dog–human attachment bond

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IS THE DOGHUMAN RELATIONSHIP

AN ATTACHMENT BOND? AN OBSERVATIONAL STUDYUSING AINSWORTHS STRANGE SITUATION

by

EMANUELA PRATO-PREVIDE 1,3) , DEBORAH MARY CUSTANCE 2) ,CATERINA SPIEZIO 1) and FRANCESCA SABATINI 1,4)

(1 Istituto di Psicologia, Universit di Milano, Italy; 2 Goldsmith College, Department of Psychology, University of London)

(Acc. 24-I-2003)

Summary

Ainsworths strange situation procedure was used to investigate the dog ( Canis familiaris )

human relationship. 38 adult dog-owner pairs were observed in an unfamiliar room, intro-duced to a human stranger and subjected to four short episodes of separation. The procedureand behaviouralanalyses were as similar as possible to those used in studying human infants,except for the inclusion of an extra separation period in which the dogs were left alone inthe room with articles of clothing belonging to the owner and stranger. A secure base effectwas suggested by the fact that the dogs accepted to play with the stranger more in the pres-ence of their owner than during his or her absence. They also explored more in the presenceof their owner, but this appeared to be due to diminishing curiosity over time rather than asecure base effect. The dogs also exhibited a range of attachment behaviours, i.e. search andproximityseeking behaviourswhen separated from their owner, includingfollowing, scratch-ing and jumping up on the door, remaining oriented to the door or the owners empty chairand vocalising. They also greeted their owner more enthusiasticallyand for longer durationscompared to the stranger. Finally, they contacted the owners clothing more often and for

3) Corresponding authors address: Prof. E. Prato-Previde, Istituto di Psicologia, Universit diMilano, Via T. Pini 1, 20134 Milano, Italy, e-mail: [email protected]) This research was supported by funds from Universit di Milano to Emanuela Prato-Previde. We are grateful to Marcello Cesa-Bianchi and Marco Poli for allowing us to carryout the work in the Psychology Institute of Universit di Milano We thank Barbara Rotta for


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226 PRATO-PREVIDE, CUSTANCE, SPIEZIO & SABATINI

longer durations compared to the strangers clothing and spent more time next to the ownerschair when the owners objects were present. Hence, the dogs behaviour in the strange situ-ation was very similar to that reported in human infants and chimpanzees. However, despiteconductingdetailed behaviouralanalyses, the order effects inherent in Ainsworths procedureprevented the study from providingconclusiveevidence that the doghuman bond constitutes

an attachment.

Keywords : dog, attachment, affectional bonds, Ainsworth, Strange Situation.

In recent years, there has been increasing interest in human-dog rela-tionships and literature on this topic has ourished ( e.g. Serpell, 1995;Menanche, 1998). Most studies have either explored the issues concerning

attachment of humans to their pet dogs (Voith, 1985; Scott, 1992; Enden-burg, 1995; Collis & McNicholas, 1998), the effect of dogs on their ownerswell-being and health (Rowan & Beck, 1994; Hart, 1995; Wilson & Turner,1998), or the relationship between the owners behaviour and their dogsbehavioural problems (Voith et al ., 1992; OFarrell, 1995; Jagoe & Serpell,1996). Only a few studies have investigated the nature of the dogs affec-tional tie with its owner, and to our knowledge, the literature contains onlyone empirical study on this topic (Topal et al. , 1998).

The sparcity of empirical studies on the doghuman bond is surprisinggiven that dogs have been part of human society for longer than any otherdomestic species (Clutton-Brock, 1999) and they are by far the most popularspecies of companion animal (Hart, 1995). All modern dog breeds were do-mesticated as wolves over 10,000 years ago (Serpell, 1995; Clutton-Brock,1999) and subsequently subjected to an intense process of arti cial selection.It has been suggested that arti cial selection in dogs has not only favouredspeci c anatomical and behavioural traits, but also promoted general social-isation (Kretchmer & Fox, 1975) and the predisposition to form attachmentswith humans (Millott, 1994).

The owner-dog relationship resembles the parent-child bond in manyways. People tend to view and treat their dogs as child-like and many be-haviour patterns in dogs, like those of children, seem especially designed toelicit care (Voith, 1985; Askew, 1996). Askew (1996) argued that our petsdisplay evolutionary modi cations of ancestral behaviours that function toelicit human parental care In his opinion the behaviour of modern pet own


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DOG HUMAN ATTACHMENT 227

Among the various theories aimed to explain mother-infant attachment inhumans, the ethological-evolutionary perspective (Bowlby, 1958, 1969/1982;Ainsworth, 1964, 1967, 1969) is probably most compatible with a compara-tive approach. Bowlbys original theory was inspired by work on non-human

animals and hence it was rooted in biology with a concern for the adap-tive value of attachment and other related behavioural systems (Bretherton,1992). According to this view, social animals have evolved a predispositionto form attachment bonds, especially infants with their mothers.

Attachment can be considered as a particular kind of affectional bond.Throughout the lifespan, individuals can form a variety of different affec-tional bonds that are not attachments. Thus, in establishing whether a rela-

tionship constitutes an attachment, it is important to distinguish it from othertypes of affectional bonds. All affectional bonds (including attachments) en-dure over time, involve a speci c individual and are emotionally signi cant;furthermore, affectionally bonded individuals tend to maintain proximity andcontact and become distressed when involuntary separation occurs (Cassidy,1999). There is, however, one criterion of attachment that is not necessarilypresent in other affectional bonds: the experience of security and comfortobtained from the relationship with the partner, and yet the ability to moveoff from the secure base provided by the partner, with con dence to engagein other activities (Ainsworth, 1989, p. 711). Hence, in establishing whetherthe doghuman relationship constitutes an attachment, one must demonstratethe major elements common to all affectional bonds and in addition provideunambiguous evidence of a secure base effect.

We used Ainsworths Strange Situation procedure to test the hypothesisthat the doghuman relationship constitutes an affectional bond that can becharacterised as an infantile-like attachment. The Strange Situation proce-dure involves conducting controlled observations of a subjects response tobeing placed in an unfamiliar room, introduced to an unfamiliar adult (thestranger) and subjected to three short episodes of separation from the attach-ment gure. Although devised to test human infants, the Strange Situationprocedure has also proved an effective tool for studying affectional bondsand attachment in other species (Bard, 1991; Topal et al. , 1998; M.A. Shu-nik pers comm )


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system of secure attachment, all incidences of separation from the attach-ment gure (particularly in unfamiliar circumstances) would be expected tocause distress in the infant and attempts to re-establish proximity. Indeed,Ainsworth & Bell (1970) de ned attachment behaviour as those behaviours

aimed at promoting and restoring proximity and contact such as following,approaching, vocalising, clinging and crying. Although the presence of an-other individual with whom the infant has an affectional bond ( i.e. a sameage play mate) may provide some comfort, the child will not usually be fullycomforted or secure until she or he is reunited with the attachment gure.It is only after reunion with the attachment gure that one would expect theinfant to feel suf ciently secure to engage in non-attachment related behav-

iours such as exploration or play.Recently, Topal et al . (1998) used the Strange Situation procedure to ex-

plore the relationship between adult dogs and humans. They used a shortenedversion of the test in which each episode lasted two minutes and collecteda relatively small number of behavioural variables to compare the dogs re-sponses to their owner versus a stranger. They found that the dogs exploredand played more in the presence of the owner compared to the stranger.Furthermore, the dogs greeted their owners more enthusiastically than thestranger upon reunion episodes and stood by the door more when separatedfrom their owner versus the stranger. On the basis of these ndings, Topal et al . concluded that the dog-owner relationship conforms to an attachment.

Although Topal et al .s study constitutes a valuable contribution to theeld, in our opinion their conclusions about the nature of the doghuman

bond are somewhat premature. We believe that Topal et al .s basic behav-ioural analyses were not suf ciently detailed to be able to distinguish attach-ment from a general affectional bond. Topal et al .s ndings clearly showedthat dogs exhibit a strong preference for their owner over a stranger. How-ever, all affectional bonds involve exhibiting a preference for a speci c in-dividual, a gure who is not interchangeable with anyone else (Ainsworth,1989). To establish the presence of an attachment, one must focus much moreon the behavioural categories that indicate security-, proximity- and comfort-seeking. Topal et al . collected almost no data that would indicate distressor protest during separation such as vocalising or searching They reported


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mother to the door, standing by the door, orientation to the door from a dis-tance, pounding upon the door, trying to open the door, going to the mothersempty chair or simply looking at it (Ainsworth & Bell, 1970; Ainsworth et al ., 1978). These behaviours convey information on the level of activation

of the attachment behavioural system and on the degree to which separationcauses the infants distress and activates a proximity seeking response.

According to Ainsworth (1989), the secure base effect is the primaryfactor that distinguishes an attachment from other types of affectional bonds.Thus, the most serious omission in Topal et al .s analysis is the lack of evidence relating to the secure base effect. The fact that the dogs playedmore with their owner rather than the stranger does not necessarily indicate

a secure base effect. It could simply indicate a preference for the owner overthe stranger. Similarly, the fact that the dogs explored more in the presenceof the owner than the stranger could be due to an order effect in Ainsworthsprocedure rather than a secure base effect. The dogs were left alone with theowner for the rst two minutes of the procedure. By the time the strangerentered the room and particularly by the time the dogs were left alone withthe stranger, they had already been given plenty of opportunity to explore theroom and satisfy their curiosity. In their study, Topal et al . lumped togetherall the data on the dogs behaviour in the presence of the owner versusthe stranger providing little information on how a given behaviour changedfrom one episode to another. Such comparisons are extremely important fordiscerning possible order effects.

The Strange Situation procedure provides three different means by whichone can identify a secure base effect. First, play and exploration in humaninfants has been found to become depressed when they are in the presenceof just the stranger and when alone, but recovers after reunion with themother. Second, although human infants tend to explore the room and toysto a consistently high degree across the rst episode of the procedure, theyoften cease and return immediately to their mothers side upon the entranceof the stranger. The presence of strangers is a source of some anxiety toyoung infants and thus the mother provide a secure base from which toview this potentially fear inducing stimulus. Third, some human infants aresuf ciently con dent when in the presence of their mother to engage in play


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The present study differed from Topal et al .s work in a number of impor-tant respects. First, we conducted much more detailed behavioural analysesthat concentrated on many of the key behavioural measures for attachmentas used by Ainsworth & Bell (1970) and Ainsworth et al . (1978). Second,

the behaviour of the dogs in the presence of the stranger and when alonewas analysed separately and, as in studies on human infants, these quali-tatively different conditions were compared. Third, the dogs behaviouralchanges across episodes were evaluated. Fourth, we followed the traditionalprocedure used in studies on human infants, which incorporate episodes of 3-minutes duration. Finally, we included an extra phase at the end of the stan-dard Ainsworth procedure in which the owner and stranger left an article of

clothing and their shoes in the room while the dog was left alone for a furtherthree minutes. This extra episode aimed to test the degree to which the dogswould orient to their owners objects and the degree to which they seemedto use these objects as a source of comfort. We hypothesised that if the dogswere attached to their owners, we would nd evidence of secure base effects,proximity seeking and maintenance, search behaviours and comfort seekingthat are functionally similar to those observed in human infants.

Method

Subjects

Thirty-eight volunteer owner-dog pairs formed a convenience sample, recruited both by per-sonal contact and from advertisements distributed within the University of Milan. The dogowners comprised 10 men and 28 women whose ages ranged from 18 to 74 years (mean D38.8 years, 13.5 SD). 30 owners (78.95%) had previous experience of dog ownership and 25(65.79%) owned only one dog at the time the study took place.

The sample of dogs consisted of 19 males and 19 females whose ages ranged from 1 to 10years (mean D 4.51 years, 2.46 SD). Twenty dogs were pedigrees and 18 were mixed-breedsor mongrels. Thirteen dogs (11 mongrels an 2 pure breed) had been adopted from rescuecentres and their age of adoption varied from less than 3 months (3 subjects) to 3-6 months(3 subjects), 6-12 months (2 subjects), 1-4 years (5 subjects). The remaining 25 dogs hadbeen reared in the same family home from puppy-hood and their age at acquisition rangedbetween 50 days and 3 months. The pedigree dogs included 2 German Shepherd Dogs, 3Labrador Retrievers, 2 Siberian Huskies, 1 Fox Terrier, 1 Dachshund, 2 Boxers, 2 Shih Tzus,3 Bernese Mountain Dogs, 1 Yorkshire Terrier, 1 Beagle, 1 German Wirehaired Pointer, and1 Italian Hunting Hound


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aggression towards a human. All the owners reported that their dogs were used to stayingalone at home and could remain alone without problems.

Experimental setting and materials

The dogs were tested in a standardised and controlled strange environment, as similar aspossible to that described by Ainsworth & Bell (1970). Figure 1 is an aerial plan of theunfamiliar environment.It comprised a relatively bare room (3 :00 5:30 m) at the Instituteof Psychology of the University of Milan. The room was equipped with two chairs (one labelledas stranger and the other as owner), a selection of dog toys (one large and one small ball,a plastic bottle, a rope pull-toy, and a squeaky toy), a water bowl and two videocameras(Sony Handycam Video HI 8). One of the two videocameras was connected with a monitorpositioned in an adjacent room, so that each session could be independently observed. Tominimise extraneous noise, testing was conducted each weekend between 1430 and 1830

hours, over a period of three months.

Procedure

Pre-experimental phase (approximately 10 minutes in duration): The owner and dog weremet and escorted to a waiting room. The procedure was brie y described to the owner andthe owner was asked to ll in a questionnaire providing background information on his orher dog. The speci c goal of the study was not disclosed at this stage. Instead, the ownerwas told that the aim of the study was to investigate the exploratory behaviour of dogs in

an unfamiliar environment. After gaining the owners permission to videorecord behaviourduring the experimental phase, the two video cameras were activated and both the dog andowner were led to the experimental room.


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Experimental phase: The experimental protocol was adapted from Ainsworth & Bell(1970). The procedure lasted approximately 27 minutes and consisted of an introductoryepisode followed by 8 three-minute experimental episodes (Fig. 2, episodes 1-8). The intro-ductory episode and the rst seven experimental episodes were those typical of the StrangeSituation. An additional eighth episode was included to study the dogs response to the pres-ence of objects or articles of clothing left behind by the stranger or owner. The episodes wereas follows:

Introductoryepisode: Owner, Dog and Experimenter(approximately30 s). The owner wasguided to his or her chair, and asked to sit and complete the questionnaire. The experimentertook the dogs lead and left the room.

Episode 1: Owner and Dog (3 min). The owner sat quietly lling in the questionnaireand,as instructed, only interacted with the dog ( i.e. by petting or talking to it) if it speci callysought attention. The dog was free to explore the room.

Episode 2: Owner, Dog and Stranger (3 min). The stranger, who was always played bythe same woman and who had never met the dog before, entered the room and sat quietlyfor 1 minute. She conversed with the owner for the second minute, and then during the thirdminute she approached the dog and attempted to stimulate play by throwing a ball or offeringa pull-toy. At the end of this episode the owner left the room unobtrusively.

Episode 3: Stranger and Dog (3 min, 1st separation episode). The stranger continued toplay with the dog if it was willing; if it was inactive or distressed, the stranger attempted todistract it with play or by providing verbal and tactile comfort.

Episode 4: Owner and Dog (3 min, 1st reunion episode). The owner entered the room,

paused momentarily after opening the door to allow the dog to initiate interaction and then,as instructed, greeted and/or comforted the dog in the same manner as after returning fromwork or shopping. The stranger quietly exited the room as soon as she was con dent thatshe would cause the least possible disruption to the dog and owners reunion. The owner hadbeen told that she or he was free to play with the dog throughout the episode. At the end of the 3 minutes, a telephone in the room rang on a low volume alerting the owner to leave theroom with a verbal farewell.

Episode 5: Dog alone (3 min, 2nd separation episode). The dog was left alone for threeminutes, but was constantly observed by the owner and researchers on the monitor in the

adjacent room. The owner was instructed to remain silent throughout this period, but retainedthe right to terminate the episode if she or he believed the dog was becoming too distressed(none of the owners felt the need to execute this right).

Episode 6: Stranger and Dog (3 min, 3rd separation episode). The stranger entered theroom paused momentarily after opening the door to allow the dog to initiate interaction andgreeted the dog if it was willing by petting its head and back. She then followed the sameprotocol as in episode 3. Toward the end of the episode, the stranger removed her shoesand placed them near her chair, and also left an article of clothing (equivalent to the articleselected by the owner) on the chair before leaving.

Episode 7: Owner and Dog (3 min, 2nd reunion). The owner entered the room, pausedmomentarily after opening the door, then greeted the dog as though he or she had just returned


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TABLE 1. (Continued)

Behaviouralcategory

De nition Samplingmethod

Physicalcontact withchair

Being in physical contact with owners or strangers chair Point sampling& frequency

Contactwith objects

Being in physical contact with the owners or strangersshoes or clothing

Point sampling& frequency

Vocalising Any kind of vocalisation, i.e. barking, growling, howling,whining: vocalisations were recorded as bouts

Point sampling& frequency

Greetingbehaviour

All greeting behaviours toward the entering owner orstranger, such as approaching, tail-wagging, jumping,physical contact

Duration & in-tensity

Episode 8: Dog and Objects (3 min, 4th separation and 3rd reunion). The dog was leftalone and monitored as in episode 5. At the end of the third minute, the owner returned andgreeted and/or comforted the dog until the experimenterarrived and of cially terminated theprocedure.

Immediately after each session, the experimental room, water bowl and toys were washedusing a non-toxic, weakly scented disinfectant.

Data collection and analysis

The behaviour of each dog during the experimental episodes (ep. 1-8) was recorded onvideotapes and each session was analysed by two trained observers recording a total of 17behavioural categories. These categories were selected after a preliminary analysis of thevideotapes and on the basis of previous work based on the strange situation procedure ( i.e .Ainsworth & Bell, 1970; Ainsworth et al ., 1978; Topal et al ., 1998).

The dogs behaviour during each episode was rst scored using 5-second point sampling(instantaneous sampling). This method of time sampling was chosen because it is a way of condensing information, thereby making it possible to record several different categories of behaviour simultaneously and with accuracy when the exact duration of a given behaviouris not strictly necessary. If the sample interval is short enough, point sampling is accurate inestimating duration of behavioural states and gives a good approximation of the proportionof time spent performing a behaviour pattern. However, instantaneous point sampling is notsuitable for recording discrete events of short duration and rare behaviour patterns. There-fore, in a second round of coding we used continuous recording to collect frequencies for anumber of discrete events. Table 1 contains a list of the different behavioural categories, theirde nitions and the type of sampling method employed for data collection.

The greeting behaviour of the dogs towards the owner (ep 4 and 7) and the stranger


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then showed a mild greeting with limited physical contact and tail wagging, the score was1 (mild greeting); if physical contact was full and the greeting behaviour was intense ( i.e . jumping up on the owner, vocalising and strongly wagging the tail) the score was 2 (intensegreeting).

Interobserver reliability was assessed by means of independent parallel coding of a ran-dom sample of 4 videotaped sessions ( i.e. 10% of the total number of dogs) using percentageagreement: agreement on frequencies and greeting behaviour was evaluated separately. Per-centage agreement was always more than 96%. Since, histograms revealed that the majorityof the data were not normally distributed, all statistical tests were non-parametric and two-tailed.

Results

The results presented re ect average tendencies rather than individual differ-ences. There were clear individual differences among the dogs, but a detailedexposition of these is not within the scope of the present paper. Since, therewas a relatively small sample of dogs, subjects with extreme experiences hadthe potential to skew the overall results. Hence, the analyses were carried outusing non-parametric tests based on the median rather than the mean, which

tends to minimise this kind of distortion. The results have been arranged intofour categories: secure base effects, proximity seeking, search behavioursand comfort seeking. D refers to dog, S to stranger and O to owner.

Secure base effects

Exploration

According to the ethological approach, an attachment gure functions as asecure base and thereby allows the child to move off and engage in otherbehaviour, especially exploration. Figure 3 shows how exploratory behaviourvaried in successive episodes. Exploration declined sharply from episode 1when the dog was alone with the owner to episode 2 when also the strangerwas present (Wilcoxon test: z D 4:28, p < 0:0001 / remaining low inepisode 3, when the dog was alone with the stranger, and in the followingepisodes. A comparison between the overall proportion of sample pointsspent exploring in episodes characterised by owner (O) presence (1 4 7)


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Fig. 3. Proportion of time spent by the dogs exploring and passive across the 8 episodes.O = owner; D = dog; S = stranger.

owner than with the stranger or alone (SNK test for multiple comparisons(Glantz, 1997): O+D vs S+D, p < 0:05 I O+D vs D, p < 0:05 I S+D vs D,p D NS).

However, it is possible that these differences in exploration were due toan order effect of diminishing curiosity over time rather than to a securebase effect. When the dogs were rst introduced to the room, they were inthe presence of their owner and the most intense exploration occurred in the

rst minute. Although there was a signi cant difference in the amount of

exploration between the third minute of episode 1 and the rst minute of episode 2 (Wilcoxon test: z D 2:25, p D 0:025 / , there was also a signi cantdifference between the rst and second minute (Wilcoxon test: z D 2:49,p D 0:012 / and a decrease between the second and third minute (Wilcoxontest: z D 1:919, p D 0:055 / of episode one. Figure 4 clearly indicates thatexploration rapidly and steadily declined across the rst four minutes of theprocedure.

Overall males ( N D 19) were slightly more explorative than females(N D 19) and in particular engaged in exploratory behaviour signi -


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Fig. 4. Proportion of sample points spent in exploration across the rst 5 minutes.

Response to strangers entrance

Only 7 out of 38 dogs (18,4%) remained close to their owner or returnedto their owners side on the entrance of the stranger, observing her from adistance. Most of the dogs (81,6%) did not seem at all wary of the stranger: a

number of them greeted her or approached her, others ignored her continuingthe activities they were engaged in.

Passive behaviour

If the owner operated as a secure base, this might have allowed the dogs tofeel suf ciently calm to engage in passive behaviour when in their ownerspresence. Passive behaviour ( i.e . sitting, standing or lying down without ob-viously focussing on some aspect of the environment) was higher in episode1 and 2 and when the dogs were alone (ep. 5, 8; Fig. 3). During episodes 1and 2 the subjects tended to stay close to the owner, whereas during episodes5 and 8 most passive behaviour occurred in the door area. Comparison be-tween the overall proportion of sample points spent passive in the episodescharacterised by owner presence (1, 4, 7), stranger presence (3, 6) or by iso-lation (5, 8) revealed signi cant differences (Friedman test: O+D vs S+D vsD, 2 D 6:77, p D 0:034 / . Dogs were more passive with their owner andwhen alone than with the stranger (SNK test for multiple comparisons: O+D


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z D 2.213, p D 0:026). No differences in passive behaviour were foundcomparing abandoned ( N D 13) and non-abandoned ( N D 25) dogs. Dur-ing isolation episodes non-abandoned dogs tended to stay more passive thanabandoned ones (Mann-Whitney test: ep. 5-8, z D 1.879, p D 0:06 / .

Play

Individual play occurred rarely: only 4 out of 38 subjects (10.5%) playedwith toys in episodes 1 and 2, and 1 subject did so when left alone in episode5. In episode 2.66% of the subject accepted to play with the stranger, whereasonly 55.3% played, at least to some extent, in episode 3, and 39.5% did

so in episode 6. A comparison between the proportion of sample pointsspent playing with the stranger in episodes 2 (last minute) and 3 showedthat play decreased after the owner left the room (Wilcoxon test: ep. 2 vsep. 3, z D 2:072, p D 0:038 / . Figure 5 shows the proportion of samplepoints spent by the dogs playing with the owner (ep. 4 and 7) and withthe stranger (ep. 3 and 6): a comparison between the overall proportion of sample points spent playing with the owner and the stranger in these episodes

showed that dogs played signi cantly more with their owner (Wilcoxon test:O+D vs S+D, z D 2:08, p D 0:037 / . Social play with the owner clearlydecreased on the second reunion episode (Wilcoxon test: ep. 4 vs ep. 7,


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z D 3:468, p D 0:0005 / and declined signi cantly on the second encounterwith the stranger (Wilcoxon test: ep. 3 vs ep. 6, z D 3:563, p D 0:0004 / . Wefound no sex differences in play behaviour with the owner (ep. 4 and 7) andthe stranger (ep. 3 and 6), whereas abandoned dogs played less than non-

abandoned ones with the stranger (Mann-Whitney test: ep. 3-6, z D 1. 967,p D 0:049 / .

Proximity seeking

Approach

The dogs approached both the owner and the stranger in the different

episodes both spontaneously and when called. In episode 2 the stranger wasapproached more than the owner (Wilcoxon test: z D 2:44, p D 0:014 / Ihowever, a comparison between episodes 4 and 7 (presence of the owner)and 3 and 6 (presence of the stranger) showed that the dogs approachedtheir owner signi cantly more than the stranger (Wilcoxon test: z D 2:341,p D 0:02 / . While approach behaviour toward the owner was comparable onepisodes 4 and 7, approach behaviour toward the stranger increased remark-

ably in episode 6 (Wilcoxon test: ep. 3 vs ep. 6, z D 3:071, p D 0:002 / .

Withdraw

Of course, withdraw or avoidance is the antithesis of proximity seeking. It isincluded here to offer a direct contrast to approach. None of the dogs clearlyavoided interaction with its owner whereas 3 subjects (2 of them abandoned)showed strong avoidance of the stranger especially during episodes 3 and 6.

Avoidance responses occurred when the stranger tried to interact with thedog or to comfort him/her and varied in intensity from looking away toturning away to moving away while staring at the stranger.

Oriented to person

Orientation to a person may have different functions, one of which couldbe monitoring proximity. The dogs paid attention to both the owner andstranger. In episode 2, their attention was focused signi cantly more onthe stranger (Wilcoxon test: z D 4:285 p < 0:0001 / A comparison be


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Following

Following the owner to the door was scored for episodes 2, 4 and 7 whenthe owner left the room. Most of the dogs (86.8%) followed their owner tothe door at some point during the procedure, and only 5 subjects (13.2%)never showed following behaviour. In particular, 36.8% of the dogs followedtheir owner to the door all three times that she or he exited the room, 28.9 %followed on two occasions and 21.1% only one time. On the contrary only 4dogs (10.5%) followed the stranger to the door when she left and did it onlyone time.

VocalisingIt has been suggested that vocalising might function to promote proximitymaintenance or resumption, in addtion to indicating distress. The majorityof the dogs (86.8%) vocalised during the strange situation although to adifferent extent. Figure 6 reports the mean number of vocalisation bouts(barking, howling and whining) in successive episodes; vocal behaviour waslow in the episodes characterised by the presence of the owner (1, 4, 7)

increasing during separation episodes (3, 6 and 5, 8). Vocalisations increasedwhen the owner left the room and the dogs remained alone with the stranger(Wilcoxon test: ep. 2 vs ep. 3: z D 2:046, p D 0:04 / . A comparison of vocalbehaviour across conditions showed that the mean number of vocalization


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Fig. 7. Proportion of time spent by the dogs oriented to the door across the 8 episodes. O =owner; D = dog; S = stranger.

Male dogs ( N D 19) tended to stay more oriented towards the door thanfemales ( N D 19) during separation episodes (ep. 3, 6 and 5, 8) and staredat the door more when in the presence of the stranger (Mann-Whitney test:ep. 3-6, z D 2:016, p D 0:044). Abandoned dogs were not more oriented tothe door than non-abandoned during isolation (ep. 5, 8) but tended to stare atthe door more in the presence of the stranger and in particular in episode 3when their owner left the room for the rst time (Mann-Whitney test: ep. 3,z D 1:917, p D 0:055).

Oriented to chairAs Fig. 8 shows the dogs glanced at both the owners and strangers emptychairs during the different separation episodes; however, they were signi -cantly more oriented to their owners chair (Wilcoxon test: ep. 3, 6, Ownervs Stranger, z D 2:084, p D 0:037 I ep. 5, 8, Owner vs Stranger, z D 2:926,p D 0:003 / . Glancing at the owners chair occurred almost exclusively whenthe owner was absent (95.5% of all occurrences) and was signi cantly higherwhen the dogs were alone in the room (Wilcoxon test: S+D vs D, z D 3:60,p D 0:0003 / I this behaviour decreased the second time they remained with


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Fig. 8. Percentage of events in which the dogs were oriented or in contact with the ownersversus the strangers chair during separation episodes. O C O = oriented to owners chair;O C S = oriented to strangers chair; C C O = physical contact with owners chair; C C S =

physical contact with strangers chair.

Comfort seeking

Physical contact with chair

The dogs made contact with both the owners and strangers empty chairsduring the different episodes; however, when in the presence of the stranger(ep. 3, 6) and when alone (ep. 5, 8) they were signi cantly more in contactwith their owners chair (Wilcoxon test: ep. 3, 6, Owner vs Stranger, z D3:354, p D 0:0008 I ep. 5, 8, Owner vs Stranger, z D 2:481, p D 0:013 I

Fig. 8). Three different types of contact with the chair were observed: puttingthe head on the chair and snif ng it for a while, sitting or lying down withthe body in contact with the chair legs, and climbing on the chair remainingseated on it: these last two type of contact were almost exclusively with theowners chair.

Contact with objects

71% of the dogs made contact with the objects (shoes and piece of clothing)during episode 8 and mainly with those of the owner (65 2% of all contacts)


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with objects ranged from snif ng them to maintaining physical contact withthem ( i.e. sitting on the clothes on the owners chair): physical contact wasdirected to only the owners objects. Furthermore, a comparison between theproportion of sample points spent by the dogs in the owners area (Area 3,

see Fig. 1) during social isolation (ep. 5 and 8) showed that the amount of time spent next to the owners chair increased signi cantly when the ownersobject were present (Wilcoxon test: ep. 5 vs ep. 8, z D 3:026, p D 0:002 / .

Physical contact with person

The dogs sought and maintained physical contact with both the owner and

the stranger during the different episodes. However, a comparison betweenthe proportion of sample points spent in physical contact with the owner (ep.1, 4, 7) and with the stranger (ep. 3, 6) showed that the dogs spent more timein contact with their owner (Wilcoxon test: z D 2:31, p D 0:021 / . Duringseparation episodes the dogs, although to a different extent, accepted to stayin physical contact with the stranger and to be petted: physical contact wassigni cantly higher in episode 6 (Wilcoxon test: ep. 3 vs ep. 6, z D 4:424,

p < 0:0001 / . However, when in contact with the stranger they were muchmore oriented to the door than when in contact with their owner (Wilcoxontest: ep. 3, 6 vs ep. 4, 7, z D 4:259, p < 0:0001 / .

Greeting

Greeting behaviour was scored during the rst minute of episodes 2 and 6(entrance of the stranger) and 4 and 7 (reunion with the owner). Only 2 outof 38 subjects showed no greeting towards both the owner and the stranger,7 subjects (18.4%) never greeted the stranger and 29 (76.3%) greeted, atleast to some extent, both the owner and the stranger. Dogs showed consid-erably more intense levels of greeting towards the entering owner comparedwith the stranger. As Fig. 9 shows, differences in overall greeting durationtowards the owner (ep. 4, 7) and the stranger (ep. 2, 6) were highly signif-icant (Wilcoxon test: z D 2:99, p D 0:002 / and the duration of greetingbehaviour did not decrease on the second reunion with the owner (Wilcoxontest: ep 4 vs ep 7 p D NS) and on the second encounter with the stranger


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Fig. 9. Duration of greetings directed toward the entering owner (ep. 4, 7) versus thestranger (ep. 2, 6). O = owner; D = dog; S = stranger.

(60.5%) showed intense greeting on the rst reunion with the owner. Sim-ilarly, after being left completely alone in episode 5, and even though the

stranger entered rst (ep. 6), the dogs still showed more intense greetingstowards their owner when she or he returned three minutes later at the startof episode 7 (Sign test: p < 0:05 / . Differences in greeting intensity wereassessed comparing the scores of each dog during episodes 2 and 4 ( rst en-counter) and episodes 6 and 7 (second encounter). In both cases, greetingstowards the owner were signi cantly more intense (Sign test: p < 0:05 / .

Discussion

The aim of this study was to investigate in some detail the nature of the doghuman social relationship by observing owner-dog pairs under controlledconditions using a modi ed version of the strange situation procedure devel-oped by Mary Ainsworth. This procedure seemed particularly suitable fortesting dogs as it reproduces situations that dogs are likely to encounter intheir everyday life, such as being in a new environment, meeting a stranger,and being separated from their owner for short periods Overall our ndings


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Ainsworth (1989) stated that the secure base effect was a primary factorin identifying an attachment bond. Three measures of the secure base effecthave been identi ed: (1) play and exploration become depressed when inthe presence of just the stranger and when alone, but recover after reunion

with the mother; (2) infant cease playing or exploring on the entrance of the stranger and return to their mothers side; and (3) infants will sometimesplay with the stranger in their mothers presence, but not her absence. In ourstudy there was an insuf cient amount of individual play in the dogs to usethis as a measure of the secure base effect. In addition, only 18.4% of thedogs remained close to their owner or returned to their owners side on theentrance of the stranger. Most of the dogs did not seem at all wary of the

stranger and hence her presence did not appear to activate the attachmentsystem.

The dogs exploratory behaviours consisted mainly of locomotory ex-ploration. Other forms of exploration reported in human infants and chim-panzees were either rare ( i.e. visual) or physically dif cult for dogs to per-form ( i.e. manipulatory). Exploration was higher in the presence of the owner(see also Topal et al ., 1998). Moreover, similar to what is reported for humaninfants and hand-reared chimpanzees (Ainsworth & Bell, 1970; Ainsworthet al ., 1978; Bard, 1991), exploration occurred mainly in episode 1, whenthe dogs were with their owner, and a signi cant decline was observed fromepisode 1 to episode 2 with the entrance of the stranger.

At rst glance, the above pattern of results suggests that the owner pro-vided a secure base for exploration and that the entrance of the stranger neg-atively affected exploratory behaviour, indicating strangers wariness or fear.However, by the end of the third minute of episode 1 most of the dogs hadeither nished exploring the room or were doing so to a much lesser extentthan before. In addition to there being a signi cant difference between thelast minute of episode 1 and the rst minute of episode 2, there was also asigni cant decline in exploration across the whole of the rst episode. Thusthe overall pro le of exploration during the rst ve minutes of the proceduresuggests that these differences could be due to an order effect of reduced cu-riosity over time. Therefore, the dogs exploratory behaviour did not supplyconvincing evidence of a secure base effect


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Instead, it might suggest that the owner was a preferred playmate. If the dogshad engaged in individual play more in the presence of the owner rather thanthe stranger, there would have been better evidence of a secure base effect.However, very few dogs engaged in individual play of any kind, whether

with or without their owner.Rather more indicative of a secure base effect was the nding that the

proportion of social play with the stranger was higher in the presence of the owner ( i.e. during the last minute of episode 2) than when the dogswere left alone with the stranger in episode 3. This nding suggests that inepisode 2 the presence of the owner provided a suf cient sense of security topromote play with the stranger. Although this decrease of play in the absence

of the owner might be partly due to fatigue or reduced interest, the overallbehaviour of the dogs during episode 2 and 3 suggests that in episode 3 theattachment behavioural system was activated and interfered with play: inparticular, play became discontinuous and a variety of behaviours indicatingdistress, protest and searching appeared ( i.e. vocalising, running to the dooror looking at it continuously). Play behaviour with the owner was intenseagain in episode 4, thus suggesting that the decrease in play in the absenceof the owner in episode 3 and the differences in the propensity to play withthe owner versus the stranger were unlikely to be due to fatigue or satiation.

In general the dogs showed little distress in the pre-separation episodes.In fact, some of them were so deeply engrossed in play with the stranger inthe last minute of episode 2 that they did not even notice their owner leavingthe room. However, once they did notice their owners absence, most dogsshowed distress and protest during separation and engaged in a variety of behaviours indicating that they were searching for the absent owner eitheractively or by orienting to the last place in which she or he was seen. Ourobservations during separation episodes (ep. 3, 6, 5 and 8) show that thedogs search behaviours closely resembled those described in human infantsand chimpanzees and included following the owner to the door, scratching atand jumping up on the door, pulling on the door handle with the forelegs ormouth, remaining oriented to the door, going to the owners empty chair orlooking at it from a distance.

Both human infants and chimpanzees have been reported to show alarm


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mainly of attention seeking, play soliciting and greeting vocalisations. Incontrast, during separation episodes whining and barking increased, reachingthe highest levels during social isolation (ep. 5 and 8). Vocal behaviour wasespecially activated by being left alone and was reduced by the presence of the stranger. This suggests that for dogs separation from the owner in anunfamiliar environment was distressing, but not as distressing as being leftcompletely alone. The decline of vocal behaviour in episode 6, together withthe increase of physical contact with the stranger suggests that, in general,the dogs did not nd the stranger frightening per se and she was able toprovide some comfort. Nevertheless, a number of dogs continued to whineeven when in physical contact with the stranger. Some accepted petting, butremained oriented to the door most of the time, others did not vocalise butshowed an increase in search behaviours such as going to the owners chairor looking at it. Therefore, the friendly stranger was not able to providesuf cient comfort to curtail search and protest behaviours during the ownersabsence. The continuation of distress and search behaviour by the dogs whenthey were left alone with the stranger, but not the owner, is consistent with

the pattern of attachment behaviours described by Ainsworth & Bell (1970)in human infants.Separation from the owner promoted proximity and contact seeking be-

haviour upon reunion (ep. 4 and 7). During reunion with the owner, prox-imity seeking behaviour included greeting responses, approaching, and fol-lowing the owner around the room. Greeting toward the entering owner wassigni cantly different from greeting toward the entering stranger in terms of

duration and quality and the stranger was approached signi cantly less incomparison to the owner.

Avoidance or withdrawal behaviour was seldomly exhibited by the dogs.In fact, it was recorded in only three dogs (all of whom had been abandonedat some time in their life) and only in response to the stranger. Human infantsexhibit resistant behaviours, in which they resist being picked up or held andstruggle to be put down again. None of the owners attempted to pick up their

dogs and nothing that could be characterised as resistance was observed.Although the dogs visually oriented to both the owner and the stranger


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in mutual eye contact with their owners and spend considerable time observ-ing their movements, an activity which according to Serpell (1986) plays acentral role in building and maintaining the relationship between people andtheir pets. Prior to separation (ep. 1 and 2), most dogs looked at their owneronly occasionally. In episode 2, their attention was clearly captured by thestranger: this appeared to be due to a variable combination of curiosity, ex-ploration, wariness and sociability. All dogs looked at the entering stranger,but not all approached, sniffed or greeted her. A number of subjects observedthe stranger from a distance remaining close to their owners chair withoutinteracting or playing with her. This nding is consistent with what reportedin both human infants and chimpanzees. Visual orientation toward the ownerincreased signi cantly during reunion episodes and occurred frequently dur-ing physical contact. In contrast, visual orientation toward the stranger (ep.3 and 6) occurred mainly during play or in response to the strangers at-tempts to interact. These differences in the use of visual orientation suggestthat looking at the stranger was related to socialisation toward humans ingeneral, whereas looking at the owner was related to affection and comfort

seeking.The behaviour of the dogs during the last episode, when they remainedalone in the presence of the owners and strangers objects, suggests that atleast a number of the dogs used the owners objects as a source of comfort.The dogs showed a clear preference for their owners objects: there weresigni cantly more contacts with the owners objects and prolonged physicalcontact was only ever directed to the owners objects. Behaviour in episode 8

differed from that of episode 5 in a number of ways. First, barking, whiningand scratching at the door decreased signi cantly. Second, the time spent ori-ented to the door decreased while the time spent oriented to the owners chairincreased signi cantly. Last but not least, the amount of time spent by thedogs in the owners chair area where the owners objects were increased sig-ni cantly. In fact, during episode 8 a number of dogs jumped on the ownerschair and sat on the clothes while others remained next to their owners chair

sitting or lying down. Although potentially confounding order effects can-not be excluded the signi cant increase in the amount of time spent close


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used the owners clothing as a source of comfort because it carried famil-iar odour s. It is also possible that previous experience during the procedurecould have decreased distress ( i.e. by promoting the expectation in the dogsof their owners return) and this could have lead to a decrease in searchingand proximity seeking behaviours and a corresponding increase in passivebehaviours.

In summary, we found that adult dogs behaviour in the Strange Situationtest resembled that of human and chimpanzee infants to a remarkable degree.Our results clearly indicate that the doghuman relationship is an affectionalbond, but our evidence that it conforms to an attachment is not entirelyconclusive. The order effects inherent in Ainsworths procedure meant thatwe could nd only one positive indicator of the secure base effect, namely,the fact that the dogs would play with the stranger in the presence of theowner, but not in his or her absence. This suggests that the conclusions drawnin the previous study by Topal et al . were premature and that further researchis needed to gain a better understanding of the nature of the doghumanbond and to test speci cally for secure base effects. Modi ed versions of

the procedure could be devised to test speci c hypotheses avoiding the ordereffects typical of Ainsworths original design.Nevertheless, the Strange Situation procedure and possible modi ed ver-

sions aimed at counteracting order effects would appear to be an appropriateand useful tool to test hypotheses about the bond between dogs and theirowners and to evaluate the quality of the relationship. In fact, in terms of the doghuman affectional bond and attachment, there are very many areas

of possible future research. With a larger sample size than that used here,one could compare different breeds of dogs and the effect of gender withrespect to the dogs and their owners. Even with our relatively small sample,our data show males dogs spent more time exploring the new environmentthan females during the rst episode, whereas female were signi cantly morepassive.

One could also investigate the effect of early socialisation with humans

and previous experiences on the doghuman bond. A rather dramatic experi-ence that can have a profound in uence on doghuman relationship is aban-


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found several trends (although most were statistically non-signi cant) sug-gesting that these dogs were more anxious and perhaps less securely bonded:they explored and played less in the presence of the owner, were less passivewhen left alone and withdrew from the stranger more than those dogs thathad lived in the same household since puppyhood. A particularly interesting

nding, that deserves further attention, is the signi cant difference in socialplay with the stranger between abandoned and non-abandoned dogs.

Physiological measures could be used to support the behavioural data withrespect to anxiety, distress and comfort seeking (Palestrini et al ., 2001). Noneof the owners in our study reported that their dogs suffered any serious be-havioural problems, and almost all reported that their dogs could stay alone athome without problems, however during the test a number of dogs showedbehaviours that could be related to separation anxiety (Voith & Borchelt,1985). The Strange Situation could be used to investigate the behaviour of dogs that exhibit separation anxiety and to make comparisons with dogsnot showing this behaviour problem.

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(1967). Infancy in Uganda: Infant care and the growth of attachment. Johns HopkinsUniversity Press, Baltimore.

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(1989). Attachments beyond infancy. Am. Psychol. 44, p. 709-716. & Bell, S.M. (1970). Attachment, exploration, and separation: illustrated by the behav-

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