1. Introduction
Dogs are a popular choice of pet in United Kingdom (UK) households (nine millions [
1]), yet, between 2017–2018, over 56 thousand strays were handled by local authorities in the UK [
2]; of these, 24% were passed onto animal welfare organisations for rehoming. There is increasing pressure on shelter staff to rehome dogs and ensure that dog-owner matches are successful, which minimises the rate of returned dogs [
3,
4,
5] due to behaviour problems, particularly aggression, disobedience, and hyperactivity/destruction [
3,
4]. Behavioural assessments are used within animal shelters to evaluate a dog’s reaction to a range of stimuli and situations to increase the chances of a successful dog-owner match [
6,
7,
8,
9]. One of the few comprehensively validated temperament tests for shelter dogs is the one that was developed by Valsecchi and collaborators [
9] who have published key test attributes such as reliability and validity [
5,
10]. Since its publication, the Valsecchi et al. temperament test (hereby TT) has not been, to our knowledge, adopted by other researchers or tested on different shelter populations. A key element of good science, often overlooked in many fields, including behavioural testing and animal welfare science, is the reproducibility of published experimental results [
11,
12].
In addition to the goodness and appropriateness of the measures used, it is important to also assess test feasibility (i.e., how easily the test can be carried out and the dog behaviour scored, and how practical it is to perform the test in different settings [
10]). One of the practical limitations of Valsecchi et al.’s TT was the use of real stimulus dogs to assess intra-specific sociability. The dog-to-dog interaction test is crucial within pre-adoption evaluation to assess a dog’s reaction towards conspecifics. However, the inherent safety and ethical concerns that arise when using real stimuli dogs makes a test less widely applicable: i.e., having to rely on the availability of a calm and well socialised stimulus dog might be challenging in a shelter with fast turnovers. Previous studies have introduced the use of artificial dogs for dog-dog assessments; however, their validity in assessing the sociability to dogs is still debated and in need of further investigation [
13,
14,
15]. Overall, there seems to be a weak correlation between the behaviour of the tested dogs toward the real vs. fake stimulus dogs [
13,
14]: the inherent stiffness and absence of odour of the fake dog is likely to be among the main reasons causing these different responses. Another confounding factor that has never been taken into account and that could affect the behavioural reaction of dogs during a social interaction is the size of the stimulus [
16,
17]. The few existing experiments so far have been carried out by using one single artificial dog of medium size [
13,
14,
15]. However, dogs are able to assess and react differently toward conspecifics of different sizes [
16,
17], an ability termed mutual assessment [
18], with size reflecting a proxy of fighting ability, a concept known as resource holding potential (RHP) and observed in many species [
18]. Given the above, we introduced, in the TT, the presentation of two fake dogs of different size and compared the reaction of the tested dogs to these fake stimuli and to two real dogs that also differed in size in an analogous way. More specifically, we hypothesise that, consistent with assessment theory, the responses of focal dogs to conspecifics will differ according to the contexts of real/fake and large/small stimulus dog.
In summary, the present study addresses the following objectives:
- (1)
Adapt and replicate the work by Valsecchi et al. [
9] to provide feedback on the replicability and easiness of application of their temperament test in different experimental settings. A supplemented version of the test was implemented in two different rescue shelters in the United Kingdom to do this.
- (2)
Assess the validity constructs of the test, such as content validity and internal consistency, and compare, where appropriate, the results with those of Valsecchi and collaborators [
9]. The results were also used to analyse possible demographic factors (e.g., sex, history, shelter location) that affect the behavioural responses of two populations of dogs to the test.
- (3)
In the realm of feasibility, introduce the use of differently sized artificial dogs and check their appropriateness in correctly assessing dog-sociability, to both maximise future applicability and minimise ethical/safety concerns that are associated with the use of real stimulus dogs.
2. Method
2.1. Shelters
A convenient sample of two shelters (in Northern Ireland, UK) was selected for the study (site 1, S1 and site 2, S2). Shelters adhered to local legislation, were registered as no-kill shelters, and had a small team of staff and heavily relied on volunteers and on funding from external sources and charitable donations. Both shelters could care for an average of 45 dogs per week. The dogs at S1 were individually housed within purpose-built kennel blocks and received three 25-min. walks daily. The testing area at S1 consisted of an indoor training room approximately 8 × 11 m with windows and two doors. The dogs at S2, whilst being kennelled indoors at night, were placed in pairs in outdoor runs with chain-linked fencing during the day. The testing area at S2 was in a shed approximately 8 × 10 m, with windows and two doors. Both sites are open to the public for the rehoming of dogs. Tests were performed during closing hours to avoid interruption and distractions.
2.2. Subjects
A total of 50 dogs were involved in the study: 20 males (75% neutered) and 30 females (70% spayed) of different breed and mixed breeds. S1 allowed the intake of welfare cases and Staffordshire Bull Terriers and their crosses (5/25), whereas S2 did not. This might, in part, influence any differences found between shelters. Twenty-five dogs were recruited from S1 and 25 dogs from S2. To be eligible for inclusion, dogs had to be declared healthy by staff and undergo veterinary health checks on arrival to the shelter, to be a minimum of 12 months of age and resident at the shelter for at least one week. If the history of the dog was unknown, age was estimated by the shelter veterinarian on the basis of dental and overall health condition. Upon entrance, the dogs were recorded either as previously owned (dogs relinquished by owner for various reasons), welfare case (dog confiscated from the owner), or stray (brought into shelters from the council after short duration in pounds). Dogs that were excluded were those deemed unsafe for testing by shelter staff, due to illness or aggression towards the handlers and dogs that were on any form of medication that could influence behaviour. The mean age of dogs tested was 4.2 years old (SD = ±2.45), with weight 22 kg (SD = ±10.63) and average height of 42.6 cm (SD = ±14.8). Most dogs (62%) were previously owned, 32% were strays and 6% were welfare cases. Reasons as to why the previously owned dogs were relinquished were unknown.
2.3. Procedure
The temperament test (TT) that was used was based on the Valsecchi et al. [
9] study. The original test consisted of 22 subtests that measured the dog behaviour in the kennel, sociability to humans, intraspecific sociability, docility to leash, playfulness, cognitive skills, and reactivity. We kept the procedures as identical as possible to those that were described in the original paper. An important novel modification of the current study was the addition of two artificial dogs introduced during the dog-dog interaction subtest (described below). Due to the study design, subtests were administrated to all dogs in the same order, with the exception of the real/fake dogs presented in randomised order, as explained later. The experimenters had considerable previous experience in volunteering at shelters and handling dogs; however, they were unfamiliar to the test subjects. One experimenter (female) was always the one administering the test, the other experimenter (male) was observing and scoring the dogs’ reaction.
The test was scored live, although the dog-dog interaction subtest was also recorded for additional detailed behavioural analysis. An initial training phase was conducted before data collection to standardise the protocol (see details in the
supplementary material).
2.3.1. Temperament test (TT)
The test protocol and scoring system are detailed in the online
supplementary information (Table S1). Initial observations were made from outside the kennel (subtests 1 and 2). The activity of the dog inside its home pen was recorded along with any signs of stereotypical behaviour (e.g., pacing, tail chasing). The experimenter then briefly interacted with the dog first from outside the kennel (subtests 3–5), then from inside the kennel (subtests 6, 7), and took the dog out on a lead into the testing area (subtest 8, 9). In subtest 10, an artificial hand measuring 45 cm in length (Mekuti Assessor Hand) was initially used to pet the dog. If safe, the experimenter would then carry out additional handling (e.g., lift paws, wear muzzle, brush). Subtests 11–13 assessed the dog’s ability to respond to basic commands (“sit”, “stay”) and solve a simple problem task (i.e., retrieve a treat from underneath an upside-down bowl). Playfulness was assessed (subtests 14 and 15) by throwing a ball and a squeaky toy to the dog and then asking it to retrieve. In subtest 16, the fake hand was used to remove a bowl with food from the dog while eating to assess resource guarding. Subtests 17 to 20 were used to assess intraspecific sociability (described below). A startle response (subtest 21) was evaluated by opening an umbrella in the direction of the dog (without contact) and by sounding an air horn. During this reactivity test, habituation to the stimuli was scored and a maximum of ten trials was allowed to habituate the dog if necessary. Finally, the dog was returned to its kennel on a lead (subtest 22).
2.3.2. Dog-Dog Interaction Assessment
This assessment was carried out by the two experimenters: one person holding the stimulus dog (handler 1, H1) and the other person holding the test dog (handler 2, H2). The test was recorded while using a Sony HDR-CX450 camcorder for later analysis, and the dogs’ responses were also rated live by H1 after each encounter following the TT scoring presented in
Supplementary Table S1. An artificial large and small dog were used in the assessment (Hansa, UK), and they were chosen for their life-like features (
Supplementary Figure S1). The fake stimulus dog breeds selected were a Siberian husky (large-measuring 93 cm in length and 65 cm in height) and a Finnish lapdog (small-measuring 53 cm in length and 37 cm in height).
At site S1, the real large stimulus dogs was a male Staffordshire bull terrier cross (tan four-year-old, neutered, 56 cm in height). The small stimulus dog used was a male Bichon-Frise (white three-year-old, intact, 25 cm in height). At site S2, the real large stimulus dog was a male Alaskan malamute (black and white five-year-old neutered, 66 cm in height), the small real stimulus dog was a male Griffon (black four-year-old, intact, 30 cm in height). The real stimulus dogs were selected from the population within each site and they were described by shelter staff to have a good level of friendliness towards other dogs.
All of the stimulus dogs were provided with regular breaks away from the testing area. Prior to testing, each dog was walked for approximately five minutes to get them used to the handler. A repeated measures design was used to investigate the effect of the independent variable termed ‘stimulus dog’. This consisted of each focal dog (referred to hereafter as the ‘test dog’) being exposed to the four conditions (large real; small real; large fake; and, small fake) in a random order achieved using a random number generator (random.org). Real and artificial stimulus dogs were introduced to the test subjects in the same manner every time. Both real and artificial dogs wore a 1 m lead during all of the testing period. The procedure consisted of three phases:
- (1)
Distance: H1 and the stimulus dog moved in position 1. H2 entered the room and walked the test dog to the start position (
Figure 1A), 5m opposite from H1. H2 remained positioned facing H1 for 15 sec holding the dog on a loose lead.
- (2)
Approach: H2 followed a predefined route on the floor (drawn using coloured duck-tape) which ended 1 m in front of H1 (
Figure 1B).
- (3)
Proximity: H2 remains in front of H1 for 15 sec. There was a 1 m buffer zone between handlers for safety purposes with no contact between the test dog or fake dog (
Figure 1C).
Once this component of the test was complete, the (real) stimulus dog was taken back to its kennels, while the test dog was walked outside the testing area for a few minutes before continuing with the TT.
The test dog was monitored throughout for levels of aggression; however, none of the assessments had to be stopped due to unmanageable aggression.
The behaviour of dogs during this test was scored from video while using an ethogram consisting of 21 behaviours that were compiled from previous work by Shabelansky et al. [
14] and De Palma et al. [
19] and from scoring a random selection of five videos (
Table S2). The behaviours were scored as frequency or duration of behaviour and were analysed while using The Observer XT 14.0 (Noldus, The Netherlands) software.
2.4. Statistical Analysis
To enable comparison with Valsecchi et al. [
9] the same original scoring was used with some slight amendments. Various scales were used in the scoring process, ranging from two to ten point scales (
Table S1). A score of zero was always given when the dog displayed the least desirable behaviour for each subtest (e.g., aggressiveness, not performing the task).
A range of statistical tests were used to assess the validity of measures while using definitions that were provided by Taylor and Mills [
10] and Valsecchi et al. [
9]. All statistical tests were carried out using IBM SPSS (v.24, IBM, Portsmouth, UK) software with alpha ≤ 0.05.
Content validity: the goodness of chosen measurements i.e., whether an item appears to be measuring the variable that it claims to. Here, for example, different subtests were developed to measure the dog willingness to interact and socialise with humans, so we would expect these items to group into one dimension. A common way to assess content validity in temperament tests is to use a data reduction technique, such as factor analysis or principal component analysis (PCA) [
10]. We applied a PCA with varimax rotation and Eigenvalue > 1. Anti-image correlation scores and Kaiser-Meyer-Okin (KMO) for sampling adequacy were checked to ensure that data assumptions were met.
Internal consistency: consistency within components designed to measure the same trait. Here, internal consistency was measured by checking the correlation within each dimension extracted by the PCA while using Cronbach’s alpha test.
Non-parametric tests were then used to assess whether the shelter location, permanence in shelter, sex, neutering status, and homing history affected the PCA component scores. Mann Whitney U test or Kruskall-Wallis tests for two or more independent samples were used for this aspect. Post-hoc pairwise comparisons were conducted where appropriate.
To reduce the number of behavioural variables used to assess the dog-dog interaction, a PCA was run, after data log-transformation, using varimax rotation. Anti-image correlation score and Kaiser-Meyer-Okin (KMO) were checked to ensure sampling adequacy. The principal components scores resulting from this analysis were used as new variables to investigate the effect of the stimulus’ characteristics on the tested dogs’ responses. A Spearman’s rank correlation test was performed to evaluate whether the dogs’ responses to fake versus real stimuli were correlated (matched by size). Subsequently, Wilcoxon signed rank tests were used to assess whether the reaction of the dogs significantly differed when faced with real versus fake dogs or with different sized stimulus dogs.
2.5. Ethical Approval
This study received full ethical approval from the participating shelters’ management and the animal research ethics committee at Queens University Belfast (Application approval number: QUB-BS-AREC-16-001). Both of the handlers were experienced kennel workers with good knowledge of the care and handling of dogs in a shelter setting. All the instructions and procedures were agreed in advance of testing. A maximum of 5 dogs was tested each day to avoid undue stress on the real stimulus dogs. The researchers were guided by guidelines laid down by the International Society for Applied Ethology ‘Ethical Treatment of Animals in Applied Animal Behaviour Research’ (ISAE, 2016).
4. Discussion
The aim of the current study was to replicate and extend the Valsecchi et al. [
9] study while using the temperament test (TT) that the authors developed to assess the behavioural profile of shelter dogs. Although several aspects of the original test were validated, no other researchers (to our knowledge) have adopted this test and applied it to different shelter populations, thus a supplemented version of the TT was applied to two populations of dogs housed in two rescue centres in Northern Ireland (UK).
Temperament test. The reduction analysis of the TT scores extracted similar behavioural dimensions to those of Valsecchi et al. [
9], especially the first two components ‘sociability to humans’ and ‘sociability to dogs’. This was in line with expectations, as these are the most robust components explaining the majority of variance in both studies (29–18% current work and 21–17% original work). It is interesting to note that, even though the sample size in the current study is smaller, the loadings on the first two components appear to be higher and more defined than in the previous study: in the original work, for example, handling (#10) loaded equally on both component #1 and #2, whereas, here, it only heavily loaded on the ‘sociability to humans’ component. As in the original work [
9], the second component ‘sociability to dogs’ is characterised by the four subtests that were designed to assess dog-dog interaction (present study: reaction to real and fake dogs of small and large size; original study: approach and contact with real dogs of same and opposite sex). This result confirms that these scores are highly correlated (internal consistency, α = 0.93) and they appear to be measuring the same behavioural construct [
10]. Hence, it can be argued that the reaction of the test dog to a fake dog is more similar to its reaction to a real dog than to any other stimulus presented during the test. A third component that was very similar between the two studies was ‘playfulness’, as described by the two variables ‘play with ball’ and ‘play with squeaky toy’. It appears that playful behaviour (object oriented in this case) can be easily detected with a couple of simple play sessions and that toys elicit a behavioural reaction that is distinct from that shown towards other elements of the test. These first three components, sociability towards people and dogs and playfulness, represent highly desirable behaviours for potential owners that are looking to adopt a dog [
20].
The remaining variables loaded somewhat differently here as compared to the original work. First it should be noted that three variables (walking on lead, commands, and attention test) were not included in this analysis, as their MSA (i.e., degree of partial correlation with all the other variables) was not ideal and would have potentially reduced the overall robustness of the test. Interestingly, in the factor analysis by Valsecchi et al. [
9], ‘walking on leash’ and ‘commands’ did not load highly on any factor. The response to these subtests may be distinct from the rest of the test as they may depend on the dog’s previous training experience rather than being a mere behavioural predisposition. In a refinement of the test, it could be discussed to drop these scores; however, even though not loading on any factors, these subtests provide important information on any previous training experience as well as the dog’s willingness to engage with the handler (stay close to the handler when on leash, respond when called, focus the attention on the task when asking for a ‘sit’). This information might be valuable when deciding how easy a dog is to train or work with. Differences emerge when considering the other subtests and the result of the reduction analysis of the two studies. In the present work, two components were extracted by the PCA: ‘reactivity’ and ‘adaptation to kennel’. The first one was represented by the variables ‘reactivity’, ‘food possessiveness’, problem solving’, and ‘placing on lead’: indeed, resource guarding can be a form of reactivity to an approaching/sudden stimulus and placing on lead can also trigger a startle/fear reaction similar to that of the reactivity test, especially if the dog is not used to being leashed or if it is afraid of people. The correlation among these elements identifies a calm dog that is able to ignore disturbance while eating, being relaxed to loud noise and to the leash, and also being relaxed enough to focus on the simple cognitive task and motivated to solve it. In the original paper, those variables loaded differently on the extracted factors (Table 4 in Valsecchi et al. [
9]). Many factors could account for this difference, i.e., here, we did not include the ‘attention test’ variable in the analysis, hence the redistribution of variables on different components, but more likely these variables may not be ideally designed to measure a separate behavioural construct and they may be underlined by other confounding traits. This is understandable, as leash walking and food possessiveness are again dependent on previous experiences/training and they may not be a proper measure of temperament, but still a useful measure of handling ease and motivation to work.
Finally, the variables on the last component recorded the dog behaviour in their home pen. In the original work, ‘stereotypical behaviour’ loaded on a separate factor and ‘observation from distance’ did not load on any factors, even though the highest loading was on the same factor as ‘stereotypical behaviours’ (Table 4 in Valsecchi et al. [
9]). A dog at the front of the kennel (as opposed to the back), returning to its pen without difficulty and not showing stereotypies could indicate a calm temperament, but also a good degree of adaptation to the kennel itself.
Overall, this analysis showed that there is very good overlap between the outcomes of the tests that were carried out by two different research teams on different dog populations, which suggests that the test was well designed to measure temperament traits, such as sociability towards people and other dogs and playfulness. The test appears not to be as robust in assessing other behavioural constructs such as motivation, docility to leash and reactivity. A number of factors may have affected inconsistencies among some of the components that were extracted, including the low variance on some of the variables, the low number of subtests designed to assess one trait, e.g., reactivity (one subtest), problem solving (one subtest), commands (two subtests that imply different underlying skills like ‘come’ or ‘sit’), and the relatively small sample size.
Within the extracted components, the internal consistency was high, especially for the first two components, which further confirmed that items loading on these factors were measuring the same constructs. The alpha value for the third component analysed (‘reactivity’ = 0.65) was indeed lower, supporting the above discussion on this being a less robust component, yet still representing a good correspondence between measures.
The factor scores of the five components extracted were used to explore the effect of dogs’ characteristics and shelter environment on the dogs’ response to the TT. We found that the neutered/spayed dogs scored higher on the ‘playfulness’ component (
Figure 2). The effect of spaying and neutering on dog behaviour is not yet clear; some studies investigating the factors affecting aggressive behaviour in dogs, for example, have found weak or no association, often confounded by the fact that, especially in male dogs, aggressiveness is often a cause of castration, rather than a consequence [
21,
22,
23,
24]. However, one study on male ferrets found that the incidence of play behaviour was significantly higher after castration [
25]. Indeed, more empirical work is needed to explore this topic. Dogs from the two shelters significantly differed on only one component: ‘sociability to dogs’ (
Figure 3). This is likely a consequence of the different kennel design, housing system, and management practises characterising the two facilities. In S1, dogs were individually housed with visual barriers between kennels and only interacted with compatible dogs in controlled socialisation sessions. Conversely, dogs in S2 were pair housed in larger outdoor runs for the majority of the time and the wire mesh allowed for them to see the dog in the adjacent kennels. Results showed lower sociability scores for dogs in S1, possibly a consequence of single housing system. It could also be that the population of dogs that the shelters were selecting to intake was different in terms of breed, provenience, and known behavioural problems (e.g., S1 was more likely to accept Staffordshire Bull Terriers and their crosses and welfare cases). However, we could not control for these factors.
Dog-dog interaction. Expanding on previous work [
13,
14,
16], we further investigated whether dogs would modulate their behavioural response when presented with real conspecifics versus fake ones and if the stimulus’ size would affect that response. The PCA extracted four main components. It is interesting to highlight that all of these components include anxiety or stress related behaviour that can be part of different coping strategies that the dogs are showing when faced with the stimulus dog. The first component is described by, on one hand, behaviour typical of a more excitable dog, willing to engage and interact with the other dog; however, behaviours like barking and play bow also loaded here, which can be an indicator of excitement as well as frustration [
26]. On the other hand, ‘investigate the environment’ and ‘look at handler’ loaded on this first component (with opposite sign) and these are more clear signs of redirected attention, trying to avoid the interaction with the stimulus and looking at the handler for support [
27]. The second component was described by the variables ‘investigate the stimulus’ and ‘deflection’. Dogs investigating the stimulus normally did so in a cautious manner when in contact and they were normally the dogs avoiding looking at the stimulus from far but at the same time breaking eye contact as an appeasing behaviour. These dogs, although somewhat engaging with the stimuli, showed signs of mild fear. The third component was characterised by dogs staring and stiffening at the sight of the stimulus dogs, yet this posture was also associated with lip/nose licking, which suggested that, probably, a component of anxiety was associated with the emotional state of the dogs when facing the stimuli [
28]. Finally, behaviours that are typical of a fearful reaction, such as assuming a low body posture and increasing the distance from the stimulus, loaded together on the last factor. These characterise dogs that are clearly avoiding the interaction with a conspecific and they are in a fearful emotional state.
When analysing whether the behavioural component scores that are described above varied in relation to the stimulus presented, we found that the reaction to real versus fake dogs was highly positively correlated and we did not detect any significant difference in the dogs’ responses to the different stimuli despite size (
Figure S2). It appears that, in these populations, the fake dog was triggering the same type of behavioural response/coping strategy as the real counterpart, and with no effect of the stimulus’ size. This is in contrast to previous work [
16,
17] that demonstrated the ability for accurate conspecific assessment in dogs. The conflicting findings likely reflect important contextual differences, with the current study involving stimulus dogs being selected to have a calm, non-aggressive temperament, and the setup lacking vocal cues (e.g., growling) that were a key component, likely used for size assessment in the previous studies [
16,
17]. The subjects were recruited according to the availability at the time of the study due to the source of dogs (i.e., rescue shelters). It was not possible to select test dogs with a specific body size that matched (or differed from) the stimulus dog size. Future studies should attempt to balance the sample to have a balanced sample of test dogs that are equal, smaller, and larger than the stimulus dog and add the test dog size as a factor, which might have an effect on the dogs’ behavioural response to the subtest.
The use of behavioural tests in shelters have recently been criticised [
29]. Behaviour evaluations are said to provide false positives and false negatives, which may hinder the chance of adoption for some dogs [
30,
31]. It is understood that no test will ever be able to 100% predict behaviour post-adoption and provide new owners absolute certainty that a dog will behave in a certain way, nor should any test claim to be able to do so. The familiar world outside the shelter environment is full of complex situations (i.e., many people in the same household, children, elderly people, other animals) and dogs need some months to adapt to it and show their true personality. The use of standard behavioural tests as screening tools is still important to identify subjects that may need more training, or other targeted interventions (e.g., desensitisation) before adoption and maximise the chances for a successful adoption. These screening tools are also useful for shelter staff to assess and address any behavioural concerns that may affect the dog’s ability to cope in the kennel environment, e.g., very fearful/reactive dogs may be difficult to handle and struggle to adapt, hence impacting on their overall welfare.