.8 4.6 6 1.7 times/5min
Urinating walking (corridor) over all† 0.1 6 0.0 0.5 6 0.3 times/2 min
Urinating food I 1.1 6 0.5 0.6 6 0.3 times/5 min
Urinating food III† 3.6 6 1.0 1.3 6 0.6 times/5 min
Defecating food I 0.8 6 0.6 0.7 6 0.5 times/5 min
Defecating food III† 2.4 6 1.0 0 times/5 min
Changes of
the state of
locomotion escape over all† 53.7 6 3.1 63.2 6 2.5 times/5 min
Changes of
the state of
locomotion noise (before) overall† 19.4 6 3.5 10.3 6 3.0 times/5 min
Changes of
the state of
locomotion novelty (before) over all‡ 18.9 6 3.7 6.3 6 2.2 times/5 min
Changes of
the state of
locomotion novelty (before) I 8.2 6 2.1 9.7 6 2.4 times/5 min
Changes of
the state of
locomotion novelty (before) III† 25.5 6 3.9 5.5 6 3.1 times/5 min
Changes of
the state of
locomotion food over all† 37.9 6 4.3 20.3 6 5.0 times/5 min
Posture walking (corridor) I 10.9 6 2.6 6.2 6 0.9 times/2 min
Posture walking (corridor) III† 6.0 6 0.5 9.9 6 1.2 times/2 min
Posture noise (after)* over all† 24.4 6 2.5 2.6 6 1.3 times/5 min
The behavior (mean 6 SEM) of dogs that were challenged during a period of spacious enriched outdoor group housing (period I), during the
second and third week of restricted indoor housing (period II), and during the fifth and sixth week of restricted indoor housing (period III). Pre-
sented are the behaviors that changed differently (from period I to periods II and/or III) in dogs that experienced nice (the PW group, n = 8) or
bad (the BW group, n = 7) weather during period I, or that were consistently performed differently in the PW and BW group. The level of signif-
icance is indicated by † (p , 0.05) and ‡ (p , 0.01).
*Behavioral responses are expressed as the scores that were obtained after the presentation of noise or a novel object minus the scores from
before stimulation.
240 BEERDA ET AL.
Autogrooming, vocalizing, and paw lifting were consis-
tently increased during social and spatial restriction. Auto-
grooming (6), vocalizing (4,6,13) and paw lifting (1,12) are be-
haviors that have been associated with stress before, and they
appear useful parameters to identify chronic stress in dogs.
During the period of restricted housing, some dogs devel-
oped coprophagy and rigid and repetitive gnawing at their
basket. The latter behavior was recorded as “manipulations of
the environment” and was predominately shown by individu-
als that had experienced pleasant weather during the period
of group housing. Rigid and repetitive gnawing may fit into
the category of stereotyped behavior and, as such, constitutes
a clear manifestation of chronic stress. Stool eating in dogs
has been associated with environmental stress (8), and our re-
sults confirm this association.
Increased sighing during restricted housing is difficult to
interpret with regard to stress. Only during the first 2 weeks of
restricted housing the dogs showed high levels of sighing. This
disqualifies sighing as an indicator of enduring stress.
In addition to the behavioral changes that we assume to
have reflected stress, social and spatial restriction induced be-
havioral changes that were probably related to other factors.
During restricted housing the dogs walked less and sat more.
Similar responses have been reported in similar situations,
namely during individual housing (9) and confinement to
small areas (6). The most obvious interpretation is that these
changes in the locomotor activity are adaptations to an envi-
ronment that obstructs the performance of walking and pro-
vides a low level of stimulation. Limited exercise may be of
little effect on the physical well-being of dogs (7,11,14), and a
reduced locomotor activity under conditions of restricted
housing does not necessarily indicate chronic stress or poor
welfare. Other behavioral changes that we do not associate
with stress are increased circling, which has been regarded as
modified locomotor activity under conditions of limited free-
dom of movement (9); decreased digging, which probably re-
sulted from the absence of the proper substrate, and a re-
duced number of intentions to change from one state of
locomotion to another, which we interpret as a secondary ef-
fect of decreased locomotor activity. With regard to circling
we noted that, during social and spatial restriction, this was
shown at high levels just before the dogs defecated. On these
occasions circling may have indicated a frustrated desire to
defecate far from the area where the dogs normally resided,
and, as such, it may have indicated stress.
The Behavior During and After Challenges
During three different stages of the experiment the dogs
were challenged: during the control period, and after 1 and 4
TABLE 4
BEHAVIORAL DIFFERENCES BETWEEN BITCHES AND MALE DOGS THAT WERE CHALLENGED DURING
GROUP HOUSING AND SUBSEQUENT INDIVIDUAL HOUSING
Behavior Challenge Period CFUnit
High posture open field over all‡ 0 2.7 6 1.6 % obs. time
High posture escape over all† 9.6 6 4.3 23.8 6 5.9 % obs. time
Neutral posture open field over all‡ 17.8 6 7.6 61.8 6 10.3 % obs. time
Neutral posture open field I 2.6 6 1.7 56.8 6 11.7 % obs. time
Neutral posture open field II† 20.4 6 9.3 54.3 6 9.6 % obs. time
Neutral posture open field III† 30.3 6 11.9 74.4 6 9.5 % obs. time
Neutral posture restraint over all‡ 18.6 6 10.2 53.2 6 7.6 % obs. time
Neutral posture noise (before) over all‡ 3.7 6 3.5 42.2 6 12.5 % obs. time
Half-low posture open field over all† 71.9 6 8.3 32.3 6 10.5 % obs. time
Half-low posture noise (after)* over all† 248.8 6 14.1 22.4 6 14.6 % obs. time
Low posture open field over all‡ 10.2 6 5.4 1.2 6 0.9 % obs. time
Low posture restraint over all‡ 7.0 6 2.5 3.5 6 1.7 % obs. time
Tail wagging open field over all† 4.6 6 3.8 7.4 6 3.6 % obs. time
Tail wagging escape over all‡ 37.7 6 11.7 43.5 6 6.5 % obs. time
Tail wagging restraint over all† 1.6 6 0.7 5.9 6 2.3 % obs. time
Paw lifting open field over all‡ 15.0 6 2.4 7.6 6 1.6 times/5 min
Paw lifting restraint over all‡ 8.8 6 1.4 4.5 6 0.7 times/5 min
Paw lifting noise (after)* over all† 9.3 6 6.0 3.6 6 2.4 times/5 min
Urinating open field over all‡ 1.5 6 0.7 5.5 6 0.9 times/5 min
Urinating escape over all‡ 0.3 6 0.3 6.5 6 1.0 times/5 min
Urinating restraint over all‡ 0.7 6 0.3 2.7 6 0.5 times/5 min
Urinating food over all† 0.4 6 0.2 2.4 6 0.7 times/5 min
Defecating restraint over all† 0.8 6 0.5 2.3 6 0.6 times/5 min
Changes of the:
state of
locomotion
posture
restraint
escape
over all†
over all†
51.6 6 3.2
18.4 6 2.7
46.3 6 2.3
14.6 6 2.0
times/5 min
times/5 min
The behavior (mean 6 SEM) of dogs that were challenged during a period of spacious enriched group housing (period I), during the second
and third week of restricted housing (period II), and during the fifth and sixth week of restricted housing (period III). Presented are the behav-
iors that changed (from period I to periods II and/or III) differently in bitches and male dogs, or that female and male subjects performed consis-
tently different throughout the experiment (over all). The level of significance is indicated by † (p , 0.05) and ‡ (p , 0.01).
*Behavioral responses are expressed as the scores that were obtained after noise administration minus the scores from before the sound blast.
CHRONIC STRESS IN THE DOG 241
weeks of social and spatial restriction. More or less regardless
of the nature of the challenges, poorly housed dogs showed a
relatively high posture, increased tail wagging, nosing, cir-
cling, urinating, and defecating, and changed more often from
one state of locomotion, or posture, to another. Also, in the
presence of conspecifics, they showed more social behaviors
that indicated aggression, namely raised hairs, growling, paw
laying, and standing over. These findings suggest that dogs
that are normally socially and spatially restricted are more ex-
cited during challenges than dogs that are normally kept in a
spacious and social environment. The behavioral indications of
excitement were accompanied by small but significant increases
in paw lifting, ambivalent posture, intentions to change from
one state of locomotion to another and, only in the dogs that
had experienced bad weather during the control period, trem-
bling. It may be that relatively high levels of excitement in
challenged dogs that are normally socially and spatially re-
stricted go together with feelings of uncertainty and stress.
Behavioral expressions of excitement, aggression, and uncer-
tainty were more pronounced after 5 than after 2 weeks of re-
stricted housing, indicating that it was a gradually developing
response pattern.
Difficult to interpret are the increased levels of body shak-
ing that the dogs showed when they were challenged after 5
weeks of social and spatial restriction. Body shaking may
serve to rearrange the fur after this has been disturbed, but it
may also be associated with the release of tension. The latter
interpretation is consistent with the above-mentioned indica-
tions of increased excitement during the period of restricted
housing.
Meteorological Effects on the Behavior
During the control period of spacious outdoor housing in
groups, differences between the first and second experimental
group occurred in circling, digging, floor licking, manipula-
tions of the environment, oral behaviors, neutral posture,
panting, paw lifting, sighing, and stretching. We attribute
these differences to the prevailing weather conditions, that
were pleasant for the first (PW) and bad for the second (BW)
experimental group. In comparison to the PW group, the BW
group showed behavioral features that were later associated
with spatial and social restriction, namely high levels of cir-
cling, paw lifting, and sighing, and a relatively low posture.
This suggests that the BW group experienced environmental
stress before they were subjected to social and spatial restric-
tion. It could be argued that the differences between the PW
and BW group did not indicate different level of stress, but
that they merely resulted from direct meteorological influ-
ences on the behavior (e.g., heat-induced panting). That the
BW group did appreciate the control period more negatively
than the PW group is demonstrated by the behavioral re-
sponse differences.
The majority of the behavioral challenges were performed
indoor (except for the open-field test), and direct meteorolog-
ical influences on the behavioral responsiveness were mini-
mal. During the control period we found that challenged BW
individuals showed increased tail wagging, nosing, trembling,
and paw lifting in comparison to PW individuals. Thus, similar
to the spontaneous behavior, BW individuals showed early
behavioral response characteristics that we later associated
with chronic housing stress. From the foregoing we conclude
that bad weather conditions during the control period induced
some stress in the BW group, and that this early episode of
stress may have attenuated the BW group’s negative appraisal
of restricted housing. As a possible result, significant increases
in stretching and manipulations of the environment were only
observed in poorly housed PW individuals.
Behavioral Differences between Bitches and Male Dogs
There are indications that bitches respond more strongly
to stressors than male dogs (5). In the present experiment,
challenged male dogs showed higher posture, more tail wag-
ging, and less paw lifting than challenged bitches. Changes
from one state of locomotion, or posture, to another were
more frequent in bitches. Especially the results of paw lifting
indicate that the challenges were more stressful to bitches
than to male dogs. Although the challenges suggested that
bitches were more susceptible to acute stress, the chronic
stress responses to restricted housing were similar for both
sexes. Throughout the experiment, male dogs urinated and
defecated more often than bitches. Because psychologically
stressed Beagles do not show the antidiuretic response that is
observed in Border Collies, Wirehair Fox Terriers, Cocker
Spaniels, and German Shepherds (3), the relatively low levels
of urinating in our female Beagles may not have been related
to stress. Other factors, for example a stronger motivation to
mark their territory, may have caused the higher frequencies
of urinating and defecating in males.
In summary, dogs that were accustomed to spacious out-
door group housing showed enduring changes in their sponta-
neous behavior and behavioral responsiveness when they
were kept singly in small indoor kennels. Increased auto-
grooming, paw lifting, and vocalizing, low posture, and the oc-
currence of repetitive behavior and coprophagy we inter-
preted as indications of chronic stress. With regard to the
behavioral responsiveness, socially and spatially restricted
dogs showed increased expressions of excitement, aggression,
and uncertainty. Such behavior will not be specific to a state
of chronic stress, and it will be of limited use for the assess-
ment of stress outside an experimental setting. The present
findings may help to identify chronic stress, but their extrapo-
lation to field situations should be exercised with caution. The
present stress period lasted only 6 weeks, and the experimen-
tal subjects were of the same breed and homogenous in age
and life history. Under field conditions, dogs may have experi-
enced stress for a longer time, may not be of the Beagle type,
and differ from our experimental animals with regards to age
and life history. As a result, they will show deviating stress re-
sponses. Also, we found indications of chronic stress that may
be specific to social and spatial restriction, and it cannot be ex-
cluded that they are inadequate when a completely different
source of stress is at order. In a serial article, we will integrate
the reported behavior with a set of physiological measures.
ACKNOWLEDGEMENTS
Students J. C. von Frijtag Drabbe Künzel and N. Geurts helped in
performing the experiments. The technical assistance by Harry van
Engelen, Ries Pel, and Han de Vries was highly appreciated. We are
indebted to H. Buijs, J. Minke, R. Remie, E. Tanboer, and other per-
sonnel from Solvey Duphar (Weesp) for their generous help. The
critical reading of the manuscript by Anne McBride is highly appreci-
ated. This work was supported by funds from the Ministry of Agricul-
ture Nature and Fishery, the Sophia Vereeniging ter Bescherming
van Dieren, and the Bond tot Bescherming van Honden.
242 BEERDA ET AL.
REFERENCES
1. Beerda, B.; Schilder, M. B. H.; Hooff, J. A. R. A. M. van; Vries,
H. W. de; Mol, J. A.: Behavioral, saliva cortisol and heart rate
responses to different types of stimuli in dogs. Appl. Anim.
Behav. Sci. 58:365–381; 1998.
2. Beerda, B.; Schilder, M. B. H.; Hooff, J. A. R. A. M. van; Vries,
H. W. de; Mol, J. A.: Unpredictable episodes of noise do not
result in behavioral or physiological signs of chronic stress in
dogs. (Submitted).
3. Corson, S. A.; O’Leary Corson, E.: Constitutional differences in
physiologic adaptation to stress and distress. In: Serban, G., ed.
Psychopathology of human adaptation. New York: Plenum Press;
1976:77–93.
4. Elliot, G.; Scott, J. P.: The development of emotional distress
reactions to separation in puppies. J. Genet. Psychol. 99:3–22;
1961.
5. Garnier, F.; Benoit, E.; Virat, M.; Ochoa, R.; Delatour, P.: Adre-
nal cortisol response in clinically normal dogs before and after
adaptation to a housing environment. Lab. Anim. 24:40–43; 1990.
6. Hetts, S.; Clark, J. D.; Calpin, J. P.; Arnold, C. E.; Mateo, J. M.:
Influence of housing conditions on beagle behaviour. Appl.
Anim. Behav. Sci. 34:137–155; 1992.
7. Hite, M.; Hanson, H. M.; Bohidar, N. R.; Conti, P. A., Mattis,
P. A.: Effect of cage size on patterns of activity and health of bea-
gle dogs. Lab. Anim. Sci. 27:60–64; 1977.
8. Houpt, H.: Ingestive behavior problems of dogs and cats. Vet.
Clin. North Am. 12:683–692; 1982.
9. Hubrecht, R. C.; Serpell, J. A.; Poole, T. B.: Correlates of pen
size and housing conditions on the behaviour of kennelled dogs.
Appl. Anim. Behav. Sci. 34:365–383; 1992.
10. Klein, E.; Uhde, T. W.: 24-hour motor activity in genetically ner-
vous and normal pointer dogs. Biol. Psychiatry 23:523–527; 1988.
11. Newton, W. M.: An evaluation of the effects of various degrees of
long-term confinement on adult beagle dogs. Lab. Anim. Sci.
22:860–864; 1972.
12. Schwizgebel, D.: Zusammenhänge zwischen dem Verhalten des
Tierlehrers und dem Verhalten des Deutschen Schäferhundes im
Hinblick auf tiergerechte Ausbildung. Akuel. Arbeit. Artgemass.
Tierhaltung 138–148; 1982.
13. Solomon, R. L.; Wynne, L. C.: Traumatic avoidance learning:
Acquisition in normal dogs. Psychol. Monogr. (Gen. Appl.) 67:1–
19; 1953.
14. Tipton, C. M.; Carey, R. A.; Eastin, W. C.; Erickson, H. H.: A sub-
maximal test for dogs: Evaluation of effects of training, detraining,
and cage confinement. J. Appl. Physiol. 37:271–275; 1974.
