Journal of Veterinary Behavior 16 (2016) 53e64

Contents lists available at ScienceDirect

Journal of Veterinary Behavior

journal homepage: www.journalvetbehavior.com

Research Paper

Minimizing fear and anxiety in working dogs: A review

Nicola J. Rooney a, *, Corinna C.A. Clark b, Rachel A. Casey c, d
a
Animal Welfare and Behaviour Group, University of Bristol, Langford, United Kingdom
b
Life Sciences, University of Warwick, Coventry, United Kingdom
c
Dogs Trust, London, United Kingdom
d
Clinical Science and Services, Royal Veterinary College, Hatfield, Hertfordshire, United Kingdom

a r t i c l e i n f o a b s t r a c t

Article history: The causes of fear and anxiety in working dogs are multifactorial and may include inherited charac-
Received 25 August 2015 teristics that differ between individuals (e.g. Goddard and Beilharz, 1982; 1984a,b), influences of the
Received in revised form environment (Lefebvre et al., 2007), and learned experiences during particular sensitive periods
2 November 2016
(Appleby et al., 2002) and throughout life. Fear-related behavior compromises performance, leads to
Accepted 3 November 2016
significant numbers of dogs failing to complete training (e.g., Murphy, 1995; Batt et al., 2008), early
withdrawals from working roles (Caron-Lormier et al., 2016), and can jeopardize dog and handler safety.
Hence, amelioration of fear and anxiety is critical to maintain dogs in working roles and to ensure their
Keywords:
fear
well-being. Although current methods of selection and training are seemingly effective at producing
anxiety many dogs which work in a remarkable array of environments, some dogs do not make the grade, and
prevention longevity of service is not always maximized. Programs should strive for optimal efficiency and they need
working dog to continually analyze the value of each component of their program, seek evidence for its value and
selection test explore potential evidence-based improvements. Here we discuss scientific evidence for methods and
habituation strategies which may be of value in reducing the risk of fear behaviors developing in the working dog
population and suggest potentially valuable techniques and future research to explore the benefit of
these approaches. The importance of environmental influences, learning opportunities, and effects of
underlying temperament on the outward expression of fear and anxiety should not be underestimated.
Identification of characteristics which predict resilience to stress are valuable, both to enable careful
breeding for these traits and to develop predictive tests for puppies and procured animals. It is vitally
important to rear animals in optimal environments and introduce them to a range of stimuli in a positive,
controlled, and gradual way, as these can all help minimize the number of dogs which develop work-
inhibiting fears. Future research should explore innovative methods to best measure the relative resil-
ience of dogs to stressful events. This could include developing optimal exposure protocols to minimize
the development of fear and anxiety, and exploring the influence of social learning and the most effective
elements of stimulus presentation.
Ó 2016 Elsevier Inc. All rights reserved.

Introduction guarding, transportation, hunting, entertainment/sport (e.g., rac-

ing), contraband detection (e.g., police, military, and rescue ser-
Domestic dogs are used for a variety of working roles in which vices, Rooney et al. 2004), emotional therapy, and medical alert
they are required to continue performing trained tasks in envi- (Strong et al., 1999; Rooney et al., 2013). This diverse range of ac-
ronments which may include novel, unexpected, or potentially tivities can expose dogs to potentially stressful stimuli in their
aversive stimuli. Roles include herding, deterring predators, surroundings: high levels of noise from machinery and gunfire
explosions (and subsequent shock waves); transportation; variable
terrain with unstable and varied surfaces underfoot; high levels of
dust and smoke; loud machinery and traffic (Brown, 2011). In
* Address for reprint requests and correspondence: Nicola J. Rooney, Animal
addition to this range of physical factors, dogs may need to cope
Welfare and Behaviour Group, University of Bristol, Langford, United Kingdom. Tel:
0117 928 9469, 0781 841 3310 (mobile); Fax: 0117 928 9582. with a variety of people, some behaving in unpredictable ways, the
E-mail address: [email protected] (N.J. Rooney). presence of other animals, and variable routines. Dogs can respond

http://dx.doi.org/10.1016/j.jveb.2016.11.001
1558-7878/Ó 2016 Elsevier Inc. All rights reserved.
54 N.J. Rooney et al. / Journal of Veterinary Behavior 16 (2016) 53e64

to these types of situations with behavioral signs of fear or anxiety, of high intensity or low predictability (Gray, 1971). Risk is increased
including freezing, withdrawing, or showing aggression (Casey, where animals have had prior exposure to other negative events in
2010). Such responses are likely to interfere with a dogs’ ability to their general environment or within the specific context. Individual
perform its role. In this study fear is defined as the behavioral differences in response thresholds mean that even seemingly
response shown to actual danger (Boissy, 1998) and anxiety as the benign stimuli will provoke a fear response in some individuals, a
emotional state elicited in potentially threatening situations, for response that may be due to inherited characteristics, previous
example, novelty, or when some elements of the environment environmental influences, learned experiences, and to interactions
predict a negative outcome (Ennaceur et al., 2006; Massar et al., between these effects.
2011). Both affective states (fear and anxiety) are particularly con- Studies on personality may shed light on individual differences
cerning in roles for which optimal performance is critical for safety. for the likelihood of animals developing fears. The “shy-bold”
For example, fear-related behaviors on the part of guide dogs or continuum has been demonstrated in a wide range of species (Jones
military search dogs can be life-threatening to both dog and and Gosling 2005). Murphree and Dykman (1965) developed a
handler and are therefore a common reason for failure in these population of pointer dogs that showed extreme fear by selecting
roles (e.g., Murphy, 1995; Rooney et al., 2002; Batt et al., 2008). for those which reacted most to a range of standardized fear-
The experience of fear is aversive (Grandin and Deesing, 2002), inducing tests. The relevance of the “shy-bold” continuum in dogs
and by analogy with the experience of humans, it is likely that is supported by Svartberg and Forkman (2002) who identified 5
anxiety is similarly aversive because it too functions to promote underlying factors of which 4 appeared to form a higher order
avoidance of eliciting stimuli. Individual dogs which show fearful factor analogous to the shy-bold characteristic.
behaviors in a rehoming kennel environment appear to have an If we simply test for the appearance of fear behaviors in an in-
impaired ability to learn operant tasks (Blackwell et al., 2010), with dividual, we cannot be sure of the extent to which observed
similar effects demonstrated in a range of species (e.g., Shors 2004). behavior is a manifestation of previous experience or underlying
This potentially makes training more time consuming and costly. personality. What need to assess “resilience” to withstand stressful
Research has also suggested that high levels of fear-related be- circumstances. Measuring contributing characteristics may be a
haviors can lead to increased disease risk (Terlouw et al., 1997) promising approach to identifying risk factors for fear. Resilience
through modulation of immune responses, and possibly ultimately (Yehuda et al., 2006a) is defined as the extent to which an indi-
lead to a reduced lifespan (Dreschel, 2010). Particularly relevant to vidual is able to adapt in the face of adversity, trauma, or risk of
dog programs with breeding schemes is the finding that decreased threat. Coping strategies are well studied and have been defined in
sperm quality is associated with anxiety in dogs (Memon, 2007). terms of approach (active or proactive coping) or avoidance (pas-
Fear and anxiety can inhibit complete erection and ejaculation sive or reactive coping) styles (Roth and Cohen, 1986). In humans,
(Kutzler, 2012, cited in Mills et al., 2014), and reduce proceptive and active coping strategies improve individuals’ ability to manage
receptive behaviors in bitches resulting in a failure to breed stressful situations and reduce their risk of psychiatric illness
(Grundy et al., 2002). Hence, in addition to welfare concerns arising (Valentiner et al., 1994). People who showed active coping strate-
from exposing working dogs to fear-provoking situations for which gies had lower levels of distress and post-traumatic stress disorder
they are poorly prepared, and the issue of handler safety when dogs 6 months after the New York World Trade Center attacks (Silver
perform poorly, there are potential economic consequences. Fear et al., 2002).
and anxiety can lead to the loss of dogs from programs at assess- Proactive and reactive types of responding have been well
ment, during training, or later through early withdrawal from active documented in laboratory rodents (de Boer et al., 2003) and in
working roles (Caron-Lormier et al., 2016), with an associated loss other species (see review, Koolhaas et al., 1999; but see also
of the potential contribution they could make during their working Forkman et al., 1995, and Jensen et al., 1995). Attempts have been
lives. made to characterize “coping styles” in dogs in rehoming centers,
Fear responses develop when animals are exposed to events or based on their physiological and behavioral responses to kenneling
stimuli that they perceive as negative and salient (i.e., above their and their ability to learn an operant task. These responses suggest a
individual threshold of tolerance). On first exposure, animals will “reactive” style of responding, or a more “proactive” style
tend to show a startle response toward a novel stimulus and (Blackwell et al., 2010). A study of police dogs found 3, not 2, cat-
orientate toward it. This is an adaptive response to a change in their egories of dogs (Horvath et al., 2007). Coping responses are not
environment. On subsequent exposures, this response may either immune to environmental influences or circumstantial changes in
increase or decrease. Habituation is the process whereby a response emotion, and individuals will often learn to show different behav-
gradually reduces with repeated presentation of the eliciting iors in response to different situations (Roth and Cohen, 1986). In a
stimulus, and the threshold increases (Grissom and Bhatnagar, working dog context, we may be inadvertently selecting for dogs
2009). In contrast, sensitization is the process whereby an ani- with specific coping styles. However some coping responses, such
mal’s response increases on presentation of a stimulus (Davis, 1974). as avoidance, may not be possible, and so we may also be causing
Having been sensitized to a stimulus and identified it as a threat, stress by not enabling dogs to perform their preferred response.
the animal will attempt to both identify predictors for the stimulus Variation in coping styles suggests that the outward manifes-
and develop a response to avoid it (e.g., to flee). In the working and tation of the same inner emotional state will differ between ani-
companion dog, the aim is to manipulate factors both in the dog mals. Some dogs may appear less overtly fearful than others
and its environment to maximize the chance that habituation oc- because their coping strategy is more passive or reactive rather
curs, while minimizing the risk of sensitization. than proactive. This pattern presents a challenge for identifying
Multiple factors influence the development of behaviors asso- signs of fear and anxiety when testing individuals and for deciding
ciated with anxiety and fear across species and specifically in dogs. at what intensity to introduce new stimuli.
The nature of the stimuli and the manner in which it is first pre- There are 3 potential approaches to reducing the risk of these
sented, including the social context, are both important. High- fear- and anxiety-related behaviors developing in working dog
intensity stimuli (e.g., explosions), or situations where aversive populations:
events occur consecutively without allowing animals a chance to
recover, are very likely to provoke a response in most animals. a) select and breed individual dogs with the lowest risk of
Sensitization is more likely to occur when the presented stimulus is developing these behaviors,
 N.J. Rooney et al. / Journal of Veterinary Behavior 16 (2016) 53e64 55

b) control the environment in which dogs are kept and reared to and so no data are available on how these dogs would have per-
minimize the risk of fear behaviors developing, and formed compared to those that passed, and hence criterion validity
c) optimize the method of initial stimulus exposure to minimize cannot be ascertained (Taylor and Mills, 2006). More data should be
the risk of dogs sensitizing and fears becoming established. collected on the relationship between tests and the outcome (e.g.,
validity), including for dogs that would ordinarily be rejected.
Most working dog agencies aim to achieve all of these, but they
vary in their approaches. We describe some of the methods used Study bias
and review evidence for their success. Possible practical solutions,
such as improved selection, management, and training of working Often studies which claim to reduce fear behaviors via selection
dogs, are also discussed, and questions raised about the value of tests concurrently change several procedures making it difficult to
some current practices. determine true cause. For example, Haverbeke et al. (2010) reported
increased efficiency in military dogs which were selected specif-
Selection of animals most suitable for working environments ically not to show fear of people, but they simultaneously intro-
duced the Human Familiarisation and Training Program, which also
Working dogs are selected in a variety of ways. Most large increased levels of training for both dogs and handlers. The effect of
assistance dog agencies have their own established breeding pro- selection based on exhibition of fear is therefore difficult to ascer-
grams, while smaller organizations often procure puppies which tain from outcome measures.
may be selected on the basis of a suite of tests (with varying degrees
of validation) and fostered before being reassessed for training. Presentation of high-intensity stimuli
Some police, military, and security dog programs include breeding
schemes, but a majority rely on purchasing adult dogs from private Many selection tests involve presentation of sudden unexpected
breeders or vendors. Some agencies procure unwanted companion stimuli. The DMA (Wilsson and Sinn, 2012) used in Scandinavia
animals from owners or rehoming centers. The Scandinavian mili- presents a stranger, a dark room, loud metallic noises, an unstable
tary (Swedish and Norwegian) has well-established and validated surface, dummies, human “ghosts” and gunfiredall of which are
methods for testing dogs before selection (e.g., Dog Mentality potentially fear-provoking. These stimuli could sensitize dogs dur-
Assessment [DMA]: Wilsson and Sundgren 1997). Other selection ing testing, resulting in increased fear behavior on subsequent
tests vary considerably in validation criteria. Most working dog presentation (Davis, 1974). Because tests are conducted consecu-
agencies have their own criteria for breeding and/or selecting ani- tively (Wilsson and Sundgren, 1997; Sherman et al., 2015), sensi-
mals with an assumed reduced risk of developing problematic fear- tization risk is increased (De Meester et al., 2011).
and anxiety-related behaviors, especially fears of humans, loud By observing the dog’s reaction to gradual exposure to specific
noises, and novel environments. Criteria are implemented differ- stimuli which they are likely to encounter during operational ac-
ently between programs and may involve selection of breeding tivities, the level of exposure at which any contextually fearful
stock, adult dogs, and/or puppies. response occurs is identified. This approach would allow treatment
for specific fears, rather than outright rejection for dogs which may
Testing for fearful behavior otherwise be suitable for some type of working life. Ogata et al.
(2006) applied a Pavlovian aversive conditioning protocol and
Many agencies that train working dogs have developed tests to measured autonomic and behavioral parameters. Increased heart
screen animals predisposed to show fearful behaviors. Details of the rate and body temperature occurred in response to a conditioned
commonly used tests are often undocumented (e.g., UK military; stimulus and suggested using fear conditioning as a method to test
Rooney et al., 2003). Some are published, including some of the for trait fear (by measuring extinction of to the learned conditioned
tests used for guide dogs (Serpell and Hsu, 2001; Asher et al., 2013), stimulus) in dogs. Behavioral changes did not consistently correlate
police dogs (Slabbert and Odendaal, 1999; Svobodová et al., 2008), with physiology and the authors concluded that autonomic re-
general service dogs (Wilsson and Sundgren, 1997), improvised actions can be more reliable and consistent measures than some
explosives devices (IED) detection (Sherman et al 2015), and mili- behavioral measures. Testing may benefit from the use of physio-
tary dogs (Haverbeke et al., 2009; Sinn et al., 2010). Predictive logical measures, such as heart rate variability, shown to be asso-
testing is fraught with difficulties, and the extent to which this is ciated with dogs’ behavioral responses to perceived stressors
objectively assessed is variable. There are several potential prob- (Vincent and Leahy, 1997), and may prove more valuable than
lems with many tests which need to be addressed. simple heart rate which was not seen to correlate with behavioral
signs of fear and anxiety during working dog assessments
Poor validity (Sherman et al., 2015).

Many tests have poor validity (Taylor and Mills, 2006). Single Lack of attention to fear behaviors during testing
tests conducted in one context do not necessarily indicate behav-
ioral responses in others. For example, tests of behavioral ten- In some organizations, testing focuses on perceived priority
dencies in rehoming centers show limited predictability of later working traits such as motivation to work and exhibition of trained
owner reports of fearful and anxious behaviors in the home attack behaviors. Behavioral signs of anxiety or fear are seldom
(Mornement et al., 2015). Tests routinely performed to select US recorded. The selection of confident dogs is a major priority for
military dogs, including tests for environmental and gun shyness, many agencies, but selection tests may not effectively select against
have been shown to have limited predictive validity when fear. Objective video analysis of Swedish military selection tests
compared to later certification outcomes (Sinn et al., 2010). revealed higher levels of fear among dogs which were selected
Haverbeke et al. (2009) found that although some test elements compared with those that were not (Foyer et al., 2016), suggesting
seemed to predict later fear behaviors in Belgian military dogs, inadvertent selection for some fearful behaviors. Observers vary in
most tests were poorly predictive of later undesired behaviors. For their ability to accurately interpret behavioral responses, especially
many working dog tests, the predictive value cannot actually be if signs are subtle (Tami and Gallagher, 2009; Marti et al., 2012).
calculated, as dogs which “fail” initial testing do not enter training Accurate and early detection of behavioral indicators of fear is
56 N.J. Rooney et al. / Journal of Veterinary Behavior 16 (2016) 53e64

critical and resources to teach observers to recognize the commonly contributions of these elements are understood to enable tests to be
missed signs have been developed (Loftus et al., 2012). Such tools developed for different requirements.
will likely be useful in conjunction with physiological indicators of When using an open-field model to assess sound-induced fear
behavioral reactivity. and anxiety in potential IED dogs, Gruen et al. (2015) exposed an-
imals to loud noises on consecutive days but did not explore dif-
Reliance on testing puppies ferences in the dogs’ past experiences or exposure to noises. In the
same population of dogs, Sherman et al, (2015) saw differences
Organisations that breed or purchase puppies wish to reject between individuals in their “emotional reactivity” and the dogs
puppies least likely to succeed as early as possible. Many agencies showed consistency in individual response across a large number of
use a suite of “puppy tests” which try to predict fearfulness among stimuli. Such responses may be affected by both personality and
other traits. Tests for fear of loud noises include using weights past history. The degree to which the responses predicted working
dropped in buckets (Murphree and Dykman, 1965) or on tables ability in operational conditions and the relative importance of
(Svobodová et al., 2008), whistles (Pfaffenberger and Scott, 1976), genetic versus experiential factors is unknown. To detect dogs that
metal cans (Fisher and Volhard, 1985), party poppers (Hoffmann are at risk for developing fear and anxiety, rather than assessing
et al., 1995), simulated thunderstorms (Seksel et al., 1999), clap- preexisting fear, one could instead test for variance in underlying
ping (Champness, 1996), or pistols (Slabbert and Odendaal, 1999). decision-making processes that influence resilience to stress
Tests may examine fear of novel people (e.g., Murphree and exposure (Yehuda et al., 2006a). Understanding whether dogs
Dykman, 1965; Slabbert and Odendaal, 1999); novel objects, exhibit “proactive” or “reactive” styles of responding (Koolhaas
including umbrellas (Hoffmann et al., 1995), hair driers (Seksel et al., 1999) may also help to identify the nature of their response
et al., 1999), novel environments (e.g., open stairs [Goddard and to fear-evoking stimuli. Other approaches could include measuring
Beilharz, 1986]), and unstable surfaces. A major flaw of testing at the relative degree of “optimism” and “pessimism” (cognitive bias).
a very young age is that it does not account for modification by Animals that have a more “pessimistic” cognitive bias tend to judge
ontogeny and learning. Analysis of the test commonly used by novel or ambiguous stimuli as “more likely to be negative” and so
Australian Guide dogs (Goddard and Beilharz, 1982; 1984a,b; 1985; may be more likely to develop fear responses. A “pessimistic”
1986) revealed that although fearfulness as an adult was signifi- cognitive bias has been associated with a tendency to show
cantly predicted by a test at 8 weeks of age (and was the only separation-related behavior (Mendl et al., 2010) and is reduced by
predictable trait), the predictive value increased with age of testing. treatment with a selective serotonin reuptake inhibitor, fluoxetine
In contrast, a large meta-analysis of 31 “personality” tests in dogs (ReconcileÔ), combined with behavior modification (Karagiannis
(Fratkin et al., 2013) found that puppy behaviors were moderately et al., 2015). Because cognitive bias appears to be a better mea-
consistent even with longer intertest intervals but that fearfulness sure of underlying mood state rather than more transient emotional
(along with responsiveness to training) in puppies was one of the responses (Mendl et al., 2010), it may be a better predictor of
least consistent dimensions. behavioral responses across contexts and a valuable tool in pre-
Scott and Bielfelt (1976) saw no increase in the adult perfor- dicting success in working environments.
mance of guide dogs when breeding stock were selected on the Research into methods by which to better predict behavioral
basis of their puppy test scores. This finding is supported by a study tendencies and predictors of resilience is required and to better
of the development of Arms and Explosives search dogs (Rooney understand the extent to which underlying temperament charac-
et al., 2003), which showed little correlation between behaviors teristics, themselves, become plastic with environmental changes
shown by 8-week-old puppies and those seen in equivalent tests in and stress exposure (Yehuda et al., 2006a). It may be beneficial to
adult dogs. Instead, an inverse correlation between fear of slippery investigate whether variation in underlying characteristics of
surfaces at 8 weeks and 11 months was found. Similarly, Asher et al. temperament correlate with patterns of allelic variation in genome-
(2013) found that puppies which scored as more confident on a wide association studies (Hayward et al 2016) or in the expression
ramp (1/5 stimuli tested) were less likely to qualify as guide dogs. in targeted areas of the genome.
These discrepancies may be partially due to using deficiencies Several novel measures have been associated with increased
highlighted in the puppy test to direct remedial training. Some resilience to stressors in laboratory species and humans (Yehuda
puppy tests detect predispositions that can subsequently be over- et al., 2006a). Neuropeptide Y (NPY) may have an important role
come by operant conditioning (e.g., puppies finding their existing in reducing risk through modulatory effects on important regu-
behavior “unsuccessful” and changing to an alternative strategy). latory systems in the brain such as the hypothalamic-pituitary
The variable and generally low degree of success in such tests adrenal (HPA) axis (Heilig, 2004), and noradrenaline release
suggests that trying to predict adult behavior from puppy tests is (Pich et al., 1993). NPY has been found to be higher in human
problematic, and as failures at procurement tests are rarely trained, military service veterans who have been exposed to extreme
the true test reliability is not assessed. The value of puppy testing is stress but did not develop PTSD, when compared with those who
therefore questionable without assessment of predictive validity. developed PTSD. NPY also appears to correlate with the extent of
symptom improvement (Yehuda et al., 2006b). Such assays may be
The influence or prior learning as well as temperament biological measures of resilience and/or ability to recover. The
ratio of plasma dehydroepiandrosterone sulphate to cortisol was
Many tests purport to measure “temperament” but actually positively correlated with peoples’ ability to perform well in
measure a dog’s behavioral response to a specific contextual chal- stressful military situations (Morgan et al., 2004). Other potential
lenge. Such contextual tests may be desirable (e.g., to detect markers of resilience associated with differences in HPA axis ac-
whether dogs being rehomed show aggression when handled), but tivity include 24-hour urinary cortisol secretion, circadian rhythm
it is potentially more problematic where tests are screening of cortisol release, lymphocyte glucocorticoid receptor number,
breeding animals. The approach cannot separate a response due to and lysozyme IC50 as an indicator of enhanced glucocorticoid
a particular historical aversive experience from an underlying responsiveness (Yehuda et al., 2006a). Investigation of some of
predisposition (e.g., “temperament”). It is unlikely that the these new measures, either in isolation or through metabolomic
“temperament” and “learned” component of a behavior in an in- profiles may indicate dogs most likely to withstand the stress of
dividual dog can be teased apart, it is important that the different working dog life.
 N.J. Rooney et al. / Journal of Veterinary Behavior 16 (2016) 53e64 57

Measures of patterns in sweat production that are linked to proportion which are flexible in their response across environ-
emotional responses such as fear can be obtained noninvasively in mental conditionsda disadvantage in a working animal needing to
humans (Lin et al., 2011) and sheep (Reefmann et al., 2009a,b). adapt to a range of environments. It is unknown whether such se-
Measurement in the dog would require modification because lection acts at the level of the animal’s perception of fear-inducing
canine apocrine gland distribution differs. stimuli, the central evaluation of stimuli and assignment of
Studies of “laterality” (preferential use of one side of the body) emotional significance, their expression of fear behaviors, or even
suggest possible links with guide dog success (Batt et al., 2008), the animal’s ability to inhibit these behaviors. By selecting against
specific aspects of guide performance (Batt et al., 2010), general dogs which show an active fear response (e.g., for those whose
problem solving ability (Marshall-Pescini et al., 2013), and some behavior changes little when presented by stimuli), we may be
measures of fear, although not with agility competition success selecting against “proactive” characteristics and favoring more
(Siniscalchi et al., 2014). In humans, an association between hand passive or “reactive” fear responses (Koolhaas et al., 1999). Dogs
preference and the propensity to experience anxiety has been with a “passive” style of responding may have a different strategy
described, and similar patterns identified in dogs. Dogs with for achieving rewards and avoiding aversive events, with conse-
weaker paw preferences (a measure of cerebral lateralization) were quent implications for training success. A less obvious behavioral
more reactive to thunderstorm and firework noise (Branson and response to a stimulus may not necessarily indicate a reduced
Rogers, 2006). Motor lateralization, combined with other factors, negative emotional experience. It is possible that selective breeding
was indicative of success in potential guide dogs (Batt et al., 2008). programs may in fact result in unreactive “zombies” (D’Eath et al.,
Different measures of laterality and different ways of interpreting 2010).
measures often yield differing results, so use of laterality measures Behavior traits may be genetically linked to other morpholog-
for other working disciplines requires further testing. ical, or physiological characteristics (e.g., Mackenzie et al., 1985),
which may be undesirable. Hence, although it is theoretically
Breeding against propensity to show fearfulness attractive to select animals from which to breed offspring with a
reduced risk of showing fearful behaviors, current knowledge about
Several breeding experiments have suggested that fearful the characteristics which underlie risk of behavioral signs, their
behavior is heritable (Murphree and Dykman, 1965; Goddard and patterns of inheritance, and their association with allelic variation
Beilharz, 1982). The distribution of behavioral phenotypes of sub- in genome-wide studies, is currently insufficient to determine the
sequent generations has been changed by selecting breeding ani- consequences of such an approach. It may be that a more suitable
mals of extreme “types” at either end of a continuum (i.e., the most approach is to investigate the heritability of underlying character-
and least fearful). These studies predominantly concentrate on so- istics such as stress resilience and optimism, rather than selecting
cial fearfulness, although several also look at nonsocial stressors directly for phenotypic presentations of fearful behavior.
including reactions to loud noises. It may therefore be possible
through selection to reduce the frequency of the more extreme Reducing the risk of fear-related behaviors through
phenotypes of fearful behaviors. The breeding program for UK environmental manipulation and rearing
guide dogs has been effective in reducing the occurrence of fear-
associated behaviors (Willis, 1995) and many breeding programs Preventing problems is ultimately more cost-effective than
have similarly bred against outward expression of fear. managing them, so it is equally important to focus on the aspects of
Studies using working dog populations (e.g., Hsu and Serpell, the environment that may influence the development of fearful
2003, Arvelius et al., 2014a,b) have similarly suggested that the responses. There are also opportunities to control both prenatal and
expression of fearful behaviors is partly heritable. In the Swedish postnatal maternal environment when there is considerable syn-
armed forces, the behavioral scores for confidence and environ- aptic plasticity, and appropriate actions can ameliorate the chance
mental sureness as measured during the DMA had heritabilities of of later problems developing.
0.23 and 0.15, respectively (Arvelius et al., 2014a) (see also Wilsson,
2016, this volume). Heritability assesses the proportion of the Manipulation of factors affecting susceptibility to stress and hence
variation in the populations’ test scores that can be accounted for by likelihood of developing fears
the genetic component. When assessing rough collies, Arvelius
et al. (2014b) found similar heritabilities for test scores and rela- Background levels of arousal and concurrent causes of fear and
tively high correlations between fearful behavior during testing and anxiety during stimulus presentation can increase the risk of
that reported by owners using the Canine Behavioral Assessment sensitization (Davis, 1974). There is considerable evidence that
and Research Questionnaire (Hsu and Serpell, 2003). Arvelius et al. states of anxiety in rodents increase the magnitude of the startle
(2014b) concluded that if breeding animals were to be selected on response (Bijlsma et al., 2010). People with anxiety disorders are
the basis of scores for curiosity/fearlessness in the DMA, then more likely to develop a range of conditioned fear responses (Lissek
breeders would also report a concurrent decrease in nonsocial fear et al., 2005). Therefore, adapting living environments, human
scores. When examining general fearfulness, 1 of 3 fear-related contact, and general training methods to avoid anxiety-provoking
factors derived from multivariate analysis of multiple subtests situations is important, both for home-living and kenneled work-
used on potential guide dogs, Goddard and Beilhraz (1984) ob- ing dogs. Detailed reviews exploring ways to minimize stress of
tained heritability estimates as high as 0.80. kenneled dogs are available (e.g., Gaines, 2008; Rooney et al., 2009).
Selection based on test scores should be considered with some
caution because little is known about the specific underlying General human contact
characteristics selected for within breeding programs based on Interactions between dogs and human handlers are important
behavioral phenotypes. It is unknown, for example, whether dog and the interspecific relationship may affect numerous aspects of
populations show the type of structure suggested by Wilson et al. social behavior, including the development of fears. Human inter-
(1994) -shy-bold characteristics where animals at both population action can be beneficial to dogs in reducing the stress of confine-
extremes show low environmental flexibility. If this were the case, ment (Coppola et al., 2006) and may increase indicators of positive
then selection against “innately shy” (or fearful) dogs may not just well-being, such as decreased blood pressure and increased b-
alter the proportion of dogs which exhibit fear, but also the endorphin (Odendaal and Meintjes, 2003). A program of human
58 N.J. Rooney et al. / Journal of Veterinary Behavior 16 (2016) 53e64

interaction in chronically stressed shelter dogs resulted in reduced performance (Haverbeke et al., 2010), suggesting that training
excitation and cortisol in the experimental dogs compared to con- methods are vital in working dog operations.
trols (Hennessy et al., 2006). Handlers of military dogs who took
their dogs home after work described them as less fearful, more Kennel management and routines
sociable, more accepting of stroking by strangers, and less likely to
bite compared to those handlers whose dogs remained in kennels Gaines (2008) stresses the importance of husbandry regimes to
(Lefebvre et al., 2007). Pet dog owners who shared more activities decrease stress of kenneled dogs. Specific husbandry processes that
with their dogs were less likely to categorize them as “nervous” can lead to distress include shutting dogs in small dark inner ken-
(Bennett and Rohlf, 2007), although cause and effect are unclear. nels while cleaning their home kennel (Gaines, 2008), using noisy
equipment such as cleaning hoses (Mills, 2005) and separating dogs
Reduction of stress during routine training from conspecifics (Walker et al., 2014). Identification and amelio-
ration of these concerns is important to stress reduction. Increasing
The type of contact dogs receive is important. Data from Hiby the predictability of a dog’s routine may be important (e.g., walking
et al. (2004), Blackwell et al. (2008), and Rooney and Cowan and feeding at predictable times) if rigidity which may limit future
(2011) strongly suggest that punishment-based methods may in- flexibility is avoided (Gaines et al., 2008). To best prepare dogs for a
crease levels of fear and anxiety and potentially lead to sensiti- range of situations and activities, gradual adaptation from initially
zation to other environmental stimuli. Punishment-based training predictable routines to less predictable and more variable sched-
of pet dogs is linked to an increased incidence of behavior prob- ules may best be done over time. In this way, dogs will “have an
lems (Hiby et al., 2004), including fear, anxiety and aggression expectation of the unexpected” and may cope better with changing
(Blackwell et al., 2008), wariness towards strangers, reduced circumstances when they become necessary.
playfulness (Rooney and Cowan, 2011), and increased anxiety-
related aggression and excitability (Arhant et al., 2010). Dogs Early-life environments
regularly trained with electric shocks show behavioral evidence of
fear and distress in the presence of their owner, even outside the Prenatal and postnatal effects
training context (Schilder and van der Borg, 2004). Dogs subjected Those programs with breeding and puppy-walking schemes can
to physical reprimands have been shown to score significantly affect adult dog behavior by influencing prenatal and postnatal
higher for aggression (Hsu and Sun, 2010) and dogs whose owners environment. Most work on early-life effects has focused on human
report using a higher proportion of punishment are less likely to development (e.g., Grant et al., 2009; Hellemans et al., 2010), ro-
interact with a stranger (Rooney and Cowan, 2011), which could dents (Bosch et al., 2007), and farmed species (e.g., pigs, Jarvis et al.,
be due to fear and anxiety. 2006; sheep, Dodic et al., 2002) and has shown that prenatal anx-
Most working dogs are now being trained primarily using pos- iety adversely affects stress reactivity in offspring. In comparison,
itive reinforcement and negative punishment. There are still some very little is known about the effect of prenatal experience on the
trainers who use coercive approaches based on a “dominance” behavior and development of puppies. Given the compelling evi-
approach to interpreting dog behavior (Bradshaw et al., 2009), and dence in other species, the ability of pups to recognize odors
rough handling remains common in specific disciplines and orga- learned in utero (Wells and Hepper, 2006), and similar endocrine
nizations (Haverbeke et al., 2009). Aversive methods, including profiles and changes in cortisol in pregnant bitches as in other
pulling the leash and hanging, are associated with low body pos- mammalian species (e.g., sheep; Concannon et al., 1978), it is likely
tures indicative of fear or distress and poor performance in military that dogs are similarly influenced by variation in maternal exposure
working dogs (Haverbeke et al., 2008). Those military dogs sus- to stressors during pregnancy. It would seem prudent that due
pected to have been handled roughly in the past were perceived to attention is given to the range of experiences of breeding bitches
be more fearful (Lefebvre et al., 2007). During protection and during pregnancy (Gaines et al., 2008).
obedience work, dogs which had received more punishment ten- There is evidence that puppies manipulated in the neonatal
ded to show more fear behaviors (Haverbeke et al., 2009).When period differ in later stress responsiveness. Battaglia (2009) de-
examining prison officers’ behavior toward their search dogs, scribes a study on a biosensor program for military dogs where
Rooney et al. (2007b) found that handlers who believed in using puppies of 3-16 days of age were stimulated daily using a range of
high levels of punishment tended to have less confident dogs. All handling techniques, including being placed on a cold towel.
studies discussed are correlational, and the possibility exists that Puppies had improved cardiovascular function (HR), stronger heart
dogs with specific problems may be more likely to be trained using beats, stronger adrenal gland function, greater tolerance to stress,
coercive methods. Regardless, such dogs show a consistent pattern and greater resistance to disease (Battaglia, 2009). Mild stressors
between aversive training methods and behavioral problems, applied in early life have been reported to promote resilience (Macrì
including fears. Longitudinal cohort studies and experimental trials and Würbel, 2006, 2007; Macri et al., 2009; 2010; 2011). Providing
would be needed to demonstrate causal links. pregnant mothers and neonatal puppies with a stimulating but not
Avoiding positive punishment-based techniques and interacting overtly fear-inducing environment may promote resilience in
with dogs in a calm and consistent way is likely to be important in puppies. Mixing bitches into new social groups, unaccustomed
reducing the development of fear-related behaviors. Horses trained confinement or social isolation (Rooney et al., 2007a), malnutrition
using positive reinforcement interacted more with the handler (Poore et al., 2010), inconsistent handling, transport, and exposure
(Sankey et al., 2010) and, zoo rhinos (Holden et al., 2006) and pri- to specific inescapable ear-eliciting situations (e.g., loud noises)
mates (Savastano et al., 2003) have been successfully trained to should be avoided.
present various body parts in a calm safe manner through operant
conditioning using positive reinforcement. This approach is used in Management of weaning
farm environments for ease of handling, reduction of stress (Kilgour
et al., 1991), and cognitive enrichment (Manteuffel et al., 2009). In In most “natural” environments, the process of weaning is a
military dogs in which positive reward training sessions were used gradual one, with offspring becoming progressively more
in conjunction with altered selection procedures and handler emotionally and nutritionally independent (Latham and Mason,
training, dogs demonstrated increased confidence and overall 2008). Many companion animals, including dogs, are removed
 N.J. Rooney et al. / Journal of Veterinary Behavior 16 (2016) 53e64 59

suddenly from their mothers, usually concurrently from their exposure (Levine, 2000), and its current emotional state (Davis,
familiar social and physical environment. Behavioral (Houpt and 1974) will all affect the probability of an animal experiencing
Hintz, 1983; McCall et al., 1985), and physiological (McCall et al., sensitization. Mills et al., (2014) identified important aspects of a
1987; Malinowski et al., 1990) signs of distress at this sudden stressor for dogs to be physical characteristics (affective quality,
weaning are observed in many species. Activation of the HPA axis intensity, magnitude, duration), the predictability, and expectation
has also been shown to continue for several weeks after weaning in of the animal in relation to the stressor, and the preparation given
both rodents and primates (Levine, 2000), and there is no reason to to enable coping and opportunities for control over the stressor.
assume this is not the case for dogs. Initial intensity of stimulus presentation needs to be below the
Appropriate management of weaning can reduce the risk of threshold of startle for the animal. In general, the principle is to
inducing fears. The nature and period over which maternal sepa- start as low as possible because it is better to increase the level
ration occurs can have positive or detrimental effects on later gradually from well below all dogs’ tolerance than risk sensitiza-
resilience to stressors. Rodents studies show that early separation of tion. Because each animal will have a unique tolerance to different
pups from their mother can induce short- and long-term changes in types of stressors, it is important to select an initial level of expo-
the stress reactivity system, as indicated by the potentiated HPA sure which is below that to which any individual in the program
axis response to subsequent stressors (e.g., Knuth and Etgen, 2007; population will respond aversely. In a diverse population of pro-
Lippmann et al., 2007). Early and abrupt separation also enhances cured dogs, it may be difficult to find a level to which no dogs
manifestations of anxiety and depression-like behaviors (Fabricius respond. A preliminary test to identify those outlying individuals
et al., 2008; Lambás-Señas et al., 2009) and impairs spatial with established fears is recommended. These dogs would then
learning and memory (Aisa et al., 2007; Tata et al., 2015) during require remedial training including desensitization, counter-
adulthood. In contrast, repeated, short maternal separation conditioning, prior to controlled exposure, and habituation.
increased resilience to stressful events later in life (Parker et al., The benefits of this type of gradual introduction to novel stimuli
2006; Benetti et al., 2007) and reduced fearfulness (Macrì and in contrast to repeated exposure of a full intensity stimulus
Würbel, 2006). The positive effects of such separations may have (“flooding”) are understood by many animal trainers. Horses given
resulted from increased attention from the mother when the pups a gradual introduction to a moving white nylon bag showed both
were returned. Increased maternal stimulation appears to have a behavioral and physiological differences compared to those
beneficial effect on neural development and can reverse the effects without such an introduction. Those with gradual exposure pro-
of early-life stressors (Imanaka et al., 2008). Slabbert and Rasa tocols needed fewer training sessions to remain calm on stimulus
(1993) studied South African Police dog puppies which received presentation, and all subjects in the gradual exposure group
equal human attention but were separated from their mothers at completed training, which was not the case for those in the full
either 6 or 12 weeks. The late weaned puppies gained weight more exposure group (Christensen et al., 2006). Sixteen IED dogs showed
quickly and were in better condition. The study did not report any an overall reduced response to noise over a 5-day testing period,
differences in fear behavior toward people or other stimuli. but as the noises presented on each day were different, it is likely
Evidence of optimal weaning protocols for working dogs is that the dog habituated to the testing environment. Some dogs did
limited. Research suggests that protocols should vary across breeds not decrease in responsiveness which suggests that the initial
because they differ in the age of onset of fear-related behaviors exposure level may have been too high (Gruen et al., 2015).
(Morrow et al., 2015). The advantages associated with maternal Habituation to noise in rats is more effective when exposure is
care, social interaction with littermates, learning social signaling, interspersed by longer gaps. Rats were exposed to either six 30-
and avoidance of sudden traumatic events all support later and minute sessions of white noise in a single day or one 30-minute
gradual weaning of puppies destined for working environments. exposure daily for 6 days (Masini et al 2008). The groups showed
Regardless, many organizations routinely wean early to ensure similar habituation of plasma corticosterone, ACTH, heart rate, and
socialization opportunities are maximized and to facilitate foster core body temperature, but the habituated responses were not
placement. For example, in the United Kingdom, Guide Dogs for the retained in the single-day exposure group, on reexposure 48 hours
Blind routinely remove puppies from their mother at 6-8 weeks, later. The effect may be associated with the experience of rapid eye
below the age generally advised for other dogs. The relative quality movement sleep between training sessions (e.g., Levin and Nielsen,
of breeding and rearing environments of pet dogs affects the ideal 2007) which consolidates memory. Habituation sessions may
weaning time (Appleby et al., 2002), a finding applicable for benefit from being separated by a period of sleep.
working dogs. Habituation in laboratory rodents is context specific, so “recov-
ery” of the response occurs in contexts different from that where
Introduction of potentially fear-provoking stimuli in an the habituation occurred (Jordan and Strasser, 2000). Should ele-
optimal way ments of the context alter, a startle response may recur, particularly
if the change of context is salient to the animal. A dog may habituate
Habituation to a noise presented in one situation but may react when this is
presented at the same intensity in a new context (Leiner and Fendt,
The relative risk of habituation or sensitization will vary with 2011). This effect is influenced by the extent to which the “new”
characteristics of the stimulus, the personality of the dog, and the context is familiar or novel for rats. Behavioral responses reoccurred
state of the individual animal at the time of stimulus presentation. when a habituated stimulus was presented in a novel context, but
Controlling all these factors is important to minimize the chances of not when the animal was familiar with the context (Nyhuis et al.,
a working dog developing fear-associated behaviors. Habituation 2010). Prior habituation to environments in which stimuli will be
protocols are commonly used by working dog programs aiming to presented, such as introducing dogs to the environments in which
introduce dogs to stimuli to which they will be exposed when potentially frightening stimuli may occur, may aid with the process
working. of habituation and help prevent fears developing. Many working
Evolutionarily relevance (e.g., Mineka and Ohman, 2002), sud- and performance dog organizations do not use this gradual
denness (Trimmer et al., 2008), predictability (Schalke et al., 2007), approach. Initial greyhound schooling generally happens in an
intensity (Winslow et al 2002), frequency of exposure of the unfamiliar location, in the presence of new people, and dogs may
stimulus (Gotz and Janik, 2011), the ability of the animal to control have been transported in a new vehicle to the schooling location.
60 N.J. Rooney et al. / Journal of Veterinary Behavior 16 (2016) 53e64

The presentation of numerous potential stressors simultaneously et al., 2010). Such associations may not be causal, and the advice
may lead to sensitization in some individuals (Rooney 2012; Cobb against comforting fearful dogs has been challenged because the
et al., 2015). Working dog programs often use screening tests reinforcement may be of the coping response rather than the fear
which present stimuli at full intensity. When adult dogs are pro- itself (Casey, 2013). Calm, informed, and diligent handlers and
cured from different sources, they may have widely different trainers are critical to any effective fear-reduction program.
background experiences. Dogs that have previously learned a fear
response may display their learned response at a very low level of Introduction of puppies to potential stressors sensitive period of
stimulus presentation. For others, test scenarios may be entirely learning (“socialization period”)
novel and potentially risk sensitization due to exposure to multiple
novel stimuli in a novel environment. Pretesting with gradual ex- In programs that breed or rear puppies, appropriate early
posures to ascertain the levels to which dogs in the population introduction to potential stressors is important. The period of
respond for each potential stressor is important. development and maturation of senses lasts until about 12-
14 weeks, when puppies become more independent. This is an
Social context affecting fear responses important time of enhanced synaptic plasticity, where exposure to
environmental stimuli has a profound influence on later behavior
Conspecifics (Casey and Bradshaw, 2008). Using this period to ensure that
The potential for dogs to be influenced in their development of puppies have had positive experiences of stimuli and situations
fear by the presence and behavior of other dogs is important. This they are likely to come across in their adult lives is commonly
has implications both for the context in which dogs should be acknowledged to reduce the risk of fear-related behaviors in com-
tested for their propensity to exhibit fear and anxiety, and for the panion (Appleby et al., 2002; Howell and Bennett, 2011) and lab-
conditions under which dogs should be introduced and habituated oratory (Boxall et al., 2004) dogs. Dogs should be introduced to the
to potentially fear-inducing stimuli. It is commonly reported that if types of situations and stimuli they will encounter in adult life
a dog first encounters a new stimulus in the presence of a fearful before 3 months of age (preferably by 8 weeks and certainly no later
dog, it is more likely to develop fear itself (e.g., Landsberg et al., than 12 weeks; Scott and Fuller, 1965). Puppies are curious about
2012). Introduction in the presence of a previously conditioned novel situations, but they can readily develop fear behaviors early in
and calm dog may reduce the likelihood of a fearful response. their exposure periods. Studies on research dogs have shown that
Trainers use the presence of calm unreactive conspecifics as a handling for 3 minutes per day and exposure to stressors (e.g.,
means of reducing fear in “nervous” animals, but the potential for changes in ambient temperature, different flooring, different han-
using a calm “demonstrator” dog in working scenarios needs to be dlers) in a manner that gradually increases in intensity and duration
evaluated. has positive effects on resistance to disease, emotional reactivity,
and problem solving (Meunier, 2006). Gazzano et al. (2008) re-
Human contact ported that well-handled puppies of various breeds were calmer.
Presentation of video images of animate (e.g., people, dogs) and
Human interaction during stressful events can also exert a inanimate (e.g., traffic, vacuum cleaner) stimuli to puppies was
calming effect. Twenty minutes of gentle stroking inhibited the associated with a reduction in later fear behaviors (Pluijmakers
immediate increase of cortisol during a venipuncture procedure et al., 2010). Such potential interventions can be explored in
(Hennessy et al., 1998). Humans generally have greater success at working dog rearing programs.
inhibiting stress responses to a novel environment in dogs than do Many working dog breeding establishments (e.g., USA Transport
familiar dog companions (Tuber et al., 1996). Security Administration; Thomas, 2011) use this sensitive period of
Some human interaction can be detrimental and increase the development to introduce dogs to a variety of stimuli including
likelihood of fears developing. The saying that fear “travels down other animals, people, children, noises, slippery surfaces, and un-
the lead” acknowledges that anxious owners and handlers can in- stable floors. When considering socialization programs and expo-
crease the likelihood of dogs reacting fearfully. Levels of cortisol sure to potentially frightening stimuli, it is important to control
increased in agility dogs when their male owners became angry exposure and the level of stimulus, increasing intensity gradually to
after losing a competition (Jones and Josephs, 2006). Inexperienced avoid sensitization and inadvertent creation of anxiety or fear re-
owners were more likely to describe their dogs as showing fear of sponses. Gradual habituation to an indoor crate, followed by an
traffic, loud noises, and other dogs (Jagoe and Serpell, 1996), sug- outdoor kennel environment, reduced physiological stress levels
gesting that fear and anxiety may result from owners lacking the when search dogs entered military training kennels (Rooney et al.,
knowledge to respond in an appropriate and helpful way. Dogs may 2007a). As risk of sensitization is increased in animals experiencing
also be influenced by the behavior and personality of their owner. concurrent stress, the experience of kenneling, handling, and
Tense and emotionally less stable owners may be more likely to enrichment also needs to be addressed.
own aggressive dogs (Podberscek and Serpell, 1997). Aggression in Puppy socialization classes are often used to exposure pet or
dogs may be associated with fear, so it is possible that owner per- companion dogs to stimuli which commonly cause fear reactions in
sonality affects the way the person behaves toward and interacts adult dogs. Stimuli may include social situations, fireworks and
with their dog, which may affect the dog’s propensity to be fearful thunder (Blackwell et al., 2013), and urban noises such as engines
(Podberscek and Gosling, 2000). Dreschel and Granger (2005) (Sherman and Mills, 2008). Population-based studies have had
noted that owners scoring highly for anger/hostility, depression/ produced mixed results about the potential benefit of such classes
dejection, and fatigue were less likely to interact with their fearful on later behavior. Four weekly puppy socialization classes were
dog during a simulated thunderstorm, although there were no successful in training companion puppies but produced no signifi-
significant effects of owner behavior on the dogs’ behaviour. cant change in responses to social stimuli 4-6 months later (Seksel
Interaction with dogs during fearful episodes has not been tradi- et al., 1999). Similarly, 5 socialization sessions did not affect the
tionally recommended as it may inadvertently reward and thus success rate of guide dog puppies (Batt et al., 2008). However, large
reinforce fearful responses. A survey of dog owners in New Zealand scale population surveys have identified positive effects, and dogs
found an association between owners comforting their dogs and that attended puppy socialization classes were less likely to be re-
increased severity and duration of fear behavior over time (Dale ported to show undesirable reactions to other dogs (Blackwell et al.,
 N.J. Rooney et al. / Journal of Veterinary Behavior 16 (2016) 53e64 61

2008). Attending puppy classes was associated with a protective fear-eliciting stimulus at an initially low level, and positively
effect against owner-reported aggression (Casey et al., 2014). The rewarding the animal for showing an alternative (calm) response to
methods used in these classes are variable and the extent to which that shown previously, are vital.
they may contribute to reducing fear will depend on stimuli pre-
sentation method and attentiveness to the dog’s behavioral Conclusions
responses.
There have been several studies on early-life experience in Propensity to show anxiety and specific fear responses results
working dogs. Goddard and Beilharz (1984) examined fearfulness from an interplay of individual differences in animals and learning
and activity/distraction in 102 potential Guide Dogs. When the throughout life. Because the development of fearful behavior is a
quality of puppy-walking experiences was rated and compared to major reason for working dog failures, attention to methods likely
later behavior, the most significant correlations were between to minimize fear in working populations is critical. Programs should
high-quality puppy walking and decreased fear of unusual objects strive for optimal and improved efficiency to reduce the wastage of
(Goddard and Beilharz, 1985). Rooney et al. (2003) found that dogs. Program managers should continually analyze the value of
compliance of puppy walkers with a program of introduction to each component of their program, for puppies and adult dogs, to
new experiences was a major factor in determining the later suc- seek evidence for its value and explore potential evidence-based
cess of specialist search dogs. Programs that provide gradual, early improvements. We have discussed valuable techniques already
introduction to stimuli for working dogs, combined with optimal used and suggested important areas for future research effort.
weaning, may be beneficial and should be investigated further. Play The development of fearful behavior has some heritable
and relaxed social interactions provide ideal contexts for puppies to component, but the environment and past learning also have ef-
encounter stimuli and learn that they are not threatening. Slabbert fects. Identification of characteristics which reliably predict resil-
and Rasa (1997) used observational learning to demonstrate that ience to stress, careful breeding for these traits, the derivation of
pups, who were allowed to stay with their mothers and observe predictive tests for puppies and procured animals, rearing animals
them in a search and retrieve task, were better at completing the in optimal environments, and introducing them to a range of
same task (without reinforcement) than nonexposed pups at stimuli in a positive, controlled, and gradual way can help minimize
6 months. The behavior of the mother could potentially be very the number of dogs which develop work-inhibiting fears. Future
powerful in influencing the behavior of her offspring and may be a research should explore innovative methods of best measuring the
potential area for research in the reduction of fear responses. relative resilience of dogs to stressful events and develop optimal
The number of potential stressors is great in working environ- protocols to enhance such resilience.
ments. For example, search and rescue or military search dogs may
be exposed to explosions in which loud noise, shock waves, and
Acknowledgments
dust are experienced simultaneously. Little evidence exists as to the
optimal timing of stimulus exposure in early life, whether com-
The authors would like to thank The Defence Science Technol-
posite stimuli need to be broken into their component parts and
ogy Laboratory (Dstl) for funding the initial work on which this
separately presented, or whether puppies will tolerate combined
study is based (Contract number Dstlx 1000059070). Rachel Casey’s
stimuli at low intensity. Because of the importance of this period in
research time during article revision generously funded by Dogs
influencing adult life across species (Casey and Bradshaw, 2008), we
Trust.
can be confident that controlled exposure will be beneficial.
The article was initially prepared by N. Rooney with significant
Agencies which breed puppies for working roles should carefully
input into academic content, writing, and editing from both C. Clark
consider policy in this area, and those which use regular suppliers
and R. Casey.
should encourage gradual controlled exposure.

Conflict of interest
Treatment

The authors declare that there are no conflicts of interest

Following evidence-based selection criteria, manipulating the
involving any of the authors and this work. Rachel Casey has started
living environment, and providing opportunities for learning will
working at the UK charity Dogs Trust since the submission of this
help to minimize the number of working dogs which develop fears
article.
and anxiety. Some fear responses remain inevitable when animals
are working and training in unpredictable and potentially
dangerous environments. Most of the fear-related behaviors in USA References
military working dogs were reported to be acquired as adult dogs
Aisa, B., Tordera, R., Lasheras, B., Del Río, J., Ramírez, M.J., 2007. Cognitive impair-
(Burghardt, 2003). There is value to developing effective treatment ment associated to HPA axis hyperactivity after maternal separation in rats.
protocols for dogs showing fear responses -for animals that Psychoneuroendocrinology 32, 256e266.
demonstrate preexisting fear responses at procurement, before Appleby, D.L., Bradshaw, J.W.S., Casey, R.A., 2002. Relationship between aggressive
and avoidance behaviour by dogs and their experience in the first six months of
training that may then interfere with ability in training and for dogs life. Vet. Rec. 150, 434e438.
already in training, in service or returning from operations, which Arhant, C., Bubna-Littitz, H., Bartels, A., Futschik, A., Troxler, J., 2010. Behaviour of
have developed fear responses. Any treatment should include a full smaller and larger dogs: effects of training methods, inconsistency of owner
behaviour and level of engagement in activities with the dog. Appl. Anim.
medical and behavioral workup of the animal to ensure there is no Behav. Sci. 123, 131e142.
underlying medical condition. This examination should be followed Arvelius, P., Eken Asp, H., Fikse, W.F., Strandberg, E., Nilsson, K., 2014. Genetic
by investigation of stimuli that elicit and maintain the dog’s fear analysis of a temperament test as a tool to select against everyday life fear-
fulness in Rough Collie. J. Anim. Sci. 92 (11), 4843e4855.
response and a decision about how best to restore the animal’s
Arvelius, P., Strandberg, E., Fikse, W.F., 2014. The Swedish Armed Forces tempera-
well-being. Such investigations may lead to some dogs ending their ment test gives information on genetic differences among dogs. J. Vet. Behav:
working career, but many dogs may be able to continue working Clin. Appl. Res. 9 (6), 281e289.
much longer than if they were untreated. Behavior modification Asher, L., Blythe, S., Roberts, R., Toothill, L., Craigon, P.J., Evans, K.M., Green, M.J.,
England, G.C.W., 2013. A standardized behavior test for potential guide dog
programs based on desensitization and counter-conditioning (e.g., puppies: methods and association with subsequent success in guide dog
Levine et al., 2007), a combination of presenting an animal with the training. J. Vet. Behav: Clin. Appl. Res. 8, 431e438.
62 N.J. Rooney et al. / Journal of Veterinary Behavior 16 (2016) 53e64

Batt, L., Batt, M., Baguley, J., McGreevy, P., 2010. Relationships between puppy Davis, M., 1974. Sensitization of rat startle response by noise. J. Comp. Physiol.
management practices and reported measures of success in guide dog training. Psychol. 87, 571e581.
J. Vet. Behav: Clin. Appl. Res. 5, 240e246. de Boer, S.F., van der Vegt, B.J., Koolhaas, J.M., 2003. Individual variation in
Batt, L.S., Batt, M.S., Baguley, J.A., McGreevy, P.D., 2008. Factors associated with aggression of feral rodent strains: a standard for the genetics of aggression and
success in guide dog training. J. Vet. Behav: Clin. Appl. Res. 3, 143e151. violence? Behav. Genet. 33, 485.
Battaglia, C.L., 2009. Periods of early development and the effects of stimula- De Meester, R.H., Pluijmakers, J., Vermeire, S., Laevens, H., 2011. The use of the so-
tion and social experiences in the canine. J. Vet. Behav: Clin. Appl. Res. 4, cially acceptable behavior test in the study of temperament of dogs. J. Vet.
203e210. Behav: Clin. Appl. Res. 6, 211e224.
Benetti, F., de Araujo, P.A., Sanvitto, G.L., Lucion, A.B., 2007. Effects of neonatal Dodic, M., Hantzis, V., Duncan, J., Rees, S., Koukoulas, I., Johnson, K., Wintour, E.M.,
novelty exposure on sexual behavior, fear, and stress-response in adult rats. Moritz, K., 2002. Programming effects of short prenatal exposure to cortisol.
Dev. Psychobiol. 49, 258e264. FASEB J. 16, 1017e1026.
Bennett, P.C., Rohlf, V.I., 2007. Owner-companion dog interactions: relationships Dreschel, N.A., 2010. The effects of fear and anxiety on health and lifespan in pet
between demographic variables, potentially problematic behaviours, training dogs. Appl. Anim. Behav. Sci. 125, 157e162.
engagement and shared activities. Appl. Anim. Behav. Sci. 102, 65e84. Dreschel, N.A., Granger, D.A., 2005. Physiological and behavioral reactivity to stress
Bijlsma, E.Y., de Jongh, R., Olivier, B., Groenink, L., 2010. Fear-potentiated startle, but in thunderstorm-phobic dogs and their caregivers. Appl. Anim. Behav. Sci. 95,
not light-enhanced startle, is enhanced by anxiogenic drugs. Pharm. Biochem. 153e168.
Behav. 96, 24e31. Ennaceur, A., Michalikova, S., Chazot, P.L., 2006. Models of anxiety: responses of rats
Blackwell, E.J., Bodnariu, A., Tyson, J., Bradshaw, J.W.S., Casey, R.A., 2010. Rapid to novelty in an open space and an enclosed space. Behav. Brain Res. 171, 26e49.
shaping of behaviour associated with high urinary cortisol in domestic dogs. Fabricius, K., Wörtwein, G., Pakkenberg, B., 2008. The impact of maternal separation
Appl. Anim. Behav. Sci. 124, 113e120. on adult mouse behaviour and on the total neuron number in the mouse hip-
Blackwell, E., Bradshaw, J., Casey, R., 2013. Fear responses to noises in domestic pocampus. Brain Struct. Funct. 212, 403e441.
dogs: prevalence, risk factors and co-occurrence with other fear related Fisher, G.T., Volhard, W., 1985. Puppy Personality Profile: The Specifics of Testing
behaviour. Appl. Anim. Behav. Sci. 145, 15e25. Procedures, Scoring, and Interpretation of the Results of PAT, Purebred Dog
Blackwell, E.J., Twells, C., Seawright, A., Casey, R.A., 2008. The relationship between American Kennel Club Gazette. The Kennel Club Publisher, London, pp. 36e42.
training methods and the occurrence of behavior problems, as reported by owners, Forkman, B., Furuhaug, I.L., Jensen, P., 1995. Personality, coping patterns and
in a population of domestic dogs. J. Vet. Behav: Clin. Appl. Res. 3, 207e217. aggression in piglets. Appl. Anim. Behav. Sci. 45, 31e42.
Boissy, A., 1998. Fear and fearfulness in determining behavior. In: Grandin, T. (Ed.), Foyer, P., Svedberg, A.M., Nilsson, E., Wilsson, E., Faresjö, Å., Jensen, P., 2016.
Genetics and the Behavior of Domestic Animals. Academic Press, New York, Behavior and Cortisol Responses of Dogs Evaluated in a Standardized Temper-
pp. 67e111. ament Test for Military Working Dogs: 4th Canine Science Forum and 1st Feline
Bosch, O.J., Müsch, W., Bredewold, R., Slattery, D.A., Neumann, I.D., 2007. Prenatal Science Forum Lincoln. UK Journal of Veterinary Behvaior-Clinical Applications
stress increases HPA axis activity and impairs maternal care in lactating female and Research, 11, 7e12.
offspring: implications for postpartum mood disorder. Psychoneur- Fratkin, J.L., Sinn, D.L., Patall, E.A., Gosling, S.D., 2013. Personality consistency in
oendocrinology 32, 267e278. dogs: a meta-analysis. PLos One 8, e54907.
Boxall, J., Heath, S., Bate, S., Brautigam, J., 2004. Modern concepts of socialization for Gaines, S., 2008. Kennelled Dog WelfaredEffects of Housing and Husbandry, PhD
dogs: implications for their behaviour, welfare and use in scientific procedures. Thesis University of Bristol. Available at: http://research-information.
Altern. Lab. Anim. 32, 81e93. bristol.ac.uk/files/34503545/492636.pdf.
Bradshaw, J.W.S., Blackwell, E.J., Casey, R.A., 2009. Dominance in domestic dogs- Gaines, S.A., Rooney, N.J., Bradshaw, J.W.S., 2008. The effect of feeding enrichment
useful construct or bad habit? J. Vet. Behav: Clin. Appl. Res. 4, 135e144. upon reported working ability and behavior of kenneled working dogs.
Branson, N.J., Rogers, L.J., 2006. Relationship between paw preference strength and J. Forensic Sci. 53, 1400e1404.
noise phobia in Canis familiaris. J. Comp. Psychol. 120, 176e183. Gazzano, A., Mariti, C., Notari, L., Sighieri, C., McBride, E.A., 2008. Effects of early
Brown, J., 2011. Developing the Disaster Search Dog, Defining, Developing and gentling and early environment on emotional development of puppies. Appl.
Documenting Success in Working Dogs. Pearl River, New York. Anim. Behav. Sci. 110, 294e304.
Burghardt, W.F., 2003. Behavioral considerations in the management of working Goddard, M.E., Beilharz, R.G., 1986. Early prediction of adult behaviour in potential
dogs. Vet. Clin. North Am. Small Anim. Pract. 33, 417e446. guide dogs. Appl. Anim. Behav. Sci. 15, 247e260.
Caron-Lormier, G., Harvey, N.D., England, G.C., Asher, L., 2016. Using the incidence Goddard, M.E., Beilharz, R.G., 1985. A multivariate analysis of the genetics of fear-
and impact of behavioural conditions in guide dogs to investigate patterns in fulness in potential guide dogs. Behav. Genet. 15, 69e89.
undesirable behaviour in dogs. Sci. Rep. 6, 23860. Goddard, M.E., Beilharz, R.G., 1984. A factor analysis of fearfulness in potential guide
Casey, R., 2013. Should Fearful Dogs Be Comforted on Fireworks Night? Reigning dogs. Appl. Anim. Behav. Sci. 12, 253e265.
Cats and Dogs: A Scientific Perspective on Companion Animal Behaviour and Goddard, M.E., Beilharz, R.G., 1984. The relationship of fearfulness to, and the effects
Welfare, by Veterinary Behaviourist Dr Rachel Casey. Available at: https:// of, sex, age and experience on exploration and activity in dogs. Appl. Anim.
behaviourvet.wordpress.com/2013/11/04/should-fearful-dogs-be-comforted- Behav. Sci. 12, 267e278.
on-fireworks-night/. Accessed August 16, 2015. Goddard, M.E., Beilharz, R.G., 1982. Genetic and environmental factors affecting the
Casey, R., 2010. In: Lindley, S., Watson, P. (Eds.), BSAVA Manual of Canine and Feline suitability of dogs as Guide Dogs for the Blind. Theor. Appl. Genet. 62, 97e102.
Rehabilitation, Supportive and Palliative Care: Case Studies in Patient Man- Gotz, T., Janik, V., 2011. Repeated elicitation of the acoustic startle reflex leads to
agement. British Small Animal Veterinary Association, Gloucester, UK. sensitization in subsequent avoidance behaviour and induces fear conditioning.
Casey, R.A., Bradshaw, J.W.S., 2008. The effects of additional socialization for kittens BMC Neurosci. 12, 30.
in a rescue centre on their behaviour and suitability as a pet. Appl. Anim. Behav. Grandin, T., Deesing, M., 2002. Distress in Animals: Is it Fear, Pain or Physical Stress?
Sci. 114, 196e205. American Board of Veterinary Practitioners, Manhattan Beach, California, USA.
Casey, R., Loftus, B., Bolster, C., Richards, G., Blackwell, E., 2014. Human directed Grant, K.A., McMahon, C., Austin, M.P., Reilly, N., Leader, L., Ali, S., 2009. Maternal
aggression in domestic dogs (Canis familiaris): occurrence in different contexts prenatal anxiety, postnatal caregiving and infants’ cortisol responses to the still-
and risk factors. Appl. Animal Behav. Sci. 152, 52e63. face procedure. Dev. Psychobiol 51, 625e637.
Champness, K.A., 1996. Development of a Breeding Program for Drug Detector Gray, J., 1971. The Psychology of Fear and Stress. McGraw Hill, New York.
DogsdBased on Studies of a Breeding Population of Guide Dogs, PhD Thesis Grissom, N., Bhatnagar, S., 2009. Habituation to repeated stress: get used to it.
University of Melbourne. Available at: https://minerva-access.unimelb.edu.au/ Neurobiol. Learn. Mem. 92, 215e224.
handle/11343/39395. Gruen, M.E., Case, B.C., Foster, M.L., Lazarowski, L., Fish, R.E., Landsberg, G.,
Christensen, J.W., Rundgren, M., Olsson, K., 2006. Training methods for horses: Depuy, V., Dorman, D.C., Sherman, B.L., 2015. The use of an open-field model to
habituation to a frightening stimulus. Equine Vet. J. 38, 439e443. assess sound-induced fear and anxiety-associated behaviors in Labrador re-
Cobb, M., Branson, N., McGreevy, P., Bennett, P., Rooney, N., Magdalinski, T., trievers. J. Vet. Behav: Clin. Appl. Res. 10, 338e345.
Howell, T., Dawson, K., 2015. Review & Assessment of Best Practice Rearing, Grundy, S.A., Feldman, E., Davidson, A., 2002. Evaluation of infertility in the bitch.
Socialization, Education and Training Methods for Greyhounds in a Racing Clin. Tech. Small Anim. Pract. 17, 108e115.
Context. Report to Greyhound Racing New South Wales. Available at: http:// Haverbeke, A., De Smet, A., Depiereux, E., Giffroy, J.M., Diederich, C., 2009. Assessing
workingdogalliance.com.au/about/publications/. undesired aggression in military working dogs. Appl. Anim. Behav. Sci. 117, 55e62.
Concannon, P.W., Butler, W.R., Hansel, W., Knight, P.J., Hamilton, J.M., 1978. Partu- Haverbeke, A., Laporte, B., Depiereux, E., Giffroy, J.M., Diederich, C., 2008. Training
rition and lactation in the bitch: serum progesterone, cortisol and prolactin. methods of military dog handlers and their effects on the team’s performances.
Biol. Reprod. 19, 1113e1118. Appl. Anim. Behav. Sci. 113, 110e122.
Coppola, C.L., Grandin, T., Enns, R.M., 2006. Human interaction and cortisol: can Haverbeke, A., Messaoudi, F., Depiereux, E., Stevens, M., Giffroy, J.M., Diederich, C.,
human contact reduce stress for shelter dogs? Physiol. Behav. 87, 537e541. 2010. Efficiency of working dogs undergoing a new Human Familiarization and
D’Eath, R.B., Conington, J., Lawrence, A.B., Olsson, I.A.S., Sandoe, P., 2010. Breeding Training Program. J. Vet. Behav: Clin. Appl. Res. 5, 112e119.
for behavioural change in farm animals: practical, economic and ethical con- Hayward, J.J., Castelhano, M.G., Oliveira, K.C., Corey, E., Balkman, C., Baxter, T.L.,
siderations. Anim. Welf. 19, 17e27. Casal, M.L., Center, S.A., Fang, M., Garrison, S.J., Kalla, S.E., Korniliev, P.,
Dale, A.R., Walker, J.K., Farnworth, M.J., Morrissey, S.V., Waran, N.K., 2010. A survey Kotlikoff, M.I., Moise, N.S., Shannon, L.M., Simpson, K.W., Sutter, N.B.,
of owners’ perceptions of fear of fireworks in a sample of cats and dogs in New Todhunter, R.J., Boyko, A.R., 2016. Complex disease and phenotype mapping in
Zealand. N. Z. Vet. J. 58, 286e291. the domestic dog. Nat. Commun. 7, 10460.
 N.J. Rooney et al. / Journal of Veterinary Behavior 16 (2016) 53e64 63

Heilig, M., 2004. The NPY system in stress, anxiety and depression. Neuropeptides Levine, E.D., Ramos, D., Mills, D.S., 2007. A prospective study of two self-help CD
38, 213e224. based desensitization and counter-conditioning programs with the use of Dog
Hellemans, K.G.C., Sliwowska, J.H., Verma, P., Weinberg, J., 2010. Prenatal alcohol Appeasing Pheromone for the treatment of firework fears in dogs (Canis
exposure: fetal programming and later life vulnerability to stress, depression familiaris). Appl. Anim. Behav. Sci. 105, 311e329.
and anxiety disorders. Neurosci. Biobehav. Rev. 34, 791e807. Lin, H.P., Lin, H.Y., Lin, W.L., Huang, A.C.W., 2011. Effects of stress, depression, and
Hennessy, M.B., Morris, A., Linden, F., 2006. Evaluation of the effects of a socializ- their interaction on heart rate, skin conductance, finger temperature, and res-
ation program in a prison on behavior and pituitary-adrenal hormone levels of piratory rate: sympathetic-parasympathetic hypothesis of stress and depres-
shelter dogs. Appl. Anim. Behav. Sci. 99, 157e171. sion. J. Clin. Psychol. 67, 1080e1091.
Hennessy, M.B., Williams, M.T., Miller, D.D., Douglas, C.W., Voith, V.L., 1998. Influ- Lippmann, M., Bress, A., Nemeroff, C.B., Plotsky, P.M., Monteggia, L.M., 2007. Long-
ence of male and female petters on plasma cortisol and behaviour: can human term behavioural and molecular alterations associated with maternal separa-
interaction reduce the stress of dogs in a public animal shelter? Appl. Anim. tion in rats. Eur. J. Neurosci. 25, 3091e3098.
Behav. Sci. 61, 63e77. Lissek, S., Powers, A.S., McClure, E.B., Phelps, E.A., Woldehawariat, G., Grillon, C.,
Hiby, E.F., Rooney, N.J., Bradshaw, J.W.S., 2004. Dog training methods: their use, Pine, D.S., 2005. Classical fear conditioning in the anxiety disorders: a meta-
effectiveness and interaction with behaviour and welfare. Anim. Welf. 13, 63e69. analysis. Behav. Res. Ther. 43, 1391e1424.
Hoffmann, G., Blackshaw, J.K., Smith, G.A., 1995. Puppy Tests: Intercorrelations and Loftus, B.A., Rooney, N.J., Casey, R.A., 2012. Recognising Fear and Anxiety in Dogs.
Test-retest Reliability, Proceedings of the 7th International Conference of Available at: http://www.bris.ac.uk/vetscience/services/behaviour-clinic/dog-
Human-animal Interactions, Geneva. behaviouralsigns/. Accessed September 10, 2016.
Holden, M.D., Gregory, J., Watkins, V., Radford, L., 2006. Operant-conditioning Mackenzie, S.A., Oltenacu, E.A.B., Leighton, E., 1985. Heritability estimate for
Program for White Rhinoceros, Black Rhinoceros and Indian or Greater One- temperament scores in German Shepherd dogs and its genetic correlation with
horned Asian Rhinoceros Ceratotherium simum, Diceros bicornis and Rhinoc- hip-displasia. Behav.Genet. 15, 475e482.
eros Unicornis at Whipsnade Wild Animal Park. International Zoo Yearbook 40, Macrì, S., Würbel, H., 2006. Developmental plasticity of HPA and fear responses in
Dunstable, UK, pp. 144e149. rats: a critical review of the maternal mediation hypothesis. Horm. Behav. 50,
Horvath, Z., Igyarto, B.Z., Magyar, A., Miklosi, A., 2007. Three different coping styles 667e680.
in police dogs exposed to a short-term challenge. Horm. Behav. 52, 621e630. Macri, S., Wurbel, H., 2007. Effects of variation in postnatal maternal environment
Houpt, K.A., Hintz, H.F., 1983. Some effects of maternal-deprivation on maintenance on maternal behaviour and fear and stress responses in rats. Anim. Behav. 73,
behavior, spatial relationships and responses to environmental novelty in foals. 171e184.
Appl. Anim. Ethol. 9, 221e230. Macri, S., Granstrem, O., Shumilina, M., dos Santos, F., Berry, A., Saso, L., Laviola, G.,
Howell, T.J., Bennett, P.C., 2011. Puppy power! Using social cognition research tasks 2009. Resilience and vulnerability are dose-dependently related to neonatal
to improve socialization practices for domestic dogs (Canis familiaris). J. Vet. stressors in mice. Horm. Behav. 56, 391e398.
Behav: Clin. Appl. Res. 6, 195e204. Macri, S., Laviola, G., Leussis, M.P., Andersen, S.L., 2010. Abnormal behavioral and
Hsu, Y.Y., Serpell, J.A., 2003. Development and validation of a questionnaire for neurotrophic development in the younger sibling receiving less maternal care
measuring behavior and temperament traits in pet dogs. J. Am. Vet. Med. Assoc. in a communal nursing paradigm in rats. Psychoneuroendocrinology 35,
223, 1293. 392e402.
Hsu, Y.Y., Sun, L.C., 2010. Factors associated with aggressive responses in pet dogs. Macri, S., Zoratto, F., Laviola, G., 2011. Early-stress regulates resilience, vulnerability
Appl. Animal Behav. Sci. 123, 108e123. and experimental validity in laboratory rodents through mother-offspring
Imanaka, A., Morinobu, S., Toki, S., Yamamoto, S., Matsuki, A., Kozuru, T., hormonal transfer. Neurosci. Biobehav. Rev. 35, 1534e1543.
Yamawaki, S., 2008. Neonatal tactile stimulation reverses the effect of neonatal Malinowski, K., Hallquist, N.A., Helyar, L., Sherman, A.R., Scanes, C.G., 1990. Effect of
isolation on open-field and anxiety-like behavior, and pain sensitivity in male separation protocols between mares and foals on plasma cortisol and cell-
and female adult Sprague-Dawley rats. Behav. Brain Res. 186, 91e97. mediated immune response. J. Equine Vet. Sci. 10, 363.
Jagoe, A., Serpell, J., 1996. Owner characteristics and interactions and the prevalence Manteuffel, G., Langbein, J., Puppe, B., 2009. From operant teaming to cognitive
of canine behaviour problems. Appl. Anim. Behav. Sci. 47, 31e42. enrichment in farm animal housing: bases and applicability. Anim. Welf. 18,
Jarvis, S., Moinard, C., Robson, S.K., Baxter, E., Ormandy, E., Douglas, A.J., Seckl, J.R., 87e95.
Russell, J.A., Lawrence, A.B., 2006. Programming the offspring of the pig by prenatal Mariti, C., Gazzano, A., Moore, J.L., Baragli, P., Chelli, L., Sighieri, C., 2012. Perception
social stress: neuroendocrine activity and behaviour. Horm. Behav. 49, 68e80. of dogs’ stress by their owners. J. Vet. Behav: Clin. Appl. Res. 7, 213e219.
Jensen, P., Rushen, J., Forkman, B., 1995. Behavioral strategies or just individual Marshall-Pescini, S., Barnard, S., Branson, N.J., Valsecchi, P., 2013. The effect of
variation in behaviourda lack of evidence for active and passive piglets. Appl. preferential paw usage on dogs’ (Canis familiaris) performance in a manipula-
Anim. Behav. Sci. 43, 135e139. tive problem-solving task. Behav. Process. 100, 40e43.
Jones, A.C., Gosling, S.D., 2005. Temperament and personality in dogs (Canis famil- Masini, C.V., Day, H.E.W., Campeau, S., 2008. Long-term habituation to repeated
iaris): a review and evaluation of past research. Appl. Anim. Behav. Sci. 95, 1e53. loud noise is impaired by relatively short interstressor intervals in rats. Behav.
Jones, A.C., Josephs, R.A., 2006. Interspecies hormonal interactions between man Neurosci. 122, 210e223.
and the domestic dog (Canis familiaris). Horm. Behav. 50, 393e400. Massar, S.A.A., Mol, N.M., Kenemans, J.L., Baas, J.M.P., 2011. Attentional bias in high-
Jordan, W.P., Strasser, H.C., 2000. Contextual control of long-term habituation in and low-anxious individuals: evidence for threat-induced effects on engage-
rats. J. Exp. Psychol. Anim. Behav. Process. 26, 323e339. ment and disengagement. Cogn. Emot. 25, 805e817.
Karagiannis, C.I., Burman, O.H., Mills, D.S., 2015. Dogs with separation-related prob- McCall, C.A., Potter, G.D., Kreider, J.L., 1985. Locomotor, vocal and other behav-
lems show a “less pessimistic” cognitive bias during treatment with fluoxetine ioural responses to varying methods of weaning foals. Appl. Anim. Behav. Sci.
(Reconcile (TM)) and a behaviour modification plan. BMC Vet. Res. 11, 1e10. 14, 27e35.
Kilgour, R., Foster, T.M., Temple, W., Matthews, L.R., Bremner, K.J., 1991. Operant McCall, C.A., Potter, G.D., Kreider, J.L., Jenkins, W.L., 1987. Physiological responses in
technology applied to solving farm animal problems. An assessment. Appl. foals weaned by abrupt or gradual methods. J. Equine Vet. Sci. 7, 368e374.
Anim. Behav. Sci. 30, 141e166. Memon, M.A., 2007. Common causes of male dog infertility. Theriogenology 68,
Knuth, E.D., Etgen, A.M., 2007. Long-term behavioral consequences of brief, 322e328.
repeated neonatal isolation. Brain Res. 1128, 139e147. Mendl, M., Brooks, J., Basse, C., Burman, O., Paul, E., Blackwell, E., Casey, R., 2010.
Koolhaas, J.M., Korte, S.M., De Boer, S.F., Van Der Vegt, B.J., Van Reenen, C.G., Dogs showing separation-related behaviour exhibit a ‘pessimistic’ cognitive
Hopster, H., De Jong, I.C., Ruis, M.A.W., Blokhuis, H.J., 1999. Coping styles in bias. Curr. Biol. 20, R839eR840.
animals: current status in behavior and stress-physiology. Neurosci. Biobehav. Meunier, L.D., 2006. Selection, acclimation, training, and preparation of dogs for the
Rev. 23, 925e935. research setting. ILAR J. 47, 326e347.
Kutzler, M.A., 2012. Canine Semen Collection and Management of Male Infertility, Mills, D., 2005. Management of noise fears and phobias in pets. Practice 27, 248e255.
Fifth Congreso Latinoamericano de Emergencias y Cuidados Intensivos, Mexico. Mills, D., Karagiannis, C., Zulch, H., 2014. Stress-its effects on health and behavior: a
Lambás-Señas, L., Mnie-Filali, O., Certin, V., Faure, C., Lemoine, L., Zimmer, L., guide for practitioners. Vet. Clin. North Am: Small Anim. Pract. 44, 525e541.
Haddjeri, H., 2009. Functional correlates for 5-HT(1A) receptors in maternally Mineka, S., Ohman, A., 2002. Born to fear: non-associative vs associative factors in
deprived rats displaying anxiety and depression-like behaviors Prog. Neuro- the etiology of phobias. Behav. Res. Ther. 40, 173e184.
psychopharmacol. Biol. Psychiatry 33, 262e268. Morgan, C.A., Southwick, S., Hazlett, G., Rasmusson, A., Hoyt, G., Zimolo, Z.,
Landsberg, G.M., Hunthausen, W.L., Ackerman, L.J., 2012. Behavior Problems of the Charney, D., 2004. Relationships among plasma dehydroepiandrosterone sulfate
Dog and Cat. Saunders Ltd, Edinburgh. and cortisol levels, symptoms of dissociation, and objective performance in
Latham, N.R., Mason, G.J., 2008. Maternal deprivation and the development of humans exposed to acute stress. Arch. Gen. Psychiatry 61, 819e825.
stereotypic behaviour. Appl. Anim. Behav. Sci. 110, 84e108. Mornement, K.M., Coleman, G.J., Toukhsati, S.R., Bennett, P.C., 2015. Evaluation of
Lefebvre, D., Diederich, C., Delcourt, M., Giffroy, J.M., 2007. The quality of the relation the predictive validity of the Behavioural Assessment for Re-homing K9’s
between handler and military dogs influences efficiency and welfare of dogs. (BARK) protocol and owner satisfaction with adopted dogs. Appl. Anim. Behav.
Appl. Anim. Behav. Sci. 104, 49e60. Sci. 167, 35e42.
Leiner, L., Fendt, M., 2011. Behavioural fear and heart rate responses of horses after expo- Morrow, M., Ottobre, J., Ottobre, A., Neville, P., St-Pierre, N., Dreschel, N., Pate, J.,
sure to novel objects: effects of habituation. Appl. Anim. Behav. Sci. 131, 104e109. 2015. Breed-dependent differences in the onset of fear-related avoidance
Levin, R., Nielsen, T.A., 2007. Disturbed dreaming, posttraumatic stress disorder, behavior in puppies. J. Vet. Behav: Clin. Appl. Res. 10 (4), 286e294.
and affect distress: a review and neurocognitive model. Psychol. Bull. 133, Murphree, O.D., Dykman, R.A., 1965. Litter patterns in the offspring of nervous and
482e528. stable dogs. 1. Behavioral-tests. J. Nerv. Ment. Dis. 141, 321e332.
Levine, S., 2000. Influence of psychological variables on the activity of the Murphy, J.A., 1995. Assessment of the temperament of potential guide dogs.
hypothalamic-pituitary-adrenal axis. Eur. J. Pharmacol. 405, 149e160. Anthrozoös 8, 224e228.
64 N.J. Rooney et al. / Journal of Veterinary Behavior 16 (2016) 53e64

Nyhuis, T.J., Sasse, S.K., Masini, C.V., Day, H.E.W., Campeau, S., 2010. Lack of Sherman, B.L., Mills, D.S., 2008. Canine anxieties and phobias: an update on sepa-
contextual modulation of habituated neuroendocrine responses to repeated ration anxiety and noise aversions. Vet. Clin. North Am: Small Anim. Pract. 38,
audiogenic stress. Behav. Neurosci. 124, 810e820. 1081e1106.
Odendaal, J.S.J., Meintjes, R.A., 2003. Neurophysiological correlates of affiliative Shors, T.J., 2004. Learning during stressful times. Learn. Mem. 11, 137e144.
behaviour between humans and dogs. Vet. J. 165, 296e301. Silver, R.C., Holman, E.A., McIntosh, D.N., Poulin, M., Gil-Rivas, V., 2002. Nationwide
Ogata, N., Kikusui, T., Takeuchi, Y., Mori, Y., 2006. Objective measurement of fear- longitudinal study of psychological responses to September 11. J. Am. Med.
associated learning in dogs. J. Vet. Behav: Clin. Appl. Res. 1, 55e61. Assoc. 288, 1235e1244.
Parker, K.J., Buckmaster, C.L., Sundlass, K., Schatzberg, A.F., Lyons, D.M., 2006. Siniscalchi, M., Bertino, D., Quaranta, A., 2014. Laterality and performance of agility-
Maternal mediation, stress inoculation, and the development of neuroendo- trained dogs. Laterality 19, 219e234.
crine stress resistance in primates. Proc. Natl. Acad. Sci. U. S. A. 103, 3000e Sinn, D.L., Gosling, S.D., Hilliard, S., 2010. Personality and performance in military
3005. working dogs: reliability and predictive validity of behavioral tests. Appl. Anim.
Pfaffenberger, C.J., Scott, J.P., 1976. Early rearing and testing. In: Pfaffenberger, C.J., Behav. Sci. 127, 51e65.
Scott, J.P., Fuller, J.L., Ginsburg, B.E., Bielfelt, S.W. (Eds.), Guide Dogs for the Blind: Slabbert, J.M., Odendaal, J.S.J., 1999. Early prediction of adult police dog efficiencyda
Their Selection, Development, and Training. Elsevier, Amsterdam, pp. 13e37. longitudinal study. Appl. Anim. Behav. Sci. 64, 269e288.
Pich, E.M., Agnati, L.F., Zini, I., Marrama, P., Carani, C., 1993. Neuropeptide-Y produces Slabbert, J.M., Rasa, O.A.E., 1997. Observational learning of an acquired maternal
anxiolytic effects in spontaneously hypertensive rats. Peptides 14, 909e912. behaviour pattern by working dog pups: an alternative training method? Appl.
Pluijmakers, J.J.T.M., Appleby, D.L., Bradshaw, J.W.S., 2010. Exposure to video images Anim. Behav. Sci. 53, 309e316.
between 3 and 5 weeks of age decreases neophobia in domestic dogs. Appl. Slabbert, J.M., Rasa, O.A.E., 1993. The effect of early separation from the mother on
Anim. Behav. Sci. 126, 51e58. pups in bonding to humans and pup health. J. S. Afr. Vet. Assoc. 64, 4e8.
Podberscek, A.L., Gosling, S.D., 2000. Personality research on pets and their owners: Strong, V., Brown, S.W., Walker, R., 1999. Seizure-alert dogsdfact or fiction? Seizure
conceptual issues and review. In: Podberscek, A.L., Paul, E.S., Serpell, J.A. (Eds.), 8, 62e65.
Companion Animals and Us: Exploring the Relationships between People and Svartberg, K., Forkman, B., 2002. Personality traits in the domestic dog (Canis
Pets. Cambridge University Press, Cambridge, pp. 143e167. familiaris). Appl. Anim. Behav. Sci. 79, 133e155.
Podberscek, A.L., Serpell, J.A., 1997. Aggressive behaviour in English cocker spaniels Svobodová, I., Vápeník, P., Pinc, L., Bartos, L., 2008. Testing german shepherd
and the personality of their owners. Vet. Rec. 141, 73e76. puppies to assess their chances of certification. Appl. Anim. Behav. Sci. 113,
Poore, K.R., Boullin, J.P., Cleal, J.K., Newman, J.P., Noakes, D.E., Hanson, M.A., 139e149.
Green, L.R., 2010. Sex- and age-specific effects of nutrition in early gestation and Tami, G., Gallagher, A., 2009. Description of the behaviour of domestic dog (Canis
early postnatal life on hypothalamo-pituitary-adrenal axis and sympathoa- familiaris) by experienced and inexperienced people. Appl. Anim. Behav. Sci.
drenal function in adult sheep. J. Physiol. 588, 2219e2237. 120, 159e169.
Reefmann, N., Kaszas, F.B., Wechsler, B., Gygax, L., 2009. Physiological expression of Tata, D.A., Markostamou, I., Ioannidis, A., Gkioka, M., Simeonidou, C.,
emotional reactions in sheep. Physiol. Behav. 98, 235e241. Anogianakis, G., Spandou, E., 2015. Effects of maternal separation on behavior
Reefmann, N., Wechsler, B., Gygax, L., 2009. Behavioural and physiological assess- and brain damage in adult rats exposed to neonatal hypoxia-ischemia. Behav.
ment of positive and negative emotion in sheep. Anim. Behav. 78, 651e659. Brain Res. 280, 51e61.
Rooney, N.J., 2012. Welfare of Racing GreyhoundsdPrioritisation of Issues. Poster Taylor, K.D., Mills, D.S., 2006. The development and assessment of temperament
Presented at Universities Federation for Animal Welfare Portsmouth UK. tests for adult companion dogs. J. Vet. Behav: Clin. Appl. Res. 1, 94e108.
Rooney, N.J., Almney, H.A., Bradshaw, J.W.S., 2004. Attributes of specialist search Terlouw, E.M.C., Schouton, W.G.P., Ladewig, P., 1997. Physiology. In: Appleby, M.C.,
dogsda questionnaire survey of UK dog handlers and trainers. J. Forensic Sci. 49 Hughes, B.O. (Eds.), Anim. Welf. CAB International, Wallingford.
(2), 300e306. Thomas, S., 2011. Development and Epigeneticsdthe New Nature-nurture Discus-
Rooney, N., Bradshaw, J.W.S., Almey, H.A., 2002. Specialist Search Dogs: An Inter- sion, Defining, Developing and Documenting Success in Working Dogs. Pearl
agency Review and Critique of Selection, Report to DERA. River, New York.
Rooney, N., Bradshaw, J.W.S., Gaines, S., 2003. Investigation Into the Effects of Trimmer, P.C., Houston, A.I., Marshall, J.A.R., Bogacz, R., Paul, E.S., Mendl, M.T.,
Rearing Conditions on the Ability of Specialist Search Dogs, Report to Defence McNamara, J.M., 2008. Mammalian choices: combining fast-but-inaccurate and
Science and Technology Laboratory, pp. 1e229. slow-but-accurate decision-making systems. Proc. Biol. Sci. 275, 2353e2361.
Rooney, N.J., Cowan, S., 2011. Training methods and owner-dog interactions: Tuber, D.S., Sanders, S., Hennessy, M.B., Miller, J.A., 1996. Behavioral and glucocor-
links with dog behaviour and learning ability. Appl. Anim. Behav. Sci. 132, ticoid responses of adult domestic dogs (Canis familiaris) to companionship and
169e177. social separation. J. Comp. Psychol. 110, 103e108.
Rooney, N.J., Gaines, S.A., Bradshaw, J.W.S., 2007a. Behavioural and glucocorticoid Valentiner, D.P., Holahan, C.J., Moos, R.H., 1994. Social support, appraisals of event
responses of dogs (Canis familiaris) to kennelling: Investigating mitigation of controllability, and coping: An integrative model. J. Pers. Soc. Psychol 66,
stress by prior habituation. Physiol. Behav. 92, 847e854. 1094e1102.
Rooney, N., Gaines, S., Hiby, E., 2009. A practitioner’s guide to working dog welfare. Vincent, I.C., Leahy, R.A., 1997. Real-time non-invasive measurement of heart rate in
J. Vet. Behav: Clin. Appl. Res. 4, 127e134. working dogs: a technique with potential applications in the objective assess-
Rooney, N.J., Morant, S., Guest, C., 2013. Investigation into the value of trained ment of welfare problems. Vet. J. 153, 179e183.
glycaemia alert dogs to clients with type I diabetes. PLoS One 8 (8), e69921. Walker, J., Waran, N., Phillips, C., 2014. The effect of conspecific removal on the
Rooney, N.J., Paul, E.S., Haig-Ferguson, A.J., Bradshaw, J.W.S., 2007b. Human Factors behaviour and physiology of pair-housed shelter dogs. Appl. Anim. Behav. Sci.
Affecting the Performance of Dog-handler Teams, Report to Defence Science 158, 46e56.
and Technology Laboratory. Wells, D.L., Hepper, P.G., 2006. Prenatal olfactory learning in the domestic dog.
Roth, S., Cohen, L.J., 1986. Approach, avoidance, and coping with stress. Am. Psychol Anim. Behav. 72, 681e686.
41, 813e819. Willis, M.B., 1995. Genetic aspects of dog behaviour with particular reference to
Sankey, C., Richard-Yris, M.A., Henry, S., Fureix, C., Nassur, F., Hausberger, M., 2010. working ability. In: Serpell, J. (Ed.), The Domestic Dog: Its Evolution, Behav-
Reinforcement as a mediator of the perception of humans by horses (Equus iour, and Interactions with People. Cambridge University Press, Cambridge,
caballus). Anim. Cogn. 13, 753e764. pp. 51e64.
Savastano, G., Hanson, A., McCann, C., 2003. The development of an operant con- Wilson, D.S., Clark, A.B., Coleman, K., Dearstyne, T., 1994. Shyness and boldness in
ditioning training program for new world primates at the Bronx Zoo. J. Appl. humans and other animals. Trends Ecol. Evol. 9, 442e446.
Anim. Welf. Sci. 6, 247e261. Wilsson, E., 2016. Nature and nurture-how different conditions affect the behavior
Schalke, E., Stichnoth, J., Ott, S., Jones-Baade, R., 2007. Clinical signs caused by the of dogs. J. Vet. Behav.: Clin. Appl. Res. this volume.
use of electric training collars on dogs in everyday life situations. Appl. Anim. Wilsson, E., Sinn, D.L., 2012. Are there differences between behavioral mea-
Behav. Sci. 105, 369e380. surement methods? A comparison of predictive validity of two rating
Schilder, M.B.H., van der Borg, J.A.M., 2004. Training dogs with help of the shock collar: methods in a working dog program. Appl. Anim. Behav. Sci. 141 (3-4),
short and long term behavioural effects. Appl. Anim. Behav. Sci. 85, 319e334. 158e172.
Scott, J.P., Bielfelt, S.W., 1976. Analysis of the puppy testing program. In: Wilsson, E., Sundgren, P.E., 1997. The use of a behaviour test for the selection of dogs
Pfaffenberger, C.J., Scott, J.P., Fuller, J.L., Ginsburg, B.E., Bielfelt, S.W. (Eds.), Guide for service and breeding, I: Method of testing and evaluating test results in the
Dogs for the Blind: Their Selection, Development, and Training. Elsevier, adult dog, demands on different kinds of service dogs, sex and breed differ-
Amsterdam, pp. 39e76. ences. Appl. Anim. Behav. Sci. 53, 279e295.
Scott, J.P., Fuller, J.L., 1965. Genetics and the Social Behavior of the Dog. University of Winslow, J.T., Parr, L.A., Davis, M., 2002. Acoustic startle, prepulse inhibition, and
Chicago Press, Chicago. fear-potentiated startle measured in rhesus monkeys. Biol. Psychiatry 51, 859e
Seksel, K., Mazurski, E.J., Taylor, A., 1999. Puppy socialization programs: short and 866.
long term behavioural effects. Appl. Anim. Behav. Sci. 62, 335e349. Yehuda, R., Brand, S., Yang, R.K., 2006. Plasma neuropeptide y concentrations in
Serpell, J.A., Hsu, Y.Y., 2001. Development and validation of a novel method for combat exposed veterans: relationship to trauma exposure, recovery from
evaluating behavior and temperament in guide dogs. Appl. Anim. Behav. Sci. 72, PTSD, and coping. Biol. Psychiatry 59, 660e663.
347e364. Yehuda, R., Flory, J.D., Southwick, S., Charney, D.S., 2006. Developing an Agenda
Sherman, B.L., Gruen, M.E., Case, B.C., Foster, M.L., Fish, R.E., Lazarowski, L., DePuy, V., for Translational Studies of Resilience and Vulnerability Following Trauma
Dorman, D.C., 2015. A test for the evaluation of emotional reactivity in Labrador Exposure. Annals of the New York Academy of Sciences 1071 (Psychobiol-
retrievers used for explosives detection. J. Vet. Behav: Clin. Appl. Res. 10, 94e ogy of Posttraumatic Stress Disorder: A Decade of Progress), Wiley,
102. pp. 379e396.