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Do disrupted early attachments affect the relationship between guide dogs and blind owners?
Applied Animal Behaviour Science 100 (2006) 241–257 www.elsevier.com/locate/applanim
Do disrupted early attachments affect the relationship between guide dogs and blind owners? Gaia Fallani a,*, Emanuela Prato Previde a, Paola Valsecchi b a
Istituto di Psicologia, Universita` degli Studi di Milano, via Tommaso Pini 1, 20134 Milano, Italy b Dipartimento di Biologia Evolutiva e Funzionale, Universita` degli Studi di Parma, Parco Area delle Scienze 11 A, 43100 Parma, Italy Accepted 11 December 2005 Available online 19 January 2006
Abstract The study investigated the affectional bond developed by dogs (Canis familiaris) towards their human companions during the selection process to become guide dogs and compared this bond with that formed by pet dogs with their owners. One hundred and nine dog-owner pairs were tested using a modified version of the Strange Situation Test: custody dogs-puppy walkers (n = 34), apprentice dogs-trainers (n = 26), guide dogs-blind owners (n = 25) and pet dogs-owners (n = 24). Twenty-six behaviours were scored using a 5 s point sampling method and two vocal behaviours were recorded as bouts. Factor analysis carried out on 24 mutually exclusive behaviours highlighted two different profiles of response. A relaxed reaction characterised by a high play activity was distinctive of custody and apprentice dogs, whereas an anxious reaction characterised by a high degree of proximity seeking behaviours was distinctive of pet dogs. Guide dogs were intermediate between these two extremes, expressing their attachment to the owners but showing a more controlled emotional reaction. This finding suggests that guide dogs can be viewed as ‘‘working pets’’. Furthermore, the experimental set-up, characterised by the presence of a frightening stimulus, revealed that untrained dogs (pets and custody dogs) were more fearful than trained dogs (guide dogs and apprentice dogs). Finally, differences in temperament emerged between retrievers: Golden retrievers showed a higher level of affection demand while Labrador retrievers were more playful.
* Corresponding author. Tel.: +39 0521 905671; fax: +39 0521 905657. E-mail address: [email protected] (G. Fallani). 0168-1591/$ – see front matter # 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.applanim.2005.12.005
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Overall, these findings show that in spite of separations from previous attachment figures, guide dogs established with their blind owner a rather good and secure affectional bond. # 2005 Elsevier B.V. All rights reserved. Keywords: Guide dogs; Behaviour; Attachment
1. Introduction The dog (Canis familiaris) was the first animal domesticated by human kind (Homo sapiens) and since ancient times has been kept for companionship and for cooperating on a variety of tasks, thus it consolidated a strict and intense relationship with humans (CluttonBrock, 1999; Schleidt and Schleidt, 2003). As a consequence of this long lasting association dogs sharpened some behavioural and cognitive characteristics already present in their co-operative ancestor the wolf as a result of a ‘‘process of enculturation’’ (Hare et al., 2002). Recent research showed that dogs’ social cognitive skills allow them to engage in complex and effective interactions with humans (for a review see Cooper et al., 2003). For example, there is evidence that dogs can learn socially from conspecifics or human beings (Slabbert and Rasa, 1997; Kubinyi et al., 2003), are able to use different human social signs (e.g. looking or pointing) as information sources to solve a task (Soproni et al., 2001; Miklo`si et al., 2003) and engage in complex communication with people (Kaminsky et al., 2004). Today in many western countries dogs are trained to provide help and to cooperate with humans in tasks that involve a particular training and require specific skills and variable levels of co-operation with the human companion (i.e. searching for objects or persons, assisting disabled people, etc.). Among assistance dogs, guide dogs for the blinds provide an interesting example as the blind owner depends completely on his/her dog for visual information and the dog does not know about the planned actions of its owner (Naderi et al., 2001). Such a delicate and subtle equilibrium requires a peculiar development of co-operation and of a strong but at the same time balanced bond. There is now evidence suggesting that the dog–human affectional bond can be characterised as an attachment: dogs show towards their owner attachment behaviours which closely resemble those reported in human infants and chimpanzees (Topa`l et al., 1998; Prato Previde et al., 2003). In order to form a good and secure affectional bond with humans a dog needs to be precociously introduced to them and to socialise during a specific sensitive period (for a review see: Serpell and Jagoe, 1995). Pfaffenberger et al. (1976) observed that puppies that lived in a kennel for 12 weeks or more after birth, and therefore could not familiarise with people, were generally insecure even if accompanied by their attachment figure and rarely succeeded in becoming guide dogs. In addition, traumatic experiences like abandonment or in general the break down of an already established bond may favour the appearance of behavioural problems thus compromising the dog–human relationship (Fox, 1968). Serpell and Hsu (2001), in a questionnaire study, found that a wrong or excessive attachment during the first period of life can determine a negative evaluation of the dog by trainers and
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its failure to become a guide dog. In particular it emerged that puppies that scored very high in attachment towards their puppy-walker and his/her family were rejected because judged too emotional and excitable and excessively protective and aggressive towards strangers. Guide dogs form their bond with the blind person after a long period of intense training and after the formation and break down of two previous important affectional bonds with different attachment figures: the puppy-walker (during the first year of life) and the trainer (during the period of training). The relationship a potential guide dog forms with the puppy-walker and the trainer and the break down of these bonds may have a negative influence on the animal’s behaviour that could in turn compromise either successful training or the relationship with the blind person. To test this hypotheses, the present study investigated the bond developed by dogs towards their human companions during the selection process to become guide dogs, and compared this bond with that formed by pet dogs with their owner(s). This goal was attained using the Strange Situation Test (SST) a procedure that has proved to be useful in investigating the dog–human relationship (Topa`l et al., 1998; Prato Previde et al., 2003, 2005). The behaviour of four groups of dogs during the SST was evaluated considering four different kinds of attachment figures: the puppy-walker, the trainer, the blind owner and the pet owner. As our sample of dogs was rather large and included mainly Labrador and Golden retrievers we investigated also the differences between these breeds in the attachment bond.
2. Methods 2.1. The school The ‘‘Scuola Nazionale Cani Guida per Ciechi-Regione Toscana’’ (National School for Guide Dogs, Scandicci, Italy) trains and provides to blind people about 50 dogs per year. The school has some breeding dogs which live in private household and reproduce once per year. In addition, the school purchases puppies from different breeders located in Tuscany. Puppies are placed with volunteer puppy walkers at 40 days of age and raised in puppy walkers’ homes until they are about 12 months old. During this period of time they periodically go back to the school to become familiar with the place and the people. At 12 months of age the dogs return to the school to start a training lasting approximately 6–8 months. The training takes place under the management of a single trainer. At the end of training, guide dogs are assigned to blind people: the dog-blind matching is mediated by school assistants during a 20 days course involving the new blind-dog pair. One year after the assignment of the guide dog, the blind person comes back to the school with his/her dog for the first evaluation of the success of the dog-blind pair. 2.2. Subjects One hundred and nine dogs (34 males, 75 females) were tested from February 2003 to December 2004. The sample included 42 Golden retrievers, 53 Labrador retrievers, 8 Golden Labrador crosses, and 6 German Shepherds.
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The dogs belonged to one of following four groups: Custody: This group consisted of 34 dogs (11 intact males and 23 intact females) ranging from 11 to 15 months of age (X S.E. = 11.6 1.3). The dogs were tested 1 month before returning to the school for the training, and therefore their attachment figure in the strange situation test (SST) was the puppy walker. Apprentice: This group consisted of 26 dogs (4 neutered males, 6 intact males and 16 intact females) ranging from 12 to 20 months of age (X S.E. = 16 2.1). The dogs were tested after 2 months of training and therefore their attachment figure in the SST was the trainer. Guide: This group consisted of 25 dogs (6 neutered males and 19 intact females) ranging from 33 to 50 months of age (X S.E. = 37.6 7.8). The dogs were tested after 1 year of service during the annual control and their attachment figure in the SST was the blind owner. Pet: The group consisted of 24 dogs (7 males and 17 females) ranging from 11 to 49 months of age (X S.E. = 29.3 11.4). All the dogs were kept exclusively for companionship and lived within the human household and, therefore, their attachment figure in the SST was their owner. All human participants were volunteers: puppy walkers, trainers and blind persons were recruited from the National School for Guide Dogs while pet owners were recruited from advertisements distributed within the University of Milan. For sake of simplicity all attachment figures will be called ‘‘owners’’ from now on. 2.3. Set-up Experimental sessions were carried out in two rooms (15 m2 surface); the first room was located at the National School for Guide Dogs and the second one at the Institute of Psychology of the University of Milan. Both rooms were unfamiliar to the dogs and their set-up was similar to that described by Ainsworth and Bell (1970); they were equipped with two chairs (one labelled as ‘‘stranger’’ and the other as ‘‘owner’’), a selection of dog toys (one large and two small balls, two plastic bottles, a rope pull-toy and a squeaky toy), a water bowl and a videocamera (Handycam Video HI 8, Sony, Tokyo) connected with a monitor positioned outside the experimental room so that each session could be independently observed. Furthermore, a 1 m high homemade puppet similar to advertising Norwegian trolls was situated in the corner opposite to the door. The puppet was unknown to dogs and had some anomalous morphological characteristics such as a very long nose, big eyes and long curled green hairs. 2.4. Procedure The study was carried out using a modified version of Ainsworth’s strange situation test (Prato Previde et al., 2003). The entire procedure consisted of an introductory episode followed by 7 three-minute experimental episodes in which dogs were placed in an unfamiliar room, introduced to a female unfamiliar stranger and subjected to two short
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Table 1 Description of the Strange Situation Procedure Episode
Description
Episode 1: owner and dog Episode 2: owner, dog and stranger
The owner sat quietly and the dog was free to explore the room The stranger entered the room, sat quietly for 1 min, conversed with the owner for the second minute, approached the dog and attempted to stimulate play during the last minute. At the end of this episode the owner left the room unobtrusively The stranger continued to play with the dog if it was willing; if it was inactive or distressed, the stranger attempted to distract it with play or by providing verbal and tactile comfort The owner entered the room and greeted and/or comforted his/her dog as usual after returning from work or shopping. The stranger quietly exited the room. The owner had been told that he/she was free to play with the dog throughout the episode. At the end of this episode the owner left the room The dog remained alone for 3 min, but was constantly observed by the owner and researchers on the monitor in the adjacent room The stranger entered the room and followed the same protocol as in episode 3 The owner entered the room greeted the dog as though he/she had just returned from work or shopping. The stranger left the room unobtrusively. At the end of this episode the experimenter arrived and officially terminated the procedure
Episode 3: stranger and dog (first separation episode) Episode 4: owner and dog (first reunion episode)
Episode 5: dog alone (second separation episode) Episode 6: stranger and dog Episode 7: owner and dog (second reunion episode)
episodes of separation from their owners. The experimental episodes are detailed in Table 1. On their arrival human–dog pairs were escorted to a waiting room where the procedure was briefly described to the owners who were asked to subscribe the permission to use the data collected according to the national Privacy Law 675/36. Then, the video camera was activated and the participants were escorted to the experimental room for testing. Blind owners were helped by an assistant in subscribing the permission and were always escorted in and out the experimental room. Immediately after each session, the experimental room, water bowl and toys were washed using a non-toxic, weakly scented disinfectant. 2.5. Data collection and statistical analysis The behaviour of each dog during the experimental episodes was videotaped and analysed by three trained observers using a 5 s point sampling and a total of 26 behaviours were recorded (see Table 2 for a detailed description of the behavioural categories). Inter observer reliability was assessed by means of independent parallel coding of a random sample of videotaped sessions (i.e., 10%) and calculated as percentage agreement; percentage agreement was always more than 91%. Behaviours were mutually exclusive except ‘‘physical contact’’, ‘‘barking’’ and ‘‘whining’’, which could be associated with other behaviours. The two vocal behaviours were recorded only in episode 5, when the dogs remained alone, and were collected as bouts. The occurrence of each behaviour was calculated as a proportion of the total number of events scored while the occurrence of each
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Table 2 Behaviours recorded in the strange situation procedure Categories
Behaviours
Definition
Proximity seeking
Oriented to person
Staring fixedly at the owner (OPO) or stranger (OPS), regardless of whether the behaviour was reciprocated Approaching while clearly visually oriented to owner (AO) or stranger (AS), either spontaneously or when called Following the owner (FO) or the stranger (FS) around the room or to the door Staring fixedly at the door, either when close to it or from a distance (OD)
Approach person
Following Oriented to door Playfulness
Social play
Individual play
Any vigorous or galloping gaited behaviour performed when interacting with the owner (PLO) or stranger (PLS); including running, jumping, active physical contact and chasing toys Any vigorous or galloping gaited behaviour directed toward a toy when clearly not interacting with persons; including chewing, biting, shaking from side to side, scratching or batting with the paw, chasing rolling balls and tossing using the mouth (PLI)
Puppet fear
Stare at the puppet Avoid puppet
Staring fixedly at the puppet from a distance (SPP) Avoiding proximity with the puppet when moving around the room (WP)
Other behaviours
Exploration
Activity directed toward physical aspects of the environment (E) or toward puppet (EP), including sniffing, close visual inspection (EV), and gentle oral examination such as licking Sitting, standing or lying down without any obvious orientation toward the physical or social environment (PA) Walking, pacing or running around, without exploring environment or playing Staring fixedly at the owner’s (OCO) or stranger’s (OCS) empty chair Approaching while clearly visually oriented to puppet (AP) All active behaviours resulting in physical contact with the door, including scratching the door with the paws, jumping on the door, pulling on the door handle with the forelegs or mouth (S) Drinking at the water bowl (D) All greeting behaviours toward the entering owner (GO) or stranger (GS), such as approaching, tail wagging, jumping, physical contact Being in physical contact with owner (CO) or stranger (CS) Barking (B) and whining (W) (recorded as bouts only during the fifth episode)
Passive behaviour
Locomotion Oriented to chair Approach puppet Scratch the door
Drink Greeting behaviour
Physical contact Vocalising
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vocal behaviour was calculated as bouts per second. To achieve normality, the proportions were arcsine transformed using Bartlett’s correction for continuity (Bartlett, 1947). Factor analysis was used as an exploratory tool to have a general view of the dogs’ reaction to the SST and to extract the maximum information contained in the multivariate data set. The analysis output allowed to extract the patterns of correlation among the 24 mutually exclusive behaviours and to group 12 behaviours into three wider behavioural categories. The behavioural categories identified through factor analysis and the other behaviours not grouped were then used as dependent variables in the analysis of variance. As the high number of possible independent variables (i.e. dogs’ age, sex, group, breed, and owner’s gender) would have excessively fragmented the sample, only the dogs’ group and breed were considered as factors in the ANOVAs. The dogs’ age was not considered because the protocol for selection and training of guide dogs established age limits for the recruitment of dogs: therefore, the dogs still living in the adoptive families, those under training and guide dogs were necessarily in different stages of their development. The sex of the dog and the gender of the owner were omitted because preliminary ANOVA’s (not included for simplicity) revealed that these variables did not affect behaviour (see Table 3 for distribution of sex and breeds among the four different experimental groups). The behaviour of the four groups of dogs across the episodes was analysed using a oneway ANOVA for repeated measures with groups (four levels: custody, apprentice, guide, pet) as between-subjects factor, and time (seven levels: episode 1 to episode 7) as withinsubjects factor. Furthermore, to detect differences in behaviour towards the owner and the stranger a second ANOVA for repeated measures was carried out comparing episodes characterised by the exclusive presence of the owner (episodes 4 + 7) with those characterised by the exclusive presence of the stranger (episodes 3 + 6). Breed differences in behaviour were assessed using a one-way ANOVA with breeds (two levels: Golden and Labrador) as between-subject factor. Since most of the dogs were Golden and Labrador Retrievers, German Sheperd (N = 6) and Labrador Golden crosses (N = 8) were excluded from this analysis. As vocalizations were recorded only in episode 5, differences in barking and whining were assessed by means of one-way ANOVA with groups (four levels: custody, apprentice, guide, pet) as independent variable(s). Table 3 Distribution of sex and breeds between the four different experimental groups Group of dogs
Females
Males
Custody
23 (13 Golden retrievers, 5 Labrador retrievers, 5 Labrador Golden crosses) 16 (8 Golden retrievers, 6 Labrador retrievers, 2 German Shepherds) 19 (3 Golden retrievers, 14 Labrador retrievers, 2 German Shepherds) 17 (7 Golden retrievers, 10 Labrador retrievers)
11 (5 Golden retrievers, 3 Labrador retrievers, 3 Labrador Golden crosses) 10 (7 Golden retrievers, 1 Labrador retriever, 2 German Shepherds) 6 Golden retrievers
Apprentice
Guide
Pet
7 (3 Golden retrievers, 4 Labrador retrievers)
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For all ANOVAs, Tukey’s HSD test was carried out to detect differences in single comparisons (level of significance: a = 0.05). Statistical analysis was carried out using the statistical package SPSS 11.0TM.
3. Results 3.1. Factor analysis Factor analysis based on the data of the 109 dogs extracted eight primary factors: first, second and third factors, accounted for 43% of the variance. Any loading of 0.6 or above was considered highly significant for this sample size and was used as a criterion when considering the relevance of the variable loading on each factor. This criterion was fulfilled only by first and second factor variables, while the remaining six factors contained behavioural items for which there was no clear correlation (Table 4). The first factor explained 26% of variance and had ten high loadings: seven variables had a positive loading and three a negative one. The positive loading characterised ‘‘oriented to door’’ (0.606), ‘‘follow owner’’ (0.663) or ‘‘follow stranger’’ (0.671), ‘‘approach owner’’ (0.618) or ‘‘approach stranger’’ (0.698) and ‘‘oriented to owner’’ (0.732) or ‘‘oriented to stranger’’ (0.850). The three negative loadings characterised: ‘‘individual play’’ ( 0.718) and ‘‘play with owner’’ ( 0.634) or ‘‘play with stranger’’ ( 0.837). Based on this pattern of loadings this factor was labelled ‘‘response to the strange situation’’. In this factor two different profiles of response emerged: (1) a relaxed reaction characterised by a high play activity, and (2) an anxious reaction characterised by a high degree of proximity seeking behaviours aimed at keeping or regaining contact with the owner and the stranger. Consequently, two behavioural categories were defined: ‘‘playfulness’’ and ‘‘proximity seeking’’. The second factor accounted for 9% of variance and had only positive loadings: ‘‘stare at the puppet’’ (0.766) and ‘‘avoid puppet’’ (0.73). Based on this pattern of loadings this factor was labelled ‘‘fear of the puppet’’. 3.2. Effects of groups and episodes on strange situation behaviour The ANOVA for repeated measures revealed the existence of a number of interesting differences in behaviour among the four groups of dogs. Across the episodes of the test, dogs differed in proximity seeking behaviour (F 18,630 = 3.39, P < 0.0001; Fig. 1). In particular, in episodes 3 and 6 when the owner left the room leaving the dog alone with the stranger, pet dogs engaged in proximity seeking behaviours significantly more than custody and apprentice dogs (episode 3: pet versus custody, P = 0.01; pet versus apprentice, P = 0.018; episode 6: pet versus custody, P < 0.0001; pet versus apprentice, P < 0.0001). Fig. 1 shows that guide dogs engaged in proximity seeking behaviours more than custody and apprentice dogs but less than pet dogs. The highest frequency of proximity seeking was observed in episode 5 during which dogs were alone in the room (episode 5 versus all the other, P < 0.0001): it is worth noting, however, that the only proximity seeking behaviour the dogs could engage in during this episode was remaining
Table 4 Matrix of components from factor analysis Behaviours
1
2
3
4
5
6
0.218 0.354 0.126 0.606 0.718 0.837 0.634 0.558 0.487 0.732 0.850 0.254 0.156 0.162 0.663 0.671 0.618 0.698 3.673E 02 6.011E 02 2.398E 02 9.713E 02 0.541 0.180
0.251 7.736E 02 6.667E 02 4.239E 02 0.140 6.339E 02 0.211 0.122 0.107 9.879E 02 7.565E 02 0.766 0.539 0.319 9.988E 02 8.289E 02 0.246 6.887E 02 0.522 0.730 8.779E 02 0.355 0.131 5.962E 02
0.458 0.189 0.193 0.211 0.321 0.215 0.143 0.443 0.423 2.290E 02 0.151 3.043E 02 0.290 0.393 0.270 7.351E 02 0.267 0.142 1.070E 02 0.299 0.208 0.229 0.203 0.552
0.284 0.187 0.417 0.248 6.583E 02 0.238 0.336 0.132 0.402 0.225 0.179 0.146 0.237 5.239E 02 0.117 0.277 0.157 0.407 0.168 0.189 0.402 0.386 0.107 0.102
2.384E 02 0.289 0.255 0.164 9.433E 02 3.189E 02 4.97E 02 0.135 0.182 0.168 7.777E 02 0.256 0.425 0.263 0.104 0.133 6.282E 02 4.027E 02 0.584 0.386 0.407 0.223 0.132 7.240E 02
8.732E 02 1.320E 02 0.599 1.313E 02 0.154 6.102E 02 0.276 0.336 0.290 0.151 0.138 6.295E 02 9.613E 02 0.231 6.235E 02 0.278 9.791E 02 0.150 9.019E 02 7.872E 02 0.137 7.405E 02 0.252 0.475
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Exploration (E) Visual exploration (EV) Puppet exploration (EP) Oriented to door (OD) Individual play (PLI) Play with stranger (PLS) Play with owner (PLO) Passive (PA) Locomotion (L) Oriented to owner (OPO) Oriented to stranger (OPS) Oriented to puppet Oriented to owner chair (OCO) Oriented to stranger chair (OCS) Follow owner (FO) Follow stranger (FS) Approach owner (AO) Approach stranger (AS) Approach puppet (AP) Avoid puppet (WP) Scratch to the door (S) Drink (D) Greeting to owner (GO) Greeting to stranger (GS)
Components
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Fig. 1. Mean frequency of proximity seeking behaviours expressed by custody, apprentice, guide and pet dogs across the seven episodes of the SST. Differing letters indicate significant differences at P < 0.05 or lower.
oriented to the door sitting, standing or lying down in front of it or staring at it from a distance. In order to distinguish between behaviours directed towards the owner/stranger and aimed at staying in contact with them (i.e. follow, approach, oriented to person) and behaviours aimed at regaining contact with them when they were not in the room (i.e. oriented to the door) these two components of the proximity seeking category were divided and their occurrence in the presence of the stranger (episodes 3 + 6) and in the presence of the owner (episodes 4 + 7) was analysed separately. The ANOVA carried out on proximity seeking excluding being oriented to the door showed that dogs had an overall preference for their owners (F 1,105 = 10.98, P = 0.0012). On the contrary, all dogs remained oriented to the door significantly more often when the stranger was in the room and the owner was absent (F 3,105 = 6.39, P < 0.0001); this was particularly evident in pet dogs, and to a lesser extent in guide dogs (pet: owner versus stranger, P < 0.0001; guide: owner versus stranger, P = 0.10). In all groups physical contact with the owner increased across the SST (F 3,315 = 6.74, P < 0.001). Interestingly, guide dogs maintained physical contact with their blind owner significantly more compared to the dogs of the other groups (F 3,105 = 4.64, P = 0.004; guide versus custody, P = 0.005; guide versus apprentice, P = 0.014; guide versus pet, P = 0.067; Fig. 2). On the contrary, in all groups physical contact with the stranger was
Fig. 2. Mean frequency of physical contact with owner expressed by custody, apprentice, guide and pet dogs during the SST. Differing letters indicate significant differences at P < 0.05 or lower.
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maximum at the beginning of the test when they met her for the first time (episode 2, F 2,210 = 17.33, P < 0.0001). Finally, greeting behaviour towards the owner increased significantly from the first to the second reunion, and the same occurred with the stranger (owner: episode 4 versus episode 7, F 1,105 = 7.74, P = 0.006; stranger: episode 2 versus episode 6, F 1,105 = 9.3, P = 0.002). There were no group differences in greeting towards the owner upon reunion, but the dogs in the custody group greeted the stranger significantly more than those in the other groups did (F 3,105 = 6.07, P = 0.003; custody versus apprentice, P = 0.006, custody versus guide, P = 0.008; custody versus pet, P = 0.004). The four groups of dogs differed significantly in their disposition to play (F 3,105 = 4.75, P = 0.004). In particular, pet dogs played significantly less than custody and apprentice dogs did (pet versus custody, P = 0.026; pet versus apprentice, P = 0.027). Although to a lesser extent also guide dogs were less playful compared to the custody and apprentice ones (guide versus custody, P = 0.072; guide versus apprentice, P = 0.07). The trend observed in play behaviour was mainly determined by SST procedure (F 6,630 = 238.59, P 0.0001): in fact play activity was high during episodes 3, 4, 6, and 7 when the owner or the stranger encouraged the dogs to play. However, comparing the amount of play with the owner with the amount of play with the stranger, the ANOVA detected a significant interaction between dog groups and human playmate (F 3,105 = 7.76, P < 0.0001; Fig. 3). A part from guide dogs, whose owner had obvious constraints in playing, all the other dogs preferred to play with their owner, even though this preference was significant only in pet dogs (P = 0.0005). The dogs’ behavioural response to isolation (episode 5) was characterised not only by remaining oriented to the door but also by protest behaviours such as scratching the door and vocalizing. Scratching the door occurred in all groups but custody dogs were more prone to engage in this behaviour (F 3,105 = 2.636, P = 0.054). The ANOVA carried out on whining showed significant differences among groups (F 3,105 = 6.44, P = 0.0004). In particular apprentice dogs whined significantly less than custody and pet dogs when alone in the experimental room (training versus custody, P = 0.0027; apprentice versus pet, P = 0.0009). On the contrary, pet dogs tended to bark more than the other groups did (F 3,105 = 2.35, P = 0.07).
Fig. 3. Mean frequency of play behaviour with stranger and with owner expressed by custody, apprentice, guide and pet dogs during the SST. Differing letters indicate P < 0.001.
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Fig. 4. Mean frequency of puppet fear behaviours expressed by custody, apprentice, guide and pet dogs during the SST.
There was a significant difference between groups in fear reaction towards the puppet (fear of puppet: F 3,105 = 3.004, P = 0.034; Fig. 4): untrained dogs (i.e. custody and pet dogs) were more fearful than trained ones. Moreover, custody dogs approached the puppet more often than guide dogs (F 3,105 = 2.951; P = 0.036; custody versus guide: P = 0.024). Fear reactions and approaches to puppet, occurred mainly in episode 1 (fear of puppet, F 6,105 = 14.015, P 0.0001; episode 1 versus all other episodes, P < 0.0001. Approach to puppet, F 6,105 = 18.78, P 0.0001; episode 1 versus all other episodes, P < 0.0001). Similarly, puppet exploration decreased across the SST (exploration puppet, F 6,105 = 41.13, P 0.0001; episode 1 versus episode 2, P = 0.02; episode 1 versus all the other episodes, P < 0.0001). Exploration of the room declined sharply during the procedure (F 6,105 = 325.8, P 0.0001; episode 1 versus all the others, P < 0.0001) with only a slight increase in episode 5 (episode 5 versus episode 3, P = 0.06; episode 5 versus episode 6, P = 0.008; episode 5 versus episode 7, P = 0.001). In all groups locomotion markedly decreased from episode 1 to 4, increasing again in episode 5 when the dogs were alone (F 6,105 = 29.058, P 0.0001; episode1 versus episode 5, P = 0.01; episode 1 versus all the others, P < 0.0001; episode 5 versus episode 2, 3, 6, and 7, P < 0.0001). Guide dogs were more passive than those in the custody and apprentice groups (F 3,105 = 5.16, P = 0.002; guide versus custody, P = 0.012; guide versus apprentice, P = 0.006). Even though guide dogs were more passive and did not play more than the other groups, they drank more than custody and pets did (F 3,105 = 4.599, P = 0.005; guide versus custody, P = 0.004; guide versus pet, P = 0.044). 3.3. Effects of breed on strange situation behaviour Main differences between Golden and Labrador retrievers are shown in Fig. 5. Golden retrievers engaged in proximity seeking behaviour significantly more than Labrador retrievers (F 1,93 = 4.28, P = 0.041), and were also more prone to stay in physical contact with both the owner (F 1,93 = 3.05, P = 0.08) and the stranger (F 1,93 = 15.48, P < 0.0001). In addition, when alone in the room they whined significantly more than Labrador retrievers did (F 1,93 = 18.89, P < 0.0001). Finally, they tended to be more passive
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Fig. 5. Mean frequency of proximity seeking, contact with stranger, whining and locomotion expressed by Golden and Labrador retrievers during SST. *P < 0.05; ***P < 0.0001.
(F 1,93 = 3.31, P = 0.07) and showed a significantly higher locomotor activity (F 1,93 = 31.58, P < 0.0001). On the contrary, Labrador retrievers tended to be more playful (F 1,93 = 3.37, P = 0.069) and to explore more the environment and the puppet (room, F 1,93 = 3.15, P = 0.07; puppet, F 1,93 = 3.46, P = 0.06).
4. Discussion While pet dogs kept for companionship usually spend all their life with the same human companion, guide dogs in the first 2 years of their lives experience three different bonds: they are initially grown up by puppy walkers, then trained by school trainers and eventually they are assigned to the blind people. The aim of the present study was to investigate whether this peculiar experience affects the eventual bond developed by a guide dog towards the blind person. The strange situation test highlighted three main dimensions of dogs’ behaviour: proximity seeking, playfulness and fearfulness. Proximity seeking and playfulness are two competing aspects of the factor we labelled ‘‘response to the SST’’. Proximity seeking included behaviours aimed at maintaining or regaining contact with the owner/stranger and playfulness included individual and social play. This finding suggests that the stressfulness of the SST elicited in some subjects an anxious attachment which interfered with play behaviour and in some subjects a more secure attachment which allowed the expression of play behaviour throughout the test. This is in agreement with previous evidence that a condition of distress and the sense of insecurity are not compatible with play activities in human infants, nonhuman primates and dogs (Ainsworth et al., 1978; Bard, 1991; Prato Previde et al., 2003). The two different profiles of response to the strange situation test are overall in line with previous data published by Topa`l et al. (1998). Although with some methodological differences in data collection and analysis, these authors described the human–dog relationship in the SST as characterized by three dimensions, anxiety, acceptance and attachment, which included the main behaviours enclosed in our proximity seeking and playfulness dimensions.
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Furthermore, our experimental set-up characterized by the presence of a strange and potentially frightening puppet determined the appearance of a second dimensional factor expression of fearfulness, ‘‘fear of the puppet’’. When faced with the puppet, and despite the presence of the owner, some dogs reacted by staring at it from a distance and avoided it when moving around the room, whereas other dogs ignored the stimulus or even approached and explored it. Fearfulness is a relevant trait of dog temperament and can impair the success of training because a fearful reaction from a guide dog could expose its blind owner to vehicular flow or other dangerous events (Baillie, 1972). In our groups of dogs, the more anxious during the SST were pet dogs: they showed the highest level of proximity seeking towards the owner but also towards the stranger, and remained oriented to the door more when the stranger was in the room. Furthermore, they showed the highest level of vocal protest (i.e. barking) during isolation, a lower level of play activity (especially when alone with the stranger) and a high amount of passive behaviour. A less anxious reaction to separation was observed in both custody and apprentice dogs which were more playful and engaged less in proximity seeking behaviours; in particular custody dogs were extremely friendly towards the stranger. This could be the result of a number of different factors, such as the success of the puppy walking program aimed at socializing puppies with humans and/or the effect of age. Young dogs are in general more prone to play and in the case of apprentice dogs the less consolidated relationship with the trainer might also have played a role. Nevertheless, it is worth noting that those apprentice dogs which engaged significantly less in play activities failed to become guide dogs, confirming a negative relationship between playfulness and anxiety. Interestingly guide dogs’ behaviour was in a number of aspects in-between that exhibited by pets and that shown by custody and apprentice dogs, suggesting that they can be viewed as ‘‘working pets’’. In fact, in spite of separation from previous attachment figures guide dogs expressed their attachment to the owner showing the same whole range of proximity seeking behaviours observed in pet dogs. Guide dogs showed a clear preference for their owner and during separation episodes stood at the door as all the other dogs did. However, in guide dogs all these behaviours were expressed at a lower level than those observed in pets and comparable to those observed in younger dogs (custody and apprentice). This more controlled reaction could be a result of the training the aim of which is to reduce unnecessary excitability. In fact, only 12% of guide and 19% of apprentice dogs scratched the door during separation, compared to 44% of custody and 41% of pet dogs. The more controlled response to the SST observed in guide dogs could also depend on some active selection for emotional stability carried out on the bitches belonging to the school breeding program. Nevertheless, as previously pointed out, our sample of guide dogs included also subjects obtained from various commercial breeders, therefore guide and pet dogs should have been comparably heterogeneous. However, in guide dogs, a certain unavoidable level of distress was detectable in the polydipsia (Askew, 1996) and in the marked passivity shown. The fact that guide dogs were more passive, besides being a sign of anxiety (Topa`l et al., 1998), could be the result of their habituation to restrained activity. There are several situations in which a guide dog is required to remain passive: when off duty it may have to lie quietly near the blind owner for long periods while the owner eats, works, attend a show, etc.
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Guide dogs showed other behaviours that seemed to be dependent on the specific training received. They kept physical contact with their owner significantly more than the other dogs. This behavioural pattern, which is considered a sign of attachment (Topa`l et al., 1998; Prato Previde et al., 2003) could have been enhanced by the training procedure during which dogs learn to communicate physically their presence to the owner. In fact the training requires the dogs to touch owner’s leg with their muzzle when called and to keep strict contact with the owner’s leg while walking on duty (unpublished guideline for internal use of the trainers). This finding is also supported by the evidence that along an obstacle course guide dogs maintain more physical contact in comparison with pet and police dogs (Naderi et al., 2002). Group differences were observed also in the reaction to the strange/bizarre stimulus. Not surprisingly guide and apprentice dogs were less fearful towards the puppet than custody and pet dogs. This difference in fearfulness is mainly due to the training that focalises dogs’ attention on specific stimuli which are relevant to the guide-work: this seems the best approach to reduce fearful reaction in guide dogs (Goddard and Beilharz, 1984). Our bizarre puppet mimicked a vertical strange still object that could be encountered along a city walk, and it elicited avoidance behaviours mainly in untrained dogs. In such a complex service, traditionally the German Shepherd has been the breed of choice (Willis, 1995) but in more recent years there has been an increase in the use of both Labrador and Golden retrievers which are considered more sociable, less aggressive and possessive and also more adaptable to restrained activity (Witchel, 1996; Svatberg and Forkman, 2002). In this study we found that Golden retrievers showed a shyer and more insecure temperament than Labrador retrievers who were more playful and explorative. The behavioural profile of Golden retrievers is in agreement with findings reported by Hart and Miller (1985). These authors interviewed many trainers and dog specialists: Golden retrievers were described as very trainable dogs with a high attitude to play, but also as very timid with high affectional demand. In our opinion, these temperament differences should not be considered as a ‘‘mistake’’ in selection program but rather an important source of variability: as people differ from each other in their temperament, variability in guide dogs is necessary to assure an optimal blind owner-dog matching. In summary, the results of the present study indicate that guide dogs are able to form an intense bond with their blind owners, and this attachment appears to be modulated by the experience of the training. Although the ability to form attachment is associated with an early sensitive period, Ga`csi et al. (2001), who studied the effect of brief interactions with an unfamiliar human on the development of attachment behaviour of sheltered adult dogs, demonstrated that these interactions may result in attachment behaviour. Nevertheless, adult dogs adopted from shelters and tested in the SST showed more anxious and insecure bond with new owners (Prato Previde et al., 2003). However, the breakdown of the two bonds formed by the guide dogs is not a traumatic event comparable to that experienced by dogs abandoned in rescue shelters (Mondelli et al., 2003). In fact, while living with the puppy walkers, dogs are accustomed to visit the school monthly for the sanitary check-up and vaccinations, and most of all, to stay overnight in the school kennel with other dogs. This protocol was introduced 5 years ago in the program of the National School for Guide Dogs to make less stressful the separation from the puppy-walker and to habituate dogs to unfamiliar people and to the kennel routine. Our study provides empirical support to the
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effectiveness of this protocol, since the breakdown of the bond with the puppy-walker does not negatively affect both the learning abilities and the capacity to re-establish an equilibrate bond with humans. 5. Conclusions Our data show that guide dogs form new affectional bonds whose quality and integrity is not compromised by the experience of separation per se and there is no evidence that, as suggested by Fox (1968), the loss of the first attachment figure causes behavioural problems in these dogs. A further step of this research on the characteristics of the attachment bond in guide dogs will be a longitudinal study carried out on a group of dogs and aimed at evaluating the development of the bond and the effect of age.
Acknowledgments We are especially indebted to the staff of the ‘‘Scuola Nazionale Cani Guida per Ciechi-Regione Toscana’’ for providing dogs and logistical support, and for time devoted to discussion and helpful comments. We also thank Jenny Bertozzi and Emmanuela Diana for their invaluable assistance in collecting data. Finally, a special warm thanks to the puppy walkers, the trainers, the owners and the dogs for participating in the project. We are very grateful to Marco Poli for his interest and support of the project and for allowing us to carry out the work on pet dogs at the Psychology Institute of Universita` di Milano. We thank Orazio Rossi and Lamberto Soliani (Universita` di Parma) for statistical advice. This research was funded by Universita` di Milano (FIRT 2003) and MIUR (Ministero dell’Istruzione, dell’Universita` e della Ricerca-PRIN 2004) grants to Emanuela Prato-Previde, by Universita` di Parma (FIL 2003) and MIUR (PRIN 2004) grants to Paola Valsecchi and by Unione Italiana dei Ciechi Postdoctoral Grant to Gaia Fallani.
References Ainsworth, M.D.S., Bell, S.M., 1970. Attachment, exploration, and separation: illustrated by the behaviour of oneyear-olds in a strange situation. Child Dev. 41, 49–67. Ainsworth, M.D.S., Blehar, M.C., Waters, E., Wall, S., 1978. Patterns of Attachment: A Psychological Study of the Strange Situation. Lawrence Erlbaum Associates, Hillsdale, NJ. Askew, H.R., 1996. Treatments of Behaviour Problems in Dog and Cat. A Guide for the Small Animal Veterinarian. Blackwell Science, Oxford. Baillie, J.R., 1972. The behavioural requirements necessary for guide dogs for the blind in the United Kingdom. Br. Vet. J. 128–477. Bard, K., 1991. Distribution of attachment classifications in nursery chimpanzees. Am. J. Primatol. 24, 88. Bartlett, M.S., 1947. The use of transformations. Biometrics 3, 39–52. Clutton-Brock, J., 1999. A Natural History of Domesticated Mammals, 2nd ed. Cambridge University Press, Cambridge.
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Cooper, J.J., Ashton, C., Bishop, S., West, R., Mills, D.S., Young, R.J., 2003. Clever hounds: social cognition in the domestic dog (Canis familiaris). Appl. Anim. Behav. Sci. 81, 229–244. Fox, M.W., 1968. The influence of domestication upon Behaviour of animals. In: Fox, M.W. (Ed.), Abnormal Behaviour in Animals. Saunders, Philadelphia, pp. 64–76. Ga`csi, M., Topa`l, J., Miklo`si, A., Do`ka, A., Csa`ni, V., 2001. Attachment behaviour of adult dogs (Canis familiaris) living at rescue centers, forming new bonds. J. Comp. Psychol. 115 (4), 423–431. Goddard, M.E., Beilharz, R.G., 1984. A factor analysis of fearfulness in potential guide dogs. Appl. Anim. Behav. Sci. 12, 253–265. Hare, B., Brown, M., Williamson, C., Tommasello, M., 2002. The domestication of social cognition in dogs. Science 298, 1634–1636. Hart, B.L., Miller, M.F., 1985. Behavioural profiles of dog breeds. J. Am. Vet. Med. Assoc. 186 (11), 1175–1180. Kaminsky, J., Call, J., Fisher, J., 2004. Word learning in a domestic dog: evidence for ‘‘fast mapping’’. Science 304, 1682–1683. ´ ., Csa`nyi, V., 2003. Dogs (Canis familiaris) learn from their owners via Kubinyi, E., Topa`l, J., Miklo`si, A observation in a manipulation task. J. Comp. Psychol. 117, 156–165. ´ ., Kubinyi, E., Topa`l, J., Ga`csi, M., Vira´nyi, Z., Csa`nyi, V., 2003. A simple reason for a big difference: Miklo`si, A wolves do not look back at humans, but dog do. Curr. Biol. 13, 763–766. Mondelli, F., Zannoni, S., Berretta, V., Accorsi, P.A., Valsecchi, P., 2003. Behavioural adaptation of dogs entering a rescue shelter. In: Proceedings of the ASAB Summer Meeting, Grunau, Austria. ´ ., Do`ka, A., Csa`nyi, V., 2001. Co-operative interactions between blind persons and their Naderi, Sz., Miklo`si, A dogs. Appl. Anim. Behav. Sci. 74, 59–80. ´ ., Do`ka, A., Csa`nyi, V., 2002. Does dog–human attachment affect their inter-specific Naderi, Sz., Miklo`si, A cooperation? Acta Biol. Hun. 53 (4), 537–550. Pfaffenberger, C.J., Scott, J.P., Fuller, J.L., Ginsburg, B.E., Bielfelt, S.W., 1976. Guide Dogs for the Blind: Their Selection, Development, and Training. Elsevier Scientific Publishing Company, Amsterdam. Prato Previde, E., Custance, D.M., Spiezio, C., Sabatini, F., 2003. Is the dog–human relationship an attachment bond? An observational study using Ainsworth’s strange situation. Behaviour 140, 225–254. Prato Previde, E., Fallani, G., Valsecchi, P., 2005. Gender differences in owners interacting with pet dogs: an observational study. Ethology 111, 1–16. Schleidt, W.M., Schleidt, M.D., 2003. Co-evolution of humans and canids. An alternative view of dog domestication: Homo Homini Lupus? Evol. Cogn. 9, 57–72. Serpell, J.A., Hsu, Y., 2001. Development and validation of a novel method for evaluating behaviour and temperament in guide dogs. Appl. Anim. Behav. Sci. 72, 347–364. Serpell, J., Jagoe, J.A., 1995. Early experience and development of behaviour. In: Serpell, J. (Ed.), The Domestic Dog: Its Evolution, Behaviour, and Interactions with People. Cambridge University Press, Cambridge, pp. 79– 102. Slabbert, J.M., Rasa, A.E., 1997. Observational learning of an acquired maternal behaviour pattern by working dog pups: an alternative training method? Appl. Anim. Behav. Sci. 53, 309–316. ´ ., Csa`nyi, V., Topa`l, J., 2001. Comprehension of human communicative signs in pet dogs Soproni, K., Miklo`si, A (Canis familiaris). J. Comp. Psychol. 115 (2), 122–126. Svatberg, K., Forkman, B., 2002. Personality traits in the domestic dog (Canis familiaris). Appl. Anim. Behav. Sci. 79, 133–155. ´ ., Csa`nyi, V., Do`ka, A., 1998. Attachment behavior in dogs (Canis familiaris): a new Topa`l, J., Miklo`si, A application of Ainsworth’s (1969) strange situation test. J. Comp. Psychol. 112 (3), 219–229. Willis, M.B., 1995. Genetic aspects of dog behaviour with particular reference to working ability. In: Serpell, J. (Ed.), The Domestic Dog: Its Evolution, Behaviour, and Interactions with People. Cambridge University Press, Cambridge, pp. 52–64. Witchel, A., 1996. Teaching man’s best eyes to see. The New York Times, C1, C9, March 6.
Do disrupted early attachments affect the relationship between guide dogs and blind owners? Gaia Fallani a,*, Emanuela Prato Previde a, Paola Valsecchi b a
Istituto di Psicologia, Universita` degli Studi di Milano, via Tommaso Pini 1, 20134 Milano, Italy b Dipartimento di Biologia Evolutiva e Funzionale, Universita` degli Studi di Parma, Parco Area delle Scienze 11 A, 43100 Parma, Italy Accepted 11 December 2005 Available online 19 January 2006
Abstract The study investigated the affectional bond developed by dogs (Canis familiaris) towards their human companions during the selection process to become guide dogs and compared this bond with that formed by pet dogs with their owners. One hundred and nine dog-owner pairs were tested using a modified version of the Strange Situation Test: custody dogs-puppy walkers (n = 34), apprentice dogs-trainers (n = 26), guide dogs-blind owners (n = 25) and pet dogs-owners (n = 24). Twenty-six behaviours were scored using a 5 s point sampling method and two vocal behaviours were recorded as bouts. Factor analysis carried out on 24 mutually exclusive behaviours highlighted two different profiles of response. A relaxed reaction characterised by a high play activity was distinctive of custody and apprentice dogs, whereas an anxious reaction characterised by a high degree of proximity seeking behaviours was distinctive of pet dogs. Guide dogs were intermediate between these two extremes, expressing their attachment to the owners but showing a more controlled emotional reaction. This finding suggests that guide dogs can be viewed as ‘‘working pets’’. Furthermore, the experimental set-up, characterised by the presence of a frightening stimulus, revealed that untrained dogs (pets and custody dogs) were more fearful than trained dogs (guide dogs and apprentice dogs). Finally, differences in temperament emerged between retrievers: Golden retrievers showed a higher level of affection demand while Labrador retrievers were more playful.
* Corresponding author. Tel.: +39 0521 905671; fax: +39 0521 905657. E-mail address: [email protected] (G. Fallani). 0168-1591/$ – see front matter # 2005 Elsevier B.V. All rights reserved. doi:10.1016/j.applanim.2005.12.005
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Overall, these findings show that in spite of separations from previous attachment figures, guide dogs established with their blind owner a rather good and secure affectional bond. # 2005 Elsevier B.V. All rights reserved. Keywords: Guide dogs; Behaviour; Attachment
1. Introduction The dog (Canis familiaris) was the first animal domesticated by human kind (Homo sapiens) and since ancient times has been kept for companionship and for cooperating on a variety of tasks, thus it consolidated a strict and intense relationship with humans (CluttonBrock, 1999; Schleidt and Schleidt, 2003). As a consequence of this long lasting association dogs sharpened some behavioural and cognitive characteristics already present in their co-operative ancestor the wolf as a result of a ‘‘process of enculturation’’ (Hare et al., 2002). Recent research showed that dogs’ social cognitive skills allow them to engage in complex and effective interactions with humans (for a review see Cooper et al., 2003). For example, there is evidence that dogs can learn socially from conspecifics or human beings (Slabbert and Rasa, 1997; Kubinyi et al., 2003), are able to use different human social signs (e.g. looking or pointing) as information sources to solve a task (Soproni et al., 2001; Miklo`si et al., 2003) and engage in complex communication with people (Kaminsky et al., 2004). Today in many western countries dogs are trained to provide help and to cooperate with humans in tasks that involve a particular training and require specific skills and variable levels of co-operation with the human companion (i.e. searching for objects or persons, assisting disabled people, etc.). Among assistance dogs, guide dogs for the blinds provide an interesting example as the blind owner depends completely on his/her dog for visual information and the dog does not know about the planned actions of its owner (Naderi et al., 2001). Such a delicate and subtle equilibrium requires a peculiar development of co-operation and of a strong but at the same time balanced bond. There is now evidence suggesting that the dog–human affectional bond can be characterised as an attachment: dogs show towards their owner attachment behaviours which closely resemble those reported in human infants and chimpanzees (Topa`l et al., 1998; Prato Previde et al., 2003). In order to form a good and secure affectional bond with humans a dog needs to be precociously introduced to them and to socialise during a specific sensitive period (for a review see: Serpell and Jagoe, 1995). Pfaffenberger et al. (1976) observed that puppies that lived in a kennel for 12 weeks or more after birth, and therefore could not familiarise with people, were generally insecure even if accompanied by their attachment figure and rarely succeeded in becoming guide dogs. In addition, traumatic experiences like abandonment or in general the break down of an already established bond may favour the appearance of behavioural problems thus compromising the dog–human relationship (Fox, 1968). Serpell and Hsu (2001), in a questionnaire study, found that a wrong or excessive attachment during the first period of life can determine a negative evaluation of the dog by trainers and
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its failure to become a guide dog. In particular it emerged that puppies that scored very high in attachment towards their puppy-walker and his/her family were rejected because judged too emotional and excitable and excessively protective and aggressive towards strangers. Guide dogs form their bond with the blind person after a long period of intense training and after the formation and break down of two previous important affectional bonds with different attachment figures: the puppy-walker (during the first year of life) and the trainer (during the period of training). The relationship a potential guide dog forms with the puppy-walker and the trainer and the break down of these bonds may have a negative influence on the animal’s behaviour that could in turn compromise either successful training or the relationship with the blind person. To test this hypotheses, the present study investigated the bond developed by dogs towards their human companions during the selection process to become guide dogs, and compared this bond with that formed by pet dogs with their owner(s). This goal was attained using the Strange Situation Test (SST) a procedure that has proved to be useful in investigating the dog–human relationship (Topa`l et al., 1998; Prato Previde et al., 2003, 2005). The behaviour of four groups of dogs during the SST was evaluated considering four different kinds of attachment figures: the puppy-walker, the trainer, the blind owner and the pet owner. As our sample of dogs was rather large and included mainly Labrador and Golden retrievers we investigated also the differences between these breeds in the attachment bond.
2. Methods 2.1. The school The ‘‘Scuola Nazionale Cani Guida per Ciechi-Regione Toscana’’ (National School for Guide Dogs, Scandicci, Italy) trains and provides to blind people about 50 dogs per year. The school has some breeding dogs which live in private household and reproduce once per year. In addition, the school purchases puppies from different breeders located in Tuscany. Puppies are placed with volunteer puppy walkers at 40 days of age and raised in puppy walkers’ homes until they are about 12 months old. During this period of time they periodically go back to the school to become familiar with the place and the people. At 12 months of age the dogs return to the school to start a training lasting approximately 6–8 months. The training takes place under the management of a single trainer. At the end of training, guide dogs are assigned to blind people: the dog-blind matching is mediated by school assistants during a 20 days course involving the new blind-dog pair. One year after the assignment of the guide dog, the blind person comes back to the school with his/her dog for the first evaluation of the success of the dog-blind pair. 2.2. Subjects One hundred and nine dogs (34 males, 75 females) were tested from February 2003 to December 2004. The sample included 42 Golden retrievers, 53 Labrador retrievers, 8 Golden Labrador crosses, and 6 German Shepherds.
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The dogs belonged to one of following four groups: Custody: This group consisted of 34 dogs (11 intact males and 23 intact females) ranging from 11 to 15 months of age (X S.E. = 11.6 1.3). The dogs were tested 1 month before returning to the school for the training, and therefore their attachment figure in the strange situation test (SST) was the puppy walker. Apprentice: This group consisted of 26 dogs (4 neutered males, 6 intact males and 16 intact females) ranging from 12 to 20 months of age (X S.E. = 16 2.1). The dogs were tested after 2 months of training and therefore their attachment figure in the SST was the trainer. Guide: This group consisted of 25 dogs (6 neutered males and 19 intact females) ranging from 33 to 50 months of age (X S.E. = 37.6 7.8). The dogs were tested after 1 year of service during the annual control and their attachment figure in the SST was the blind owner. Pet: The group consisted of 24 dogs (7 males and 17 females) ranging from 11 to 49 months of age (X S.E. = 29.3 11.4). All the dogs were kept exclusively for companionship and lived within the human household and, therefore, their attachment figure in the SST was their owner. All human participants were volunteers: puppy walkers, trainers and blind persons were recruited from the National School for Guide Dogs while pet owners were recruited from advertisements distributed within the University of Milan. For sake of simplicity all attachment figures will be called ‘‘owners’’ from now on. 2.3. Set-up Experimental sessions were carried out in two rooms (15 m2 surface); the first room was located at the National School for Guide Dogs and the second one at the Institute of Psychology of the University of Milan. Both rooms were unfamiliar to the dogs and their set-up was similar to that described by Ainsworth and Bell (1970); they were equipped with two chairs (one labelled as ‘‘stranger’’ and the other as ‘‘owner’’), a selection of dog toys (one large and two small balls, two plastic bottles, a rope pull-toy and a squeaky toy), a water bowl and a videocamera (Handycam Video HI 8, Sony, Tokyo) connected with a monitor positioned outside the experimental room so that each session could be independently observed. Furthermore, a 1 m high homemade puppet similar to advertising Norwegian trolls was situated in the corner opposite to the door. The puppet was unknown to dogs and had some anomalous morphological characteristics such as a very long nose, big eyes and long curled green hairs. 2.4. Procedure The study was carried out using a modified version of Ainsworth’s strange situation test (Prato Previde et al., 2003). The entire procedure consisted of an introductory episode followed by 7 three-minute experimental episodes in which dogs were placed in an unfamiliar room, introduced to a female unfamiliar stranger and subjected to two short
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Table 1 Description of the Strange Situation Procedure Episode
Description
Episode 1: owner and dog Episode 2: owner, dog and stranger
The owner sat quietly and the dog was free to explore the room The stranger entered the room, sat quietly for 1 min, conversed with the owner for the second minute, approached the dog and attempted to stimulate play during the last minute. At the end of this episode the owner left the room unobtrusively The stranger continued to play with the dog if it was willing; if it was inactive or distressed, the stranger attempted to distract it with play or by providing verbal and tactile comfort The owner entered the room and greeted and/or comforted his/her dog as usual after returning from work or shopping. The stranger quietly exited the room. The owner had been told that he/she was free to play with the dog throughout the episode. At the end of this episode the owner left the room The dog remained alone for 3 min, but was constantly observed by the owner and researchers on the monitor in the adjacent room The stranger entered the room and followed the same protocol as in episode 3 The owner entered the room greeted the dog as though he/she had just returned from work or shopping. The stranger left the room unobtrusively. At the end of this episode the experimenter arrived and officially terminated the procedure
Episode 3: stranger and dog (first separation episode) Episode 4: owner and dog (first reunion episode)
Episode 5: dog alone (second separation episode) Episode 6: stranger and dog Episode 7: owner and dog (second reunion episode)
episodes of separation from their owners. The experimental episodes are detailed in Table 1. On their arrival human–dog pairs were escorted to a waiting room where the procedure was briefly described to the owners who were asked to subscribe the permission to use the data collected according to the national Privacy Law 675/36. Then, the video camera was activated and the participants were escorted to the experimental room for testing. Blind owners were helped by an assistant in subscribing the permission and were always escorted in and out the experimental room. Immediately after each session, the experimental room, water bowl and toys were washed using a non-toxic, weakly scented disinfectant. 2.5. Data collection and statistical analysis The behaviour of each dog during the experimental episodes was videotaped and analysed by three trained observers using a 5 s point sampling and a total of 26 behaviours were recorded (see Table 2 for a detailed description of the behavioural categories). Inter observer reliability was assessed by means of independent parallel coding of a random sample of videotaped sessions (i.e., 10%) and calculated as percentage agreement; percentage agreement was always more than 91%. Behaviours were mutually exclusive except ‘‘physical contact’’, ‘‘barking’’ and ‘‘whining’’, which could be associated with other behaviours. The two vocal behaviours were recorded only in episode 5, when the dogs remained alone, and were collected as bouts. The occurrence of each behaviour was calculated as a proportion of the total number of events scored while the occurrence of each
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Table 2 Behaviours recorded in the strange situation procedure Categories
Behaviours
Definition
Proximity seeking
Oriented to person
Staring fixedly at the owner (OPO) or stranger (OPS), regardless of whether the behaviour was reciprocated Approaching while clearly visually oriented to owner (AO) or stranger (AS), either spontaneously or when called Following the owner (FO) or the stranger (FS) around the room or to the door Staring fixedly at the door, either when close to it or from a distance (OD)
Approach person
Following Oriented to door Playfulness
Social play
Individual play
Any vigorous or galloping gaited behaviour performed when interacting with the owner (PLO) or stranger (PLS); including running, jumping, active physical contact and chasing toys Any vigorous or galloping gaited behaviour directed toward a toy when clearly not interacting with persons; including chewing, biting, shaking from side to side, scratching or batting with the paw, chasing rolling balls and tossing using the mouth (PLI)
Puppet fear
Stare at the puppet Avoid puppet
Staring fixedly at the puppet from a distance (SPP) Avoiding proximity with the puppet when moving around the room (WP)
Other behaviours
Exploration
Activity directed toward physical aspects of the environment (E) or toward puppet (EP), including sniffing, close visual inspection (EV), and gentle oral examination such as licking Sitting, standing or lying down without any obvious orientation toward the physical or social environment (PA) Walking, pacing or running around, without exploring environment or playing Staring fixedly at the owner’s (OCO) or stranger’s (OCS) empty chair Approaching while clearly visually oriented to puppet (AP) All active behaviours resulting in physical contact with the door, including scratching the door with the paws, jumping on the door, pulling on the door handle with the forelegs or mouth (S) Drinking at the water bowl (D) All greeting behaviours toward the entering owner (GO) or stranger (GS), such as approaching, tail wagging, jumping, physical contact Being in physical contact with owner (CO) or stranger (CS) Barking (B) and whining (W) (recorded as bouts only during the fifth episode)
Passive behaviour
Locomotion Oriented to chair Approach puppet Scratch the door
Drink Greeting behaviour
Physical contact Vocalising
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vocal behaviour was calculated as bouts per second. To achieve normality, the proportions were arcsine transformed using Bartlett’s correction for continuity (Bartlett, 1947). Factor analysis was used as an exploratory tool to have a general view of the dogs’ reaction to the SST and to extract the maximum information contained in the multivariate data set. The analysis output allowed to extract the patterns of correlation among the 24 mutually exclusive behaviours and to group 12 behaviours into three wider behavioural categories. The behavioural categories identified through factor analysis and the other behaviours not grouped were then used as dependent variables in the analysis of variance. As the high number of possible independent variables (i.e. dogs’ age, sex, group, breed, and owner’s gender) would have excessively fragmented the sample, only the dogs’ group and breed were considered as factors in the ANOVAs. The dogs’ age was not considered because the protocol for selection and training of guide dogs established age limits for the recruitment of dogs: therefore, the dogs still living in the adoptive families, those under training and guide dogs were necessarily in different stages of their development. The sex of the dog and the gender of the owner were omitted because preliminary ANOVA’s (not included for simplicity) revealed that these variables did not affect behaviour (see Table 3 for distribution of sex and breeds among the four different experimental groups). The behaviour of the four groups of dogs across the episodes was analysed using a oneway ANOVA for repeated measures with groups (four levels: custody, apprentice, guide, pet) as between-subjects factor, and time (seven levels: episode 1 to episode 7) as withinsubjects factor. Furthermore, to detect differences in behaviour towards the owner and the stranger a second ANOVA for repeated measures was carried out comparing episodes characterised by the exclusive presence of the owner (episodes 4 + 7) with those characterised by the exclusive presence of the stranger (episodes 3 + 6). Breed differences in behaviour were assessed using a one-way ANOVA with breeds (two levels: Golden and Labrador) as between-subject factor. Since most of the dogs were Golden and Labrador Retrievers, German Sheperd (N = 6) and Labrador Golden crosses (N = 8) were excluded from this analysis. As vocalizations were recorded only in episode 5, differences in barking and whining were assessed by means of one-way ANOVA with groups (four levels: custody, apprentice, guide, pet) as independent variable(s). Table 3 Distribution of sex and breeds between the four different experimental groups Group of dogs
Females
Males
Custody
23 (13 Golden retrievers, 5 Labrador retrievers, 5 Labrador Golden crosses) 16 (8 Golden retrievers, 6 Labrador retrievers, 2 German Shepherds) 19 (3 Golden retrievers, 14 Labrador retrievers, 2 German Shepherds) 17 (7 Golden retrievers, 10 Labrador retrievers)
11 (5 Golden retrievers, 3 Labrador retrievers, 3 Labrador Golden crosses) 10 (7 Golden retrievers, 1 Labrador retriever, 2 German Shepherds) 6 Golden retrievers
Apprentice
Guide
Pet
7 (3 Golden retrievers, 4 Labrador retrievers)
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For all ANOVAs, Tukey’s HSD test was carried out to detect differences in single comparisons (level of significance: a = 0.05). Statistical analysis was carried out using the statistical package SPSS 11.0TM.
3. Results 3.1. Factor analysis Factor analysis based on the data of the 109 dogs extracted eight primary factors: first, second and third factors, accounted for 43% of the variance. Any loading of 0.6 or above was considered highly significant for this sample size and was used as a criterion when considering the relevance of the variable loading on each factor. This criterion was fulfilled only by first and second factor variables, while the remaining six factors contained behavioural items for which there was no clear correlation (Table 4). The first factor explained 26% of variance and had ten high loadings: seven variables had a positive loading and three a negative one. The positive loading characterised ‘‘oriented to door’’ (0.606), ‘‘follow owner’’ (0.663) or ‘‘follow stranger’’ (0.671), ‘‘approach owner’’ (0.618) or ‘‘approach stranger’’ (0.698) and ‘‘oriented to owner’’ (0.732) or ‘‘oriented to stranger’’ (0.850). The three negative loadings characterised: ‘‘individual play’’ ( 0.718) and ‘‘play with owner’’ ( 0.634) or ‘‘play with stranger’’ ( 0.837). Based on this pattern of loadings this factor was labelled ‘‘response to the strange situation’’. In this factor two different profiles of response emerged: (1) a relaxed reaction characterised by a high play activity, and (2) an anxious reaction characterised by a high degree of proximity seeking behaviours aimed at keeping or regaining contact with the owner and the stranger. Consequently, two behavioural categories were defined: ‘‘playfulness’’ and ‘‘proximity seeking’’. The second factor accounted for 9% of variance and had only positive loadings: ‘‘stare at the puppet’’ (0.766) and ‘‘avoid puppet’’ (0.73). Based on this pattern of loadings this factor was labelled ‘‘fear of the puppet’’. 3.2. Effects of groups and episodes on strange situation behaviour The ANOVA for repeated measures revealed the existence of a number of interesting differences in behaviour among the four groups of dogs. Across the episodes of the test, dogs differed in proximity seeking behaviour (F 18,630 = 3.39, P < 0.0001; Fig. 1). In particular, in episodes 3 and 6 when the owner left the room leaving the dog alone with the stranger, pet dogs engaged in proximity seeking behaviours significantly more than custody and apprentice dogs (episode 3: pet versus custody, P = 0.01; pet versus apprentice, P = 0.018; episode 6: pet versus custody, P < 0.0001; pet versus apprentice, P < 0.0001). Fig. 1 shows that guide dogs engaged in proximity seeking behaviours more than custody and apprentice dogs but less than pet dogs. The highest frequency of proximity seeking was observed in episode 5 during which dogs were alone in the room (episode 5 versus all the other, P < 0.0001): it is worth noting, however, that the only proximity seeking behaviour the dogs could engage in during this episode was remaining
Table 4 Matrix of components from factor analysis Behaviours
1
2
3
4
5
6
0.218 0.354 0.126 0.606 0.718 0.837 0.634 0.558 0.487 0.732 0.850 0.254 0.156 0.162 0.663 0.671 0.618 0.698 3.673E 02 6.011E 02 2.398E 02 9.713E 02 0.541 0.180
0.251 7.736E 02 6.667E 02 4.239E 02 0.140 6.339E 02 0.211 0.122 0.107 9.879E 02 7.565E 02 0.766 0.539 0.319 9.988E 02 8.289E 02 0.246 6.887E 02 0.522 0.730 8.779E 02 0.355 0.131 5.962E 02
0.458 0.189 0.193 0.211 0.321 0.215 0.143 0.443 0.423 2.290E 02 0.151 3.043E 02 0.290 0.393 0.270 7.351E 02 0.267 0.142 1.070E 02 0.299 0.208 0.229 0.203 0.552
0.284 0.187 0.417 0.248 6.583E 02 0.238 0.336 0.132 0.402 0.225 0.179 0.146 0.237 5.239E 02 0.117 0.277 0.157 0.407 0.168 0.189 0.402 0.386 0.107 0.102
2.384E 02 0.289 0.255 0.164 9.433E 02 3.189E 02 4.97E 02 0.135 0.182 0.168 7.777E 02 0.256 0.425 0.263 0.104 0.133 6.282E 02 4.027E 02 0.584 0.386 0.407 0.223 0.132 7.240E 02
8.732E 02 1.320E 02 0.599 1.313E 02 0.154 6.102E 02 0.276 0.336 0.290 0.151 0.138 6.295E 02 9.613E 02 0.231 6.235E 02 0.278 9.791E 02 0.150 9.019E 02 7.872E 02 0.137 7.405E 02 0.252 0.475
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Exploration (E) Visual exploration (EV) Puppet exploration (EP) Oriented to door (OD) Individual play (PLI) Play with stranger (PLS) Play with owner (PLO) Passive (PA) Locomotion (L) Oriented to owner (OPO) Oriented to stranger (OPS) Oriented to puppet Oriented to owner chair (OCO) Oriented to stranger chair (OCS) Follow owner (FO) Follow stranger (FS) Approach owner (AO) Approach stranger (AS) Approach puppet (AP) Avoid puppet (WP) Scratch to the door (S) Drink (D) Greeting to owner (GO) Greeting to stranger (GS)
Components
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Fig. 1. Mean frequency of proximity seeking behaviours expressed by custody, apprentice, guide and pet dogs across the seven episodes of the SST. Differing letters indicate significant differences at P < 0.05 or lower.
oriented to the door sitting, standing or lying down in front of it or staring at it from a distance. In order to distinguish between behaviours directed towards the owner/stranger and aimed at staying in contact with them (i.e. follow, approach, oriented to person) and behaviours aimed at regaining contact with them when they were not in the room (i.e. oriented to the door) these two components of the proximity seeking category were divided and their occurrence in the presence of the stranger (episodes 3 + 6) and in the presence of the owner (episodes 4 + 7) was analysed separately. The ANOVA carried out on proximity seeking excluding being oriented to the door showed that dogs had an overall preference for their owners (F 1,105 = 10.98, P = 0.0012). On the contrary, all dogs remained oriented to the door significantly more often when the stranger was in the room and the owner was absent (F 3,105 = 6.39, P < 0.0001); this was particularly evident in pet dogs, and to a lesser extent in guide dogs (pet: owner versus stranger, P < 0.0001; guide: owner versus stranger, P = 0.10). In all groups physical contact with the owner increased across the SST (F 3,315 = 6.74, P < 0.001). Interestingly, guide dogs maintained physical contact with their blind owner significantly more compared to the dogs of the other groups (F 3,105 = 4.64, P = 0.004; guide versus custody, P = 0.005; guide versus apprentice, P = 0.014; guide versus pet, P = 0.067; Fig. 2). On the contrary, in all groups physical contact with the stranger was
Fig. 2. Mean frequency of physical contact with owner expressed by custody, apprentice, guide and pet dogs during the SST. Differing letters indicate significant differences at P < 0.05 or lower.
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maximum at the beginning of the test when they met her for the first time (episode 2, F 2,210 = 17.33, P < 0.0001). Finally, greeting behaviour towards the owner increased significantly from the first to the second reunion, and the same occurred with the stranger (owner: episode 4 versus episode 7, F 1,105 = 7.74, P = 0.006; stranger: episode 2 versus episode 6, F 1,105 = 9.3, P = 0.002). There were no group differences in greeting towards the owner upon reunion, but the dogs in the custody group greeted the stranger significantly more than those in the other groups did (F 3,105 = 6.07, P = 0.003; custody versus apprentice, P = 0.006, custody versus guide, P = 0.008; custody versus pet, P = 0.004). The four groups of dogs differed significantly in their disposition to play (F 3,105 = 4.75, P = 0.004). In particular, pet dogs played significantly less than custody and apprentice dogs did (pet versus custody, P = 0.026; pet versus apprentice, P = 0.027). Although to a lesser extent also guide dogs were less playful compared to the custody and apprentice ones (guide versus custody, P = 0.072; guide versus apprentice, P = 0.07). The trend observed in play behaviour was mainly determined by SST procedure (F 6,630 = 238.59, P 0.0001): in fact play activity was high during episodes 3, 4, 6, and 7 when the owner or the stranger encouraged the dogs to play. However, comparing the amount of play with the owner with the amount of play with the stranger, the ANOVA detected a significant interaction between dog groups and human playmate (F 3,105 = 7.76, P < 0.0001; Fig. 3). A part from guide dogs, whose owner had obvious constraints in playing, all the other dogs preferred to play with their owner, even though this preference was significant only in pet dogs (P = 0.0005). The dogs’ behavioural response to isolation (episode 5) was characterised not only by remaining oriented to the door but also by protest behaviours such as scratching the door and vocalizing. Scratching the door occurred in all groups but custody dogs were more prone to engage in this behaviour (F 3,105 = 2.636, P = 0.054). The ANOVA carried out on whining showed significant differences among groups (F 3,105 = 6.44, P = 0.0004). In particular apprentice dogs whined significantly less than custody and pet dogs when alone in the experimental room (training versus custody, P = 0.0027; apprentice versus pet, P = 0.0009). On the contrary, pet dogs tended to bark more than the other groups did (F 3,105 = 2.35, P = 0.07).
Fig. 3. Mean frequency of play behaviour with stranger and with owner expressed by custody, apprentice, guide and pet dogs during the SST. Differing letters indicate P < 0.001.
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Fig. 4. Mean frequency of puppet fear behaviours expressed by custody, apprentice, guide and pet dogs during the SST.
There was a significant difference between groups in fear reaction towards the puppet (fear of puppet: F 3,105 = 3.004, P = 0.034; Fig. 4): untrained dogs (i.e. custody and pet dogs) were more fearful than trained ones. Moreover, custody dogs approached the puppet more often than guide dogs (F 3,105 = 2.951; P = 0.036; custody versus guide: P = 0.024). Fear reactions and approaches to puppet, occurred mainly in episode 1 (fear of puppet, F 6,105 = 14.015, P 0.0001; episode 1 versus all other episodes, P < 0.0001. Approach to puppet, F 6,105 = 18.78, P 0.0001; episode 1 versus all other episodes, P < 0.0001). Similarly, puppet exploration decreased across the SST (exploration puppet, F 6,105 = 41.13, P 0.0001; episode 1 versus episode 2, P = 0.02; episode 1 versus all the other episodes, P < 0.0001). Exploration of the room declined sharply during the procedure (F 6,105 = 325.8, P 0.0001; episode 1 versus all the others, P < 0.0001) with only a slight increase in episode 5 (episode 5 versus episode 3, P = 0.06; episode 5 versus episode 6, P = 0.008; episode 5 versus episode 7, P = 0.001). In all groups locomotion markedly decreased from episode 1 to 4, increasing again in episode 5 when the dogs were alone (F 6,105 = 29.058, P 0.0001; episode1 versus episode 5, P = 0.01; episode 1 versus all the others, P < 0.0001; episode 5 versus episode 2, 3, 6, and 7, P < 0.0001). Guide dogs were more passive than those in the custody and apprentice groups (F 3,105 = 5.16, P = 0.002; guide versus custody, P = 0.012; guide versus apprentice, P = 0.006). Even though guide dogs were more passive and did not play more than the other groups, they drank more than custody and pets did (F 3,105 = 4.599, P = 0.005; guide versus custody, P = 0.004; guide versus pet, P = 0.044). 3.3. Effects of breed on strange situation behaviour Main differences between Golden and Labrador retrievers are shown in Fig. 5. Golden retrievers engaged in proximity seeking behaviour significantly more than Labrador retrievers (F 1,93 = 4.28, P = 0.041), and were also more prone to stay in physical contact with both the owner (F 1,93 = 3.05, P = 0.08) and the stranger (F 1,93 = 15.48, P < 0.0001). In addition, when alone in the room they whined significantly more than Labrador retrievers did (F 1,93 = 18.89, P < 0.0001). Finally, they tended to be more passive
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Fig. 5. Mean frequency of proximity seeking, contact with stranger, whining and locomotion expressed by Golden and Labrador retrievers during SST. *P < 0.05; ***P < 0.0001.
(F 1,93 = 3.31, P = 0.07) and showed a significantly higher locomotor activity (F 1,93 = 31.58, P < 0.0001). On the contrary, Labrador retrievers tended to be more playful (F 1,93 = 3.37, P = 0.069) and to explore more the environment and the puppet (room, F 1,93 = 3.15, P = 0.07; puppet, F 1,93 = 3.46, P = 0.06).
4. Discussion While pet dogs kept for companionship usually spend all their life with the same human companion, guide dogs in the first 2 years of their lives experience three different bonds: they are initially grown up by puppy walkers, then trained by school trainers and eventually they are assigned to the blind people. The aim of the present study was to investigate whether this peculiar experience affects the eventual bond developed by a guide dog towards the blind person. The strange situation test highlighted three main dimensions of dogs’ behaviour: proximity seeking, playfulness and fearfulness. Proximity seeking and playfulness are two competing aspects of the factor we labelled ‘‘response to the SST’’. Proximity seeking included behaviours aimed at maintaining or regaining contact with the owner/stranger and playfulness included individual and social play. This finding suggests that the stressfulness of the SST elicited in some subjects an anxious attachment which interfered with play behaviour and in some subjects a more secure attachment which allowed the expression of play behaviour throughout the test. This is in agreement with previous evidence that a condition of distress and the sense of insecurity are not compatible with play activities in human infants, nonhuman primates and dogs (Ainsworth et al., 1978; Bard, 1991; Prato Previde et al., 2003). The two different profiles of response to the strange situation test are overall in line with previous data published by Topa`l et al. (1998). Although with some methodological differences in data collection and analysis, these authors described the human–dog relationship in the SST as characterized by three dimensions, anxiety, acceptance and attachment, which included the main behaviours enclosed in our proximity seeking and playfulness dimensions.
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Furthermore, our experimental set-up characterized by the presence of a strange and potentially frightening puppet determined the appearance of a second dimensional factor expression of fearfulness, ‘‘fear of the puppet’’. When faced with the puppet, and despite the presence of the owner, some dogs reacted by staring at it from a distance and avoided it when moving around the room, whereas other dogs ignored the stimulus or even approached and explored it. Fearfulness is a relevant trait of dog temperament and can impair the success of training because a fearful reaction from a guide dog could expose its blind owner to vehicular flow or other dangerous events (Baillie, 1972). In our groups of dogs, the more anxious during the SST were pet dogs: they showed the highest level of proximity seeking towards the owner but also towards the stranger, and remained oriented to the door more when the stranger was in the room. Furthermore, they showed the highest level of vocal protest (i.e. barking) during isolation, a lower level of play activity (especially when alone with the stranger) and a high amount of passive behaviour. A less anxious reaction to separation was observed in both custody and apprentice dogs which were more playful and engaged less in proximity seeking behaviours; in particular custody dogs were extremely friendly towards the stranger. This could be the result of a number of different factors, such as the success of the puppy walking program aimed at socializing puppies with humans and/or the effect of age. Young dogs are in general more prone to play and in the case of apprentice dogs the less consolidated relationship with the trainer might also have played a role. Nevertheless, it is worth noting that those apprentice dogs which engaged significantly less in play activities failed to become guide dogs, confirming a negative relationship between playfulness and anxiety. Interestingly guide dogs’ behaviour was in a number of aspects in-between that exhibited by pets and that shown by custody and apprentice dogs, suggesting that they can be viewed as ‘‘working pets’’. In fact, in spite of separation from previous attachment figures guide dogs expressed their attachment to the owner showing the same whole range of proximity seeking behaviours observed in pet dogs. Guide dogs showed a clear preference for their owner and during separation episodes stood at the door as all the other dogs did. However, in guide dogs all these behaviours were expressed at a lower level than those observed in pets and comparable to those observed in younger dogs (custody and apprentice). This more controlled reaction could be a result of the training the aim of which is to reduce unnecessary excitability. In fact, only 12% of guide and 19% of apprentice dogs scratched the door during separation, compared to 44% of custody and 41% of pet dogs. The more controlled response to the SST observed in guide dogs could also depend on some active selection for emotional stability carried out on the bitches belonging to the school breeding program. Nevertheless, as previously pointed out, our sample of guide dogs included also subjects obtained from various commercial breeders, therefore guide and pet dogs should have been comparably heterogeneous. However, in guide dogs, a certain unavoidable level of distress was detectable in the polydipsia (Askew, 1996) and in the marked passivity shown. The fact that guide dogs were more passive, besides being a sign of anxiety (Topa`l et al., 1998), could be the result of their habituation to restrained activity. There are several situations in which a guide dog is required to remain passive: when off duty it may have to lie quietly near the blind owner for long periods while the owner eats, works, attend a show, etc.
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Guide dogs showed other behaviours that seemed to be dependent on the specific training received. They kept physical contact with their owner significantly more than the other dogs. This behavioural pattern, which is considered a sign of attachment (Topa`l et al., 1998; Prato Previde et al., 2003) could have been enhanced by the training procedure during which dogs learn to communicate physically their presence to the owner. In fact the training requires the dogs to touch owner’s leg with their muzzle when called and to keep strict contact with the owner’s leg while walking on duty (unpublished guideline for internal use of the trainers). This finding is also supported by the evidence that along an obstacle course guide dogs maintain more physical contact in comparison with pet and police dogs (Naderi et al., 2002). Group differences were observed also in the reaction to the strange/bizarre stimulus. Not surprisingly guide and apprentice dogs were less fearful towards the puppet than custody and pet dogs. This difference in fearfulness is mainly due to the training that focalises dogs’ attention on specific stimuli which are relevant to the guide-work: this seems the best approach to reduce fearful reaction in guide dogs (Goddard and Beilharz, 1984). Our bizarre puppet mimicked a vertical strange still object that could be encountered along a city walk, and it elicited avoidance behaviours mainly in untrained dogs. In such a complex service, traditionally the German Shepherd has been the breed of choice (Willis, 1995) but in more recent years there has been an increase in the use of both Labrador and Golden retrievers which are considered more sociable, less aggressive and possessive and also more adaptable to restrained activity (Witchel, 1996; Svatberg and Forkman, 2002). In this study we found that Golden retrievers showed a shyer and more insecure temperament than Labrador retrievers who were more playful and explorative. The behavioural profile of Golden retrievers is in agreement with findings reported by Hart and Miller (1985). These authors interviewed many trainers and dog specialists: Golden retrievers were described as very trainable dogs with a high attitude to play, but also as very timid with high affectional demand. In our opinion, these temperament differences should not be considered as a ‘‘mistake’’ in selection program but rather an important source of variability: as people differ from each other in their temperament, variability in guide dogs is necessary to assure an optimal blind owner-dog matching. In summary, the results of the present study indicate that guide dogs are able to form an intense bond with their blind owners, and this attachment appears to be modulated by the experience of the training. Although the ability to form attachment is associated with an early sensitive period, Ga`csi et al. (2001), who studied the effect of brief interactions with an unfamiliar human on the development of attachment behaviour of sheltered adult dogs, demonstrated that these interactions may result in attachment behaviour. Nevertheless, adult dogs adopted from shelters and tested in the SST showed more anxious and insecure bond with new owners (Prato Previde et al., 2003). However, the breakdown of the two bonds formed by the guide dogs is not a traumatic event comparable to that experienced by dogs abandoned in rescue shelters (Mondelli et al., 2003). In fact, while living with the puppy walkers, dogs are accustomed to visit the school monthly for the sanitary check-up and vaccinations, and most of all, to stay overnight in the school kennel with other dogs. This protocol was introduced 5 years ago in the program of the National School for Guide Dogs to make less stressful the separation from the puppy-walker and to habituate dogs to unfamiliar people and to the kennel routine. Our study provides empirical support to the
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effectiveness of this protocol, since the breakdown of the bond with the puppy-walker does not negatively affect both the learning abilities and the capacity to re-establish an equilibrate bond with humans. 5. Conclusions Our data show that guide dogs form new affectional bonds whose quality and integrity is not compromised by the experience of separation per se and there is no evidence that, as suggested by Fox (1968), the loss of the first attachment figure causes behavioural problems in these dogs. A further step of this research on the characteristics of the attachment bond in guide dogs will be a longitudinal study carried out on a group of dogs and aimed at evaluating the development of the bond and the effect of age.
Acknowledgments We are especially indebted to the staff of the ‘‘Scuola Nazionale Cani Guida per Ciechi-Regione Toscana’’ for providing dogs and logistical support, and for time devoted to discussion and helpful comments. We also thank Jenny Bertozzi and Emmanuela Diana for their invaluable assistance in collecting data. Finally, a special warm thanks to the puppy walkers, the trainers, the owners and the dogs for participating in the project. We are very grateful to Marco Poli for his interest and support of the project and for allowing us to carry out the work on pet dogs at the Psychology Institute of Universita` di Milano. We thank Orazio Rossi and Lamberto Soliani (Universita` di Parma) for statistical advice. This research was funded by Universita` di Milano (FIRT 2003) and MIUR (Ministero dell’Istruzione, dell’Universita` e della Ricerca-PRIN 2004) grants to Emanuela Prato-Previde, by Universita` di Parma (FIL 2003) and MIUR (PRIN 2004) grants to Paola Valsecchi and by Unione Italiana dei Ciechi Postdoctoral Grant to Gaia Fallani.
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