Applied Animal Behaviour Science 124 (2010) 113–120
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Applied Animal Behaviour Science
journal homepage: www.elsevier.com/locate/applanim
Rapid shaping of behaviour associated with high urinary cortisol in
domestic dogs
Emily-Jayne Blackwell
a
, Alina Bodnariu
a,b
, Jane Tyson
a,b
,
John William Stephen Bradshaw
a,∗
, Rachel Alison Casey
a
a
Anthrozoology Institute, Department of Clinical Veterinary Science, University of Bristol, Langford BS40 5DU, UK
b
Royal (Dick) School of Veterinary Studies, University of Edinburgh, Roslin EH25 9RG, UK
article info
Article history:
Accepted 18 February 2010
Available online 21 March 2010
Keywords:
Dog
Stress
Associative learning
Glucocorticoids
Displacement behaviour
Repetitive behaviour
Coping style
abstract
The occurrence of stress has widely been associated with impairments in learning abilities
in animals, although the influence of stress appears to differ with the complexity of tasks.
Previous research has suggested that some domestic dogs exhibit both physiological (ele-
vated cortisol) and behavioural signs of stress when newly admitted to re-homing centres.
In this study we have investigated whether levels of stress as measured by urinary cortisol:
creatinine is sufficient to impair the learning of simple associations. On the day following
their admission to a re-homing centre, 32 dogs were trained on one classical conditioning
task and one operant conditioning task; 6 days later, they were trained on a second operant
conditioning task. Their mean urinary cortisol:creatinine ratio (C/C) fell from 27.1 × 10
-6
to 22.3 × 10
-6
(nmol/l:nmol/l) between these 2 days; a substantial proportion (78% on day
1, 63% on day 7) of dogs had ratios above the range of 5–20 × 10
-6
, which is that defined as
clinically normal (Bush, 1991), suggesting high levels of stress. The dogs’ average time to
reach criterion on either task on day 1 was unrelated to C/C or to behavioural signs of stress;
this lack of correspondence may reflect the diverse previous experiences of the dogs. On day
7, the six dogs which failed to reach criterion for the operant association were significantly
less active and interactive in their kennels than the others. For the remainder, a high rate
of learning the operant association was associated with high C/C (in excess of 40 × 10
-6
),
and a poor performance was associated with fearful behaviour in the kennel. Dogs appear
to have adopted one of two coping strategies: either the display of fearful behaviours and
an impaired ability to learn the tasks, which may reflect a ‘reactive’ style of responding, or
a higher level of HPA axis activation and an enhanced ability to rapidly learn a new task,
which may be indicative of a more ‘proactive’ coping style.
© 2010 Elsevier B.V. All rights reserved.
1. Introduction
The effects of stress on learning and memory are com-
plex, and appear to depend upon several interacting factors,
including the nature of the external stressor, the prior his-
tory of the individual animal, the type of learning, and the
temporal and contextual relationship between the stres-
∗
Corresponding author. Tel.: +44 117 928 9673; fax: +44 117 928 9582.
E-mail address: J.W.S.Bradshaw@bristol.ac.uk (J.W.S. Bradshaw).
sor and the learning or retrieval task (Joëls et al., 2006; Kim
and Diamond, 2002; McEwen and Sapolsky, 1995; Mendl,
1999). Hanoch and Vitouch (2004) have argued that rather
than a decrease in overall ‘performance’ with increasing
stress, there is a switch in strategy, from attending to and
processing a large number of cues to a focussing of atten-
tion on to fewer salient cues. This is likely to be adaptive,
since although evaluating multiple cues from the environ-
ment may lead to a more accurate response, processing will
also take longer (Trimmer et al., 2008). As the perceived
threat in a context increases, it makes sense for an animal
0168-1591/$ – see front matter © 2010 Elsevier B.V. All rights reserved.
doi:10.1016/j.applanim.2010.02.011