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. 2021 Dec 22;16(12):e0261790. doi: 10.1371/journal.pone.0261790

Secure base effect in former shelter dogs and other family dogs: Strangers do not provide security in a problem-solving task

Giulia Cimarelli 1,2,*, Julia Schindlbauer 1, Teresa Pegger 1, Verena Wesian 1, Zsófia Virányi 1
Editor: I Anna S Olsson3
PMCID: PMC8694447  PMID: 34936692

Abstract

Domestic dogs display behavioural patterns towards their owners that fulfil the four criteria of attachment. As such, they use their owners as a secure base, exploring the environment and manipulating objects more when accompanied by their owners than when alone. Although there are some indications that owners serve as a better secure base than other human beings, the evidence regarding a strong owner-stranger differentiation in a manipulative context is not straightforward. In the present study, we conducted two experiments in which pet dogs were tested in an object-manipulation task in the presence of the owner and of a stranger, varying how the human partner would behave (i.e. remaining silent or encouraging the dog, Experiment 1), and when alone (Experiment 2). Further, to gain a better insight into the mechanisms behind a potential owner-stranger differentiation, we investigated the effect of dogs’ previous life history (i.e. having lived in a shelter or having lived in the same household since puppyhood). Overall, we found that strangers do not provide a secure base effect and that former shelter dogs show a stronger owner-stranger differentiation than other family dogs. As former shelter dogs show more behavioural signs correlated with anxiety towards the novel environment and the stranger, we concluded that having been re-homed does not necessarily affect the likelihood of forming a secure bond with the new owner but might have an impact on how dogs interact with novel stimuli, including unfamiliar humans. These results confirm the owner’s unique role in providing security to their dogs and have practical implications for the bond formation in pet dogs with a past in a shelter.

Introduction

Caregivers do not only provide infants with protection and support but also with security to explore the environment and interact with different stimuli [1]. This so-called “secure base” effect allows infants to learn about the environment and, ultimately, to become self-reliant, independent adults [1, 2]. Most research aiming at understanding the development and consequences of attachment bonds has been conducted on humans, even though the general theoretical framework was originally developed to explain infants-mother relationships in a variety of species [2]. Over the past 20 years, however, another species has become central in the study of attachment bonds: the domestic dog [3]. Due to its long domestication history and co-existence with humans [4], the dog-human relationship has been suggested to parallel the infant-mother bond and to inform us about its evolution and development [5]. Dogs seem to fulfil all four criteria distinguishing attachment bonds from other affectional bonds (see [6] for a recent review): (a) dogs seek for proximity to their caregiver in novel situations, (b) show distress when separated from their owner, (c) approach the owner in threatening or stressful situations (the so-called “safe haven effect”), and (d) explore the environment more in presence of their owner than when alone (the so-called “secure base effect”, [1]).

Owners’ secure base effect on their dogs has been shown mainly using a modified version of an experimental task originally designed to measure toddlers’ attachment towards their caregivers: the Ainsworth’s Strange Situation Test (SST, [1]). In this task, consisting of a series of separations and reunions from/with the caregiver and an unfamiliar person, dogs play and explore more in presence of the owner than when alone or in presence of an unfamiliar experimenter [3, 79]. These differing behaviours in presence of the owner vs. a stranger have been interpreted as a sign that owners can provide their dogs with a secure base and that the dog-owner bond is an individualized relationship that makes the caregiver uninterchangeable with others [1].

This means that a dog-owner relationship can be identified as attachment only if the dog can benefit from the presence of its owner more than that of a stranger or even of another familiar being. It is important to realise, however, that such an owner-stranger differentiation depends not only on the strength of the dog’s bond to its owners but also on the ease with which a dog accepts strangers as social partners. Stranger acceptance varies greatly across individual dogs and does so independent of the dogs’ bonds to their owners [3, 1012]. Many studies, however, do not make an effort to disentangle these two factors, and attempt to characterize the dog-owner relationship based on the dogs’ differing behaviours towards the owner and a stranger. For instance, in a study investigating the development of attachment of guide dogs to their three subsequent caregivers (i.e. the puppy walker, the trainer and, finally, the blind owner), the authors found that young guide dogs discriminate very little between a stranger and their first two attachment figures in the SST [13]. Interpreting these findings is difficult, however, because this lack of differentiation may be due either to the intensive socialization of these dogs and their consequent ability to use strangers as a source of comfort when they are separated from their owner [13] or to their weaker bonds to their initial two, inevitably temporary, caregivers. The attachment of these dogs to their final owner becomes apparent, however, as at a later age they show clearly differing behaviours to their blind owner and strangers [13]. This later finding in guide dogs has been confirmed by other studies that have shown that also pet dogs, after having moved from one household to another, can form strong attachment bonds with their new caregivers [14]. In fact, re-homed adult dogs do not differ in their attachment behaviours when tested with their old or new caregivers [14], suggesting that breaking bonds even repeatedly is not detrimental for dogs to form new attachment relationships even when adults.

Being relinquished in a shelter and adopted later on by a new owner may have different consequences, however [6, 15], if being abandoned by the primary caregiver affects later relationships of dogs, as it does in human children [16]. In dogs, only one non peer-reviewed study has compared the animals’ attachment to their caregivers between dogs adopted from a shelter or having lived in the same household since puppyhood [6, 17]. The authors found that former shelter dogs tested in the SST generally play less, look more towards the partner, and engage more in locomotion (a potential sign of discomfort) than other family dogs [6, 17]. Dogs showed these behavioural patterns both with the owner and with the stranger, suggesting a weak owner-stranger differentiation. Nevertheless, former shelter dogs did not differ from other family dogs in terms of exploration, proximity seeking, physical contact, vocalizations during separation, and greeting. Based on these two sets of results, the authors suggested that former shelter dogs might be more anxious in response to a novel environment and/or to a stranger (as children, [18]), but also that they can indeed form a strong bond with their new owners, even if probably in a less secure way than other family dogs [6, 17]. Based on the fact that former shelter dogs seemed to show a less pronounced owner-stranger differentiation than other family dogs, the authors raised the possibility that former shelter dogs might show a more sociable behaviour towards strangers, as this might have improved their condition in the shelter (i.e. through a favoured treatment by shelter staff) or have favoured their adoption [20]. Having lived in a shelter might affect the dogs’ stranger acceptance as well as their bond towards their new owners, in comparison to dogs who have lived in the same family since puppyhood, for a variety of reasons. For instance, in addition to having been abandoned, living in a stressful environment may also represent a traumatic experience [1921]. Furthermore, owners who end up to relinquish their dog in a shelter may be more likely to have a poor relationship to their dogs [22] or to even mistreat them. To the best of our knowledge, no study has specifically investigated whether dogs with and without a past in a shelter differ in terms of owner-stranger differentiation, specifically regarding the secure base effect. Understanding whether former shelter dogs develop a secure attachment bond with their new caregivers and how the presence of a stranger affects them in potentially challenging situations has both theoretical and practical relevance. In particular, such an investigation could shed light on how flexible dogs are in forming new bonds [15, 23], how novel individualized relationships develop, and what impact the potential disruption of an attachment bond have on cognitive performance [24]. Therefore, in the current study we aimed to directly compare whether and to what extent former shelter dogs and dogs that always lived in the same family (that we refer to as constant family dogs from now on) can benefit from the presence of their owner or of a stranger, as compared to being alone, in a problem solving situation, where one would expect more object manipulation if the owners have a secure base effect on their dogs.

To compare dogs’ behaviours in presence of the owner to when in presence of a stranger or when alone, and investigate potential differences between former shelter dogs and family dogs acquired since puppyhood in this regard, we adopted a recently developed experimental paradigm specifically designed to investigate whether owners and only owners have a secure base effect on dogs [25]. The test consists of an object-manipulation task where dogs are free to interact with an object either alone, in presence of their owner, or in presence of a stranger (in a counterbalanced order), with the aim of investigating whether also strangers could provide security to dogs in a problem-solving task [25]. However, in the first study using this paradigm [25], some methodological limitations did not allow to fully compare to what extent owners and strangers could serve as a secure base for dogs. Specifically, while there was a condition in which the owner would be encouraging the dog, no corresponding condition existed for the stranger. Although results showed that dogs spent more time manipulating the object when the owner was encouraging them as compared to when the stranger was silent, and no differences were found between the silent owner and the silent stranger conditions, the possibility is still open that also an encouraging unfamiliar human could facilitate dogs’ manipulation, when compared to the owner. Moreover, the presence of a coordinating experimenter (in addition to the owner or the stranger) seemed to have provided some support to the dog even if this was not strictly considered as a partner in the experimental design [25].

To overcome these limitations, in the present study, we adopted Horn et al [25] methodology by using a complete 2x2 design in which both the owner and the stranger remained either silent or encouraged the dog to interact with the object, while an unfamiliar experimenter was present in the room in all conditions (Experiment 1). Moreover, we compared the dogs’ behaviours in presence of either the owner or the stranger to when left alone in the room, with no additional experimenter present in the room (Experiment 2). We did so to understand if the sole presence of a stranger could improve dogs’ performance in such problem-solving context (in comparison to when the dog is left alone), even if at a lesser extent than owners.

Based on the hypothesis that dogs form individualized attachment-like relationships specifically with their owner, we expected that dogs would: explore and manipulate the object for longer when the owner was with them than when a stranger was accompanying them, especially when the owner was encouraging them; be close to the owner for longer than to the stranger; spend more time close to the door and to the experimenter in presence of the stranger than when tested with the owner (Experiment 1 and 2). Nevertheless, following the hypothesis that strangers can also act as a secure base, we predicted that dogs would manipulate the object and explore for longer in the stranger presence than when left alone, and spend more time close to the door when left alone than in presence of the stranger (Experiment 2).

Concerning the differences between former shelter dogs and constant family dogs, we formulated three alternative hypotheses (and consequent predictions). (a) Dogs might be very flexible and could be able to build new bonds easily, even when adults [15, 23], resulting in no differences between constant family and former shelter dogs and a less strong owner-stranger differentiation. (b) Dogs’ re-homing past might have an effect on their social development. This might lead to two alternative outcomes. (b1) Having lived in a shelter either negatively affects the future development of a secure attachment bond [26] or (b2) it increases the likelihood of accepting strangers as social partners [13, 15]. In the first case, former shelter dogs would manipulate and explore less in the presence of the owner than other family dogs. However, in the second case, the difference between former shelter dogs and other family dogs would appear in the time spent manipulating and exploring in the stranger condition. (c) Former shelter dogs might form a secure attachment bond with their owners, comparable to the one formed by other family dogs, but be generally more anxious than constant family dogs [6, 18]. Based on this, former shelter dogs would manipulate the apparatus and explore the environment less than constant family dogs with the stranger, while the two groups would not differ in the owner condition.

Overall, the present study allows us to test whether strangers could serve as a secure base for pet dogs and to compare the secure base effect of strangers to the one provided by owners. Moreover, the present study aims at investigating how having lived in a shelter may influence stranger acceptance and bonding with the owner.

Materials and methods

Ethical note

The experimental procedures were approved in accordance with Good Scientific Practice guidelines and national legislation by the Ethic Commission of the University of Veterinary Medicine Vienna (approval number: TK-02/10/2015). The owners were informed about the details of the procedures and gave their written consent to participate with their dogs.

Experiment 1

Subjects

In the first experiment, we tested 56 adult dogs of different breeds (including mixed breeds) that were kept as pets in and near Vienna. Subjects were recruited from the Clever Dog Lab database or via social media platforms. The dogs were at least one year old. Eight dogs had to be excluded due to failing the pre-test or because of technical issues with the video recording system. A total of 48 dogs (30 females and 18 males) completed the pre-test and the test (mean age ± SD = 4.17 ± 2.60 years, range: 1–10 years). Prior to the onset of the experiment, owners were informed that the aim of the study was to test the dog’s attachment to its owner. In addition to the owner, three female experimenters participated in the study. One of them coordinated the experiment (“coordinating experimenter”) whereas the other two took the roles of the two strangers participating in the test (see below).

Two groups of dogs were included: former shelter and constant family dogs. Based on the information provided by the owner, we included dogs into the group “Former Shelter Dogs” (n = 24) if they fulfilled the following criteria: 1) they had been at least three months old when they were brought into a shelter, 2) they had spent at least one month in the shelter, and 3) at the time of testing they had already been living with their owner for at least four months (following [14]). Dogs in the group “Family Dogs” (n = 24) were then selected to match the dogs in the “Former Shelter Dogs” group in respect to breed, sex and age. All constant family dogs had been living with the same owner since their age of 8–12 weeks, while dogs with a past in a shelter have been adopted either when they were less than one year old (26.09%), when they were between 1 and 4 years-old (43.48%) or older than 4 years old (30.43%).

Experimental set-up

The experiments were carried out in an experimental room (3 m x 5 m) of the Clever Dog Lab (University of Veterinary Medicine Vienna, Austria). The room had two doors, one leading to the hallway and the other one leading to an adjacent room. The room was equipped with three cameras that were connected to a monitoring and recording station placed on the hallway. A chair, where the owner or the stranger was seated (depending on the condition, see below), was placed on the left side of the door leading to the hallway. Opposite to this door, a clock was hanging on the wall. The coordinating experimenter was present in the room standing on the right-hand side of the door and was watching the clock during the trials. At the beginning of each trial, she released the dog at a specific spot marked with tape on the floor. The apparatus (a folded kitchen towel in the case of the pre-test or one of four different toys baited with food in case of the test) was placed in the middle of the room (as shown in S1 Fig 1 in S1 File).

Materials

The materials were the same folded kitchen towel and four customary dog toys as used in [11] (see S1 Fig 2 in S1 File). The apparatuses were filled with five pieces of preferred treats, e.g. sausages (∅ 1 cm). The dogs had to manipulate and move the toys either with their paw or muzzle to retrieve these five pieces of reward. We also added a bigger piece of sausage (about 3–5 cm long) that the dogs could not retrieve from the toys, in order to keep them motivated to further manipulate the toy after they had obtained all five treats.

Experimental design and general procedure

Every dog had to pass a pre-test in order to proceed to the test. The pre-test aimed at ensuring that only dogs that were food-motivated enough to engage in manipulating an object also in absence of their owner would participate in the main test.

The pre-test as well as the test followed the same general procedure: first, the coordinating experimenter handled the food reward or baited the apparatus (the kitchen towel or one of the four dog toys) in the hallway in front of the dog. Afterwards she placed it on the marked spot in the experimental room while the dog was watching her from the hallway (the door to the experimental room stayed open) while held by the owner on a leash. Then the coordinating experimenter returned to the hallway and she took the dog’s leash over from the owner and stayed with the dog in the hallway. The owner (in the “Owner” conditions) or the owner and the stranger (in the “Stranger” conditions) entered the experimental room and closed the door. The coordinating experimenter and the dog waited outside the testing room in the hallway. The owner or the stranger sat down on the chair, depending on the condition. In the conditions where the stranger was present, the owner left the room through the door to the adjacent room and waited there until the trial was over. The owner could observe the test from the adjacent room, thanks to a monitoring system. The door between the experimental room and the adjacent room where the owner watched the test trial stayed closed throughout the trial.

The coordinating experimenter waited for 10 seconds after the owner had left, she opened the door, and then she entered the experimental room together with the dog. After closing the door behind them, she released the dog at the designated spot, and positioned herself next to the door. She remained there until the trial was over (until the dog had eaten all treats or after a maximum of one minute), continuously looking at the clock on the other side of the room. The coordinating experimenter did not interact with either the dog, or the owner, or the stranger.

At the end of the trial, the coordinating experimenter called the dog by its name and attached the leash to it. She left the testing room together with the dog, and closed the door. The two then waited in the hallway. In the owner conditions, the owner waited for ten seconds and then left the testing room using the door leading to the hallway. In the stranger conditions, the stranger waited until the coordinating experimenter closed the door, then picked the owner up from the adjacent room. They left the testing room together, using the door to the hallway. A break of approximately three minutes was carried out between trials when the dog was free to interact with its owner.

Pre-test

The pre-test comprised four short trials repeated in a fixed order where the dogs needed to work more and more for the food, first in presence and then in absence of their owner.

  • Trial 1: five pieces of food were placed on the floor and the owner was present, seated on the chair next to the door and reading a magazine.

  • Trial 2: five pieces of food were placed on the floor, as in the first trial. However, after she/he had entered, the owner left the testing room through the door leading to the adjacent room where he or she waited until the trial was over.

  • Trial 3: the food was hidden in the folded cotton towel lying on the floor, and the owner was present like in the first trial.

  • Trial 4: the treats were again hidden in the folded towel as in the third trial but the owner was absent like in the second trial.

The dog passed the pre-test and could proceed to the test if she had eaten the treats at least once in the absence of its owner and in at least 3 out of 4 trials.

The coordinating experimenter was present in the testing room during the trials, thus the dog was never alone during the pre-test. Each trial ended when the dog had eaten all treats or after a maximum of one minute.

Test

The test phase consisted of four different conditions. Each condition was conducted only once, therefore each dog participated in a total of four trials. The order of conditions was counterbalanced across dogs. Each trial lasted for five minutes. Within this period, the dog had the possibility to manipulate the apparatus in order to obtain the treats. In each trial, the dog received a different toy. The assignments of the four toys and the three experimenters to the different conditions were pseudo-randomized so that each toy and each experimenter were used evenly across conditions. As such, two different persons acted as strangers in the two stranger conditions.

Across conditions, we varied whether (in addition to the coordinating experimenter) the owner or the stranger (partner) was present in the room and how they behaved during the test: they either remained silent or encouraged the dog to manipulate the toy in order to retrieve a treat.

“Silent Owner” condition: the owner was present in the testing room but had to remain silent reading a magazine. The owner was not allowed to give commands, to point or to draw the dog’s attention to the toy in any other way. However, the owner was allowed to pay attention to his/her dog and to pet it when it approached him/her.

“Encouraging Owner” condition: the owner was present and allowed to direct the dog’s attention to the toy, thus motivating the dog verbally and through pointing gestures. Nevertheless, the owner had to remain seated throughout the trial.

“Silent Stranger” condition: a stranger sat on the owner’s chair and behaved in the same way as the owner behaved in the “Silent Owner” condition.

“Encouraging Stranger” condition: a second stranger took the place of the owner and motivated the dog to manipulate the apparatus as described in the “Encouraging Owner” section.

Behavioural analysis

All experiments were videotaped and coded using Solomon Coder (© András Peter). In particular, the durations of the following behavioural variables were coded: “Manipulation” of the toy, “Close to partner” (either the owner or the stranger, depending on the testing condition), “Close to experimenter” (specifically referring to the coordinating experimenter), “Close to door”, and “Exploration” of the room. All coded behaviours followed the definitions used in the study by [25]: “Manipulation” was coded whenever the dog was touching the toy with its muzzle or paw; “Close to partner” was recorded when the dog was in arm’s reach of the respective person. If the dog was in reach of both persons present (coordinating experimenter and partner—owner or stranger), the dog was coded as being close to the person who was positioned closer to the head of the dog; “Close to door” was coded when the dog was standing, sitting or lying within the distance of one body length in front of one of the two doors and was looking at the door; “Exploration” was coded whenever the dog’s muzzle was within 5 centimetres of any surface within the room. The videos were coded by two observers independently. Inter-observer reliability between the two of them was established by double coding 20% of the videos and calculating the Intra-class Correlation Coefficient (ICC). We obtained good or excellent levels of inter-observer reliability for all coded behaviours (ICC for Manipulation: 0.99; Close to Partner: 0.89; Close to Door: 0.99; Exploration: 0.77).

Statistical analyses

All behavioural variables were analysed as proportion of duration (amount of time in which the dog showed that specific behaviour divided per the total trial duration). Generalized Mixed Models (GLMM) with beta (Manipulation and Close to Experimenter) or beta inflated (Close to Door, Close to Partner, and Exploration) distribution were used to analyse whether the following predictors were associated with the behavioural variables analysed in the current study: partner (owner vs. stranger), behaviour of the partner (silent vs. encouraging), origin (constant family vs. former shelter), order of condition (1st, 2nd, 3rd or 4th), and the three two-way interactions between partner, behaviour of the partner, and origin. The sex of the dog was included in the model to control for it. The individual dog was included as random effect. Non-significant interactions were removed from the model. When the interaction between partner and origin was found to be significant, we investigated the effect of partner post-hoc separately for constant family and former shelter dogs (Bonferroni correction was applied to correct for multiple testing). Models were fitted using the package gamlss [27] in the software R (version: 3.6.2, R Core Team, 2019). Homoscedasticity and normality of model residuals were assessed via plots of residuals against fitted values and via qq-plots respectively. The threshold for significance was alpha = 0.05 for all tests.

Results

Manipulation. Dogs spent more time manipulating the apparatus in presence of the owner than in presence of the stranger (GLMM, estimate ± SE = 0.76 ± 0.15, df = 1, t = 5.03, p < 0.001, Fig 1), and constant family dogs spent more time manipulating the apparatus than former shelter dogs (GLMM, estimate ± SE = 1.04 ± 0.15, df = 1, t = 6.67, p < 0.001, Fig 1). Behaviour of the partner, order of condition and all interactions resulted not significant (all p > 0.05, S1 Table 1 in S1 File).

Fig 1. Percentage of time spent showing the behaviours analysed in Experiment 1.

Fig 1

Percentage of time spent A) manipulating the object; B) close to the partner; C) close to the door; D) exploring in Experiment 1. Median and interquartile range (IQR; represented by the box), 25th percentile + 1.5 IQR, and 75th − 1.5 IQR (represented by the lower and the upper whiskers respectively).

Close to the partner. Dogs spent more time close to the partner when this was encouraging them than when she/he was silent (GLMM, estimate ± SE = 0.35 ± 0.14, df = 1, t = 2.63, p = 0.01). In addition, we found a significant effect of the interaction between the partner and the origin of the dog (GLMM, estimate ± SE = 0.94 ± 0.27, df = 1, t = 3.47, p < 0.001, Fig 1). In particular, former shelter dogs spent more time close to the owner than to the stranger (GLMM, estimate ± SE = 0.59 ± 0.20, df = 1, t = 2.96, p = 0.004, Fig 1), while constant family dogs spent equal time with both partners (GLMM, estimate ± SE = 0.30 ± 0.19, df = 1, t = 1.52, p = 0.13, Fig 1). Overall dogs spent more time close to the partner as sessions went by (GLMM, estimate ± SE = 0.14 ± 0.06, df = 1, t = 2.32, p = 0.02). The other interactions resulted not significant (all p > 0.05, S1 Table 1 in S1 File).

Close to the door. Dogs spent more time close to the door when the stranger was present than when the owner was present (GLMM, estimate ± SE = 0.69 ± 0.16, df = 1, t = 4.18, p < 0.001, Fig 1), more in the silent trials than in the encouraging trials (GLMM, estimate ± SE = 0.52 ± 0.16, df = 1, t = 3.33, p = 0.001) and former shelter dogs did so longer than constant family dogs (GLMM, estimate ± SE = 0.56 ± 0.16, df = 1, t = 3.54, p < 0.001, Fig 1). None of the interactions affected the time spent close to the door (all p > 0.05, S1 Table 1 in S1 File).

Exploration. Dogs spent more time exploring when the partner was encouraging them than when she/he was silent (GLMM, estimate ± SE = 0.37 ± 0.11, df = 1, t = 3.43, p < 0.001). In addition, we found a significant interaction between partner and origin of the dog (GLMM, estimate ± SE = 0.67 ± 0.22, df = 1, t = 3.05, p = 0.003). In particular, constant family dogs spent more time exploring when tested with the stranger than when tested with the owner (GLMM, estimate ± SE = 0.68 ± 0.16, df = 1, t = 4.19, p < 0.001, Fig 1), while no such difference was found in shelter dogs (GLMM, estimate ± SE = -0.02 ± 0.16, df = 1, t = -0.13, p = 0.89, Fig 1). Overall dogs spent less time exploring as sessions went by (GLMM, estimate ± SE = -0.11 ± 0.05, df = 1, t = -2.17, p = 0.03). All other interactions resulted not significant (all p > 0.05, S1 Table 1 in S1 File).

Close to the experimenter. Dogs spent more time close to the coordinating experimenter in the stranger’s presence than when the owner was present (GLMM, estimate ± SE = 0.61 ± 0.15, df = 1, t = 3.96, p < 0.001, Fig 2) and more if they were constant family dogs than if they were former shelter dogs (GLMM, estimate ± SE = 0.63 ± 0.15, df = 1, t = 4.13, p < 0.001, Fig 2). Overall dogs spent less time close to the coordinating experimenter as sessions went by (GLMM, estimate ± SE = -0.19 ± 0.07, df = 1, t = -2.85, p = 0.005). Behaviour of the partner and all interactions resulted not significant (all p > 0.05, S1 Table 1 in S1 File).

Fig 2. Percentage of time spent close to the coordinating experimenter in Experiment 1.

Fig 2

Median and interquartile range (IQR; represented by the box), 25th percentile + 1.5 IQR, and 75th − 1.5 IQR (represented by the lower and the upper whiskers respectively).

Experiment 2

Subjects

We recruited 30 adult dogs following the same selection process and criteria as in the first experiment. The mean age ± SD was 5 ± 3.71 years, range: 1–15 years. Six dogs had to be excluded due to failing the pre-test or because of technical issues with the monitoring system. A total of 24 dogs (15 females and 9 males) passed the pre-test and completed the test (mean age ± SD = 4.79 ± 3.46 years, range: 1–15 years). Twelve dogs were “Former shelter dogs” while the other 12 were “Family dogs”. Dogs were selected and assigned to the two groups using the same criteria as for Experiment 1. Also in this case all constant family dogs have been acquired when younger than 12 months, while former shelter dogs were adopted when younger than one year (9.09%), between one and 4 years of age (63.64%) and when older than 4 years (27.27%).

Differently from the previous experiment, the coordinating experimenter was not present in the testing room during testing, instead she observed the experiment through the monitoring system from the hallway. Only two experimenters participated in this experiment since the number of trials was reduced (i.e. only one stranger condition, see below). Their assignment as stranger or coordinating experimenter to the single tests was again pseudo-randomized.

Materials and experimental set-up

The experimental room remained the same as in Experiment 1, except that the clock had been removed since the coordinating experimenter was not present in the testing room in Experiment 2. Furthermore, we excluded the blue wobbling dog toy (see S1 Fig 2 in S1 File) which had been used in the first experiment, since the number of trials was reduced to three.

Experimental design and general procedure

The general procedure and the experimental design were similar to those in Experiment 1, except that the coordinating experimenter was not present anymore in the testing room during the trials. For this aim, the coordinating experimenter returned to the hallway after unleashing the dog at the release point. During the trials, she waited outside of the room, and observed the trials through the monitoring equipment. When the trial was over, the coordinating experimenter entered the room again, called the dog by its name and leashed it before leaving the room.

Pre-test

Each dog participated in the same four pre-test trials as in Experiment 1, with the only exception that the coordinating experimenter was not in the room during the trials.

Test

We conducted three trials in this experiment, as follows. As in the first study, the order of the trials was counterbalanced across dogs and the assignment of the three toys was pseudo-randomized.

“Owner” condition: followed the procedure of the “Silent Owner” condition of Experiment 1, with the exception that the coordinating experimenter was not present in the room.

“Stranger” condition: followed the procedure of the “Silent Stranger” condition of Experiment 1, with the exception that the coordinating experimenter was not present in the room.

“Alone” condition: the owner waited in the hallway during the whole trial. The coordinating experimenter released the dog in the experimental room and immediately went back to the hallway, living the dog alone in the experimental room.

Behavioural analysis

The same behaviours as in Experiment 1 were coded. However, in the “Alone” condition, “Close to partner” was coded when the dog was within the distance of one body length to the empty chair.

Statistical analyses

All behavioural variables were analysed as proportion of duration (amount of time in which the dog showed that specific behaviour divided per the total trial duration). Generalized Mixed Models (GLMM) with beta (Close to Partner and Exploration) or beta inflated (Manipulation and Close to Door) distribution were used to analyse whether the following predictors were associated with the behavioural variables analysed in the current study: partner (owner vs. stranger vs. alone), origin (constant family vs. former shelter), order of condition (1st, 2nd, or 3rd), and the two-way interaction between partner and origin. The sex of the dog was included in the model to control for it. The individual dog was included as random effect. Whenever the two-way interaction was non-significant, it was removed from the model. When the interaction between partner and origin was found to be significant, we investigated the effect of partner post-hoc separately for constant family and former shelter dogs (Bonferroni correction was applied to correct for multiple testing). Models were fitted using the package gamlss [27] in the software R (version: 3.6.2, R Core Team, 2019). Homoscedasticity and normality of models’ residuals were assessed via plots of residuals against fitted values and via qq-plots. The threshold for significance was alpha = 0.05 for all tests.

Results

Manipulation. Dogs spent more time manipulating the apparatus in presence of the owner than in presence of the stranger (GLMM, estimate ± SE = 0.86 ± 0.28, df = 1, t = 3.03, p = 0.004, Fig 3) and more with their owner than when they were tested alone (GLMM, estimate ± SE = 1.09 ± 0.30, df = 1, t = 3.64, p < 0.001, Fig 3). No difference was found between the condition in which dogs were tested alone or with the stranger (GLMM, estimate ± SE = 0.22 ± 0.30, df = 1, t = 0.73, p = 0.47, Fig 3). Moreover, constant family dogs spent more time manipulating the apparatus than former shelter dogs (GLMM, estimate ± SE = 1.20 ± 0.25, df = 1, t = 4.74, p < 0.001, Fig 3). The order of condition and interaction between partner and origin of the dog resulted not significant (all p > 0.05, S1 Table 2 in S1 File).

Fig 3. Percentage of time spent showing the behaviours analysed in Experiment 2.

Fig 3

Percentage of time spent A) manipulating the object; B) close to the partner; C) close to the door; D) exploring in Experiment 2. Median and interquartile range (IQR; represented by the box), 25th percentile + 1.5 IQR, and 75th − 1.5 IQR (represented by the lower and the upper whiskers respectively).

Close to the partner. We found a significant effect of the interaction between the partner and the origin of the dog. In particular, shelter dogs spent more time close to the owner than close to the chair in the alone condition (GLMM, estimate ± SE = 1.32 ± 0.44, df = 1, t = 2.98, p = 0.006, Fig 3) but there was no difference between the stranger and owner condition or between the stranger and the alone condition (both p > 0.05). There were also no significant differences across conditions in constant family dogs (all p > 0.05, S1 Table 2 in S1 File). The order of condition resulted not significant (p > 0.05, S1 Table 2 in S1 File).

Close to the door. Dogs spent more time close to the door when tested alone than when tested with the owner (GLMM, estimate ± SE = 1.05 ± 0.30, df = 1, t = 3.51, p < 0.001, Fig 3). However, no difference was found between the stranger and the owner condition (GLMM, estimate ± SE = 0.65 ± 0.31, df = 1, t = 2.13, p = 0.04, not significant after correction for multiple comparisons, Fig 3), nor between the stranger and the alone condition (GLMM, estimate ± SE = 0.40 ± 0.26, df = 1, t = 1.50, p = 0.14, Fig 3). Shelter dogs spent more time close to the door than constant family dogs (GLMM, estimate ± SE = 0.70 ± 0.24, df = 1, t = 2.91, p < 0.001, Fig 3). The order of condition and interaction between partner and origin of the dog resulted not significant (all p > 0.05, S1 Table 2 in S1 File).

Exploration. Dogs spent less time exploring when tested with the owner than when tested alone (GLMM, estimate ± SE = -0.64 ± 0.25, df = 1, t = -2.61, p = 0.01, Fig 3). The proportion of time dogs spent exploring did not differ when they were tested with the stranger or alone (both p > 0.05, Fig 3, S1 Table 2 in S1 File). The order of condition, the origin of the dog, and the interaction between partner and origin of the dog resulted not significant (all p > 0.05, S1 Table 2 in S1 File).

Discussion

The present study had three main aims: investigate whether strangers could serve as a secure base for pet dogs and to what extent they would do so less than owners. Thirdly, as an owner-stranger differentiation might depend on a dog’s life history, we aimed to examine whether the secure base effect provided by owners (and potentially by strangers) would differ between dogs with a past in the shelter and dogs who have always lived with the same owner. We did so by conducting two experiments where dogs faced a problem-solving task in the presence of the owner or a stranger. We varied the behaviour of the owner and the stranger (either remaining silent or encouraging the dog, Experiment 1), the presence of an unfamiliar coordinating experimenter in the room (only present in Experiment 1), and the overall presence of a partner (i.e. the dog was alone in the room in one condition of Experiment 2).

One of our main findings is that none of the two experiments found evidence that strangers could provide dogs with a secure base effect. In fact, no difference between the alone and the stranger conditions could be found in Experiment 2. However, we could confirm previous evidence that owners’ presence is a source of security for dogs [3, 25, 28]. We found this effect to be independent from the owner’s behaviour (either remaining silent or encouraging the dog) and consistent across both experiments. As such, we found that dogs, independent of their past, manipulated the object longer in presence of the owner than in presence of the stranger (both in the Experiment 1 and 2) or when left alone (Experiment 2). Furthermore, dogs spent more time close to the door (both in Experiment 1 and 2) or to the coordinating experimenter (Experiment 1) when they were alone or when the stranger was present than when the owner was present, suggesting that dogs were less comfortable in the experimental environment when separated from their owners than when the owner was in the room. These results confirm that dogs form individualized relationships with their owner [3, 25, 28] and do not seem to use a stranger as a secure base in this problem-solving context. Importantly, results of the two experiments were consistent, suggesting that the presence of an unfamiliar coordinating experimenter in Experiment 1 (in addition to the person acting as a partner) did not play a major role in affecting the behaviour of the subjects.

It is important to note that in this study the person acting as a stranger had never interacted with the dog before the onset of the experiment. It is possible that these results would have been different if a short familiarization phase had preceded the test. In fact, previous studies have shown that dogs might show attachment-like behaviours towards a human even if this has interacted with them only three times for a few minutes [15]. Future studies will need to address whether and when dogs can benefit from the presence of other humans than their owners, depending on the degree of their familiarity (e.g. after one or more interaction sessions).

Differently from Horn et al.’s study using a similar procedure [25], here we did not find that encouragement had an effect on dogs’ object manipulation. However, we found that dogs explored more, spent more time close to the partner, and less time close to the door when the partner was giving encouragements than when he/she was silent, suggesting that generally dogs were more active in the encouraging than in the silent conditions. This finding highlights that similar studies addressing the effect of human communication on dogs’ problem solving need to control for the owners’ effect on the general activity of the dogs that may indirectly increase (or in certain cases decrease, see [29]) the problem solving success of the dogs.

Concerning our second question (whether owner-stranger differentiation depends on the dogs’ life history), we found that the above-mentioned general effects did not depend on the origin of the dogs. In fact, the two tested groups (former shelter and constant family dogs) differed neither in terms of owner-alone differentiation in object manipulation, proximity to the door, room exploration nor in owner-stranger differentiation in terms of object manipulation and proximity to the door. Furthermore, encouragement affected staying in proximity to door and to the partner, and exploration similarly in both groups of dogs. Nevertheless, we did find other differences between the former shelter and constant family dogs. First, in Experiment 1 (but not in Experiment 2) we found that exploration was not affected by the identity of the partner in former shelter dogs, while constant family dogs explored the environment longer in the presence of the stranger than in the presence of the owner. This latter pattern observed in constant family dogs seems to suggest that exploration may have been more motivated by the animals’ distress (evoked by the owner’s absence or the stranger’s presence) rather than by their desire to learn about the environment (that should have rather been increased when the owner’s presence provided a secure base). If exploration was a sign of distress also in the case of former shelter dogs, then a similar duration of exploration in the presence of the owner and of the stranger might be either due to low stress when the owner is absent (stranger condition) or to received support when the owner is present (owner condition). As former shelter dogs spent more time close to the owner than to the stranger (both in Experiment 1 and 2), it is possible to assume that former shelter dogs could use their owners as a secure base to a lesser extent than constant family dogs. However, as former shelter dogs manipulated the objects more and spent less time close to the door in presence of their owner than in presence of the stranger to an extent similar to constant family dogs, we have no clear evidence that these two groups of dogs would have different bonds to their owners.

Rather, we suggest that the differences between former shelter and constant family dogs described above, including less object manipulation and more time spent close to the door (both in Experiment 1 and 2) in former shelter dogs, show that former shelter dogs were less confident with interacting with the novel object and with being in the experimental room than constant family dogs. Importantly, former shelter dogs’ general wariness did not seem to be only related to the physical environment but also to the stranger. In fact, former shelter dogs spent less time close to the coordinating experimenter than constant family dogs (Experiment 1) and they spent less time close to the stranger than to their owners (while constant family dogs did not show such a difference, Experiment 1). These results are in line with the only previous study comparing former shelter dogs to other family dogs in the SST, also suggesting that former shelter dogs are able to form an attachment bond with their owner but also that they might be more anxious when facing novel stimuli than other family dogs [6, 17]. However, although these results are in line with previous evidence showing that shelter dogs are more fearful when confronted with an unfamiliar human than pet dogs [30, 31], we recommend caution in comparing the behaviour of dogs when still housed in a stressful environment like the shelter [1921] to the one of dogs who have been living as pets already since months (as in the present study). Taken together, the differences between the two groups do not seem to depend on the relationship with the owner per se, but rather on former shelter dogs’ perceiving the test situation more stressful (as in [6, 17]).

What factors are the exact cause of the above-mentioned differences between former shelter dogs and constant family dogs remains to be explored. In fact, multiple elements might have contributed to such differences: lower manipulation time could be due to having had fewer chances to interact with novel human artefacts making former shelter dogs more neophobic [32] or less persistent [33] than constant family dogs. Traumatic experiences connected to the relinquishment or their stay in the shelter may have led to the development of learned helplessness [34, 35], hindering their motivation to engage in problem-solving activities. Moreover, differences in the interaction with the social partner (i.e. shelter dogs spending less time close to the coordinating experimenter and more time close to the owner than to the stranger in comparison to constant family dogs) could be due to potential previous mistreatment [36, 37], traumatic experience before the shelter [36], and/or in the shelter [1921], and potentially to the disruption of the first attachment bond to their first owners [38]. Additionally, it cannot be excluded that the dogs in our former shelter dog group had differed from members of the constant family dog group already before ending up in the shelter because of potential behavioural problems (e.g. anxiety) that might have emerged before the relinquishment (and potentially be the reason for it, [22]). Or that owners adopting from shelters might be different to those adopting puppies from private hands, with adopters of shelter dogs potentially being more aware and more willing to accept behavioural problems (e.g. anxiety) than owners acquiring a dog from a breeder [39, 40]. Being more tolerant towards potential behavioural problems might influence how an owner interacts with his/her dog, ultimately influencing a dog’s behaviour in novel situations [12]. For instance, more tolerant owners might be less inclined to punish their dogs when these show a problematic behaviour [41] or show a warmer and more affectionate interaction style, increasing their dogs’ reliance on their guidance and their sense of security [12]. However, to the best of our knowledge, no study has investigated whether adopters from shelters behave differently towards their dogs than other dog owners and whether these differences influence their dogs’ behaviour yet.

An additional element that future studies would need to take into account is the time that adopted dogs have spent with their new owner before the onset of the experiment. A previous study, in fact, have shown that dogs’ attachment towards their owners depended on how long they have been adopted [42]. The present sample size was not big enough to investigate the effect of this variable, which might have contributed to the within-group variability in former shelter dogs. We recommend future studies to take this element into account, as it might affect the ease with which former shelter dogs accept strangers as well as their emotional reactivity to novel stimuli [42].

Our findings have important practical implications. Despite some general differences to constant family dogs, former shelter dogs also proved to be able to benefit from their owner’s secure base effect, suggesting that adopting an adult dog from a shelter does not hinder the development of an attachment bond. Showing that re-homed dogs can form attachment bonds to their human caregivers comparable to bonds of dogs that have always lived in the same family could improve humans’ attitudes to adoption from shelters (potentially increasing the adoption rate, [40]). Still, differences related to motivation in object manipulation and anxiety in a novel situation have emerged, suggesting that previous experiences might affect dogs’ coping with novel environments and problem solving performance. Being aware of such behavioural characteristics can help owners have more realistic expectations of their dogs, reducing the risk of frustration and potential dissatisfaction, both potentially leading to a weak dog-human bond and relinquishment. Understanding how owners can provide security to their dogs when interacting with the environment is utterly important for those dogs who come from a history of deprivation and who need to be introduced to the complexities of the human environment. Understanding whether former shelter dogs differ from dogs adopted in puppyhood can help not only adopters, but also help design specific interventions to enrich the lives of dogs hosted in shelters, to support owners in their interactions with their newly adopted dogs, and to familiarize dogs with environments they might live in after adoption.

Supporting information

S1 File. Sketch of the experimental room, materials used, tables with complete models results from Experiment 1 and 2.

(DOCX)

S2 File. Complete dataset.

(XLSX)

Acknowledgments

We are most thankful to Lisa Horn for contributing to the initial plan of this study, to Sarah Marshall-Pescini and all IMHAI teachers for discussing it at intermediate stages, and to Lisa Wallis for taking part of the supervision. We thank Karin Bayer for administrative support, and Wolfgang Berger and Peter Füreder for technical support. In addition, we sincerely thank all owners and dogs for their participation in the study.

Data Availability

All relevant data are within the paper and its Supporting information files.

Funding Statement

Writing was supported by the Austrian Science Fund (FWF project P-34749 to GC).

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PONE-D-21-22971Secure base effect in former shelter dogs and other family dogs: strangers do no provide security in a problem-solving taskPLOS ONE

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Reviewer #1: The present manuscript reports a study on dog-owner attachment. The goal of the study was twofold: 1) to disentangle between the secure-base effect of owner vs stranger and 2) to investigate how a dog’s history (namely, having lived in the same household since puppyhood vs having lived part of life in a shelter) would influence this secure-base effect. To that end, in two experiments, shelter and family dogs were exposed to a problem-solving task where it was varied whom was present with the dog in the experimental room (owner, stranger, alone), as well as the behavior of the partner (encouraging, silent). It was hypothesized that, if only owners provide a secure-base effect to their dogs, dogs would spend more time trying to solve the problem when the owner was present than when the stranger was present or the dog was alone. Secondly, encouragement was expected to facilitate object manipulation (i.e., dogs would persevere more), at least in the presence of the owner. Finally, differences in behavior were expected to emerge as a function of dogs’ past history. Three major results were found:

1) Owners, but not strangers, provided dogs with a secure base effect – dogs manipulated the object longer in the presence of the owner than in the presence of the stranger or when alone;

2) This effect was independent of the owner’s behavior (silent vs encouraging)

3) The above mentioned effects did not depend on dogs’ past history. However, there were some differences in the behavior of the two groups, with shelter dogs being overall warier in the novel environment and in relation to the stranger (exhibiting more behavioral signs correlated with anxiety).

Authors concluded that both dogs that have lived since puppyhood in the same household and dogs that have been re-homed can develop a secure attachment to their owners, but that having spent some time in a shelter can hinder these dogs’ ability to cope with new environments and people.

The study was conducted with rigor, the methods are overall well-presented and the results support the conclusions. However, some more effort has to be put in the Introduction section, on the presentation of the state of the art as well as on the derivation and presentation of hypothesis. Specifically, because the study has two research questions that are answered by crossing/combining the results of the two conducted experiments, the authors need to further work on presenting the state of the art that informs their two questions and to better explain how they relate to each other, as well as to clarify the derivation of their hypothesis. I think this can be achieved mainly with some re-writing and re-organization of the Introduction section. I detail my comments in what follows.

Introduction

First, I think the Introduction needs to be shortened. I feel five pages is a lot concerning the size of the current paper but, more importantly, shortening will allow the authors to be more straightforward and direct when presenting the theoretical background and the gap that the current piece of research aims at filling. Some examples/suggestions are:

- Condense what is presented in paragraphs between lines 114 and 142. I think such a detailed presentation of Horn’s study is not necessary.

- Paragraphs between line 143 and 171: Can the authors condense and present the ideas in a more straightforward way? The level of methodological detail given here is, in my opinion, not necessary.

- As it is currently written, it almost seems that the Introduction will end on line 113. However, after that, the authors still discuss the issue on disentangling between owner and stranger secure-base effects, and afterwards they go back to shelter vs family dogs again. I would advise a reorganization in a way where the reader is not jumping from one topic to the other. An additional suggestion is that the hypotheses are only presented in the final paragraph of the Introduction. Personally, I do not think the authors need to go into so much detail regarding hypotheses in this section (currently there are several hypotheses presented across the Introduction). I would rather opt by presenting more general hypotheses (and the specific goals of each Experiment, which is not done in the current version of the manuscript) and maybe latter (for example, in the Methods section) present all the more “specific” hypotheses in detail. If the authors decide they want to present all the detailed hypotheses, I would strongly advise presenting them using bullet points, such that it is easier for the reader to follow and consult when needed.

Another comment I have to the Introduction concerns the ideas presented in lines 59-64:

“It is important to realise, however, that such an owner-stranger differentiation depends not only on the strength of the dog’s bond to its owners but also on the ease with which a dog accepts strangers as social partners. Stranger acceptance varies greatly across individual dogs and does so independent of the dogs’ bonds to their owners [3,10–12]. Many studies, however, do not make an effort to disentangle these two factors…” -- I wonder whether the authors aimed at disentangling this owner bond vs stranger acceptance effects in the present study. If they did, it is not currently clear how. If they did not, then maybe this specific issue can be dropped out of the Introduction.

Line 162-163: Please state earlier that an experimenter was always present in the room in Experiment 1, such that it is clear from early on that this was the case.

Methods

Please state early on in this section (in the Experimental Design and General Procedure) when the experimenter was or was not present in the room (in Experiment 1, Experiment 2 and pre-tests).

Line 245 - Who was holding the dog while “she placed it on the marked spot in the experimental room”?

Lines 248-249 - Why this difference between conditions? Why didn’t the owner and the stranger entered together as well in the “owner condition”?

Line 259: “At the end of the trial” – The information on what determined the end of a trial should be presented already here (currently it is only presented later, on line 270)

Line 260 – Please add to where the experimenter “left the testing room together with the dog” (hallway?)

The info on lines 271-280 should come in line 268 right after “first in presence and then in absence of their owner”.

Lines 406-408: I think the paper benefits if this info is presented earlier (see comment above).

Results

I think there are too many graphs/tables in this section. Please think reducing the number of figures – maybe create two big figures (one for Experiment 1 and one for Experiment 2) with several panels. Moreover, I would suggest moving the tables to supplementary material.

Discussion

My only comment to this section is that I missed seeing the present results compared/contrasted with those from Previde and Valsecchi (2007) [6, 17], the only other published study comparing attachment in shelter vs ‘family’ dogs.

**********

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Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: Yes: Ana Catarina Vieira de Castro

[NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files.]

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PLoS One. 2021 Dec 22;16(12):e0261790. doi: 10.1371/journal.pone.0261790.r002

Author response to Decision Letter 0


8 Oct 2021

Rebuttal letter

Manuscript PONE-D-21-22971 “Secure base effect in former shelter dogs and other family dogs: strangers do no provide security in a problem-solving task”

Dear Editor,

Thank you for considering the present manuscript for publication in PLOS ONE. We are pleased to see that the manuscript was positively received and that only few points have been raised by the reviewers that would need to be revised.

Please find below the answers to the points raised by you and by the reviewers. The answers are reported in bold immediately after each point.

Kind regards,

Giulia Cimarelli, PhD (corresponding author)

Journal requirements:

1. Please ensure that your manuscript meets PLOS ONE's style requirements, including those for file naming.

Done.

2. Please review your reference list to ensure that it is complete and correct.

Done.

Review Comments to the Author

Reviewer #1: The present manuscript reports a study on dog-owner attachment. The goal of the study was twofold: 1) to disentangle between the secure-base effect of owner vs stranger and 2) to investigate how a dog’s history (namely, having lived in the same household since puppyhood vs having lived part of life in a shelter) would influence this secure-base effect. To that end, in two experiments, shelter and family dogs were exposed to a problem-solving task where it was varied whom was present with the dog in the experimental room (owner, stranger, alone), as well as the behavior of the partner (encouraging, silent). It was hypothesized that, if only owners provide a secure-base effect to their dogs, dogs would spend more time trying to solve the problem when the owner was present than when the stranger was present or the dog was alone. Secondly, encouragement was expected to facilitate object manipulation (i.e., dogs would persevere more), at least in the presence of the owner. Finally, differences in behavior were expected to emerge as a function of dogs’ past history. Three major results were found:

1) Owners, but not strangers, provided dogs with a secure base effect – dogs manipulated the object longer in the presence of the owner than in the presence of the stranger or when alone;

2) This effect was independent of the owner’s behavior (silent vs encouraging)

3) The above mentioned effects did not depend on dogs’ past history. However, there were some differences in the behavior of the two groups, with shelter dogs being overall warier in the novel environment and in relation to the stranger (exhibiting more behavioral signs correlated with anxiety).

Authors concluded that both dogs that have lived since puppyhood in the same household and dogs that have been re-homed can develop a secure attachment to their owners, but that having spent some time in a shelter can hinder these dogs’ ability to cope with new environments and people.

The study was conducted with rigor, the methods are overall well-presented and the results support the conclusions. However, some more effort has to be put in the Introduction section, on the presentation of the state of the art as well as on the derivation and presentation of hypothesis. Specifically, because the study has two research questions that are answered by crossing/combining the results of the two conducted experiments, the authors need to further work on presenting the state of the art that informs their two questions and to better explain how they relate to each other, as well as to clarify the derivation of their hypothesis. I think this can be achieved mainly with some re-writing and re-organization of the Introduction section. I detail my comments in what follows.

Introduction

First, I think the Introduction needs to be shortened. I feel five pages is a lot concerning the size of the current paper but, more importantly, shortening will allow the authors to be more straightforward and direct when presenting the theoretical background and the gap that the current piece of research aims at filling. Some examples/suggestions are:

We shortened and restructured the Introduction, making it more concise than before.

- Condense what is presented in paragraphs between lines 114 and 142. I think such a detailed presentation of Horn’s study is not necessary.

We drastically reduced this part and condensed the previous three paragraphs into one (lines 115-131).

- Paragraphs between line 143 and 171: Can the authors condense and present the ideas in a more straightforward way? The level of methodological detail given here is, in my opinion, not necessary.

We reduced the explanation of the methods to the minimum. The paragraph now extends from line 132 to line 139.

- As it is currently written, it almost seems that the Introduction will end on line 113. However, after that, the authors still discuss the issue on disentangling between owner and stranger secure-base effects, and afterwards they go back to shelter vs family dogs again. I would advise a reorganization in a way where the reader is not jumping from one topic to the other.

We restructured the Introduction according to the following: general intro about the secure base effect � the secure base effect in dogs and the problem with previous studies: owner-stranger differentiation not always clear, especially for those dogs changing caregiver throughout their lifetime (e.g. guide dogs) � presentation of the phenomenon that former shelter dogs might differ from family dogs acquired since puppyhood in owner-stranger differentiation because of their life experiences � short presentation of the methods and aim for each experiment � hypotheses and predictions for the overall owner-stranger differentiation and for the former shelter vs. constant family dogs potential differences.

An additional suggestion is that the hypotheses are only presented in the final paragraph of the Introduction. Personally, I do not think the authors need to go into so much detail regarding hypotheses in this section (currently there are several hypotheses presented across the Introduction). I would rather opt by presenting more general hypotheses (and the specific goals of each Experiment, which is not done in the current version of the manuscript) and maybe latter (for example, in the Methods section) present all the more “specific” hypotheses in detail. If the authors decide they want to present all the detailed hypotheses, I would strongly advise presenting them using bullet points, such that it is easier for the reader to follow and consult when needed.

We have moved all hypotheses and predictions to the end of the introduction (lines 140-162) and wrote them in a more straightforward manner. We think that listing each prediction using bullet points is not necessary anymore.

Another comment I have to the Introduction concerns the ideas presented in lines 59-64:

“It is important to realise, however, that such an owner-stranger differentiation depends not only on the strength of the dog’s bond to its owners but also on the ease with which a dog accepts strangers as social partners. Stranger acceptance varies greatly across individual dogs and does so independent of the dogs’ bonds to their owners [3,10–12]. Many studies, however, do not make an effort to disentangle these two factors…” -- I wonder whether the authors aimed at disentangling this owner bond vs stranger acceptance effects in the present study. If they did, it is not currently clear how. If they did not, then maybe this specific issue can be dropped out of the Introduction.

I the present study we could directly investigate stranger’s acceptance/social support in the experimental situation thanks to the comparison with the alone condition (Experiment 2). That is, we did not only compare the behaviour of dogs in the presence of the owner and in the presence of the stranger, but compared both conditions to the alone one. Moreover, the comparison between the two groups (former shelter dogs and constant family dogs) helped us disentangling the two options. In order to make this points clearer, we revised the aims, hypotheses and predictions paragraphs at lines 137-139, 145-147 and 154-162.

Line 162-163: Please state earlier that an experimenter was always present in the room in Experiment 1, such that it is clear from early on that this was the case.

Done. It is not at lines 134-135.

Methods

Please state early on in this section (in the Experimental Design and General Procedure) when the experimenter was or was not present in the room (in Experiment 1, Experiment 2 and pre-tests).

We stated this early on at lines 135-139, but also again 199-201 in the methods section.

Line 245 - Who was holding the dog while “she placed it on the marked spot in the experimental room”?

The owner. Added at line 218.

Lines 248-249 - Why this difference between conditions? Why didn’t the owner and the stranger entered together as well in the “owner condition”?

There was a reason only in the stranger condition for sending the owner into the room together with the stranger: had the owners stayed in the corridor from where the dog entered the room, the dogs would have likely hesitated to enter the room, thereby creating a difference between conditions (e.g. dogs showing less interest in the toys not because the owner was not in the room but because they stick to the door that separates them from the owner). There was no reason, however, to send the stranger into the room in the owner condition. On the contrary, this, unnecessarily, would have made the strangers more familiar for the dogs – an effect we wanted to avoid in the current experiment where two different persons played the role of the stranger in the two stranger conditions.

Line 259: “At the end of the trial” – The information on what determined the end of a trial should be presented already here (currently it is only presented later, on line 270)

Added at lines 228-229.

Line 260 – Please add to where the experimenter “left the testing room together with the dog” (hallway?)

Added at line 231-232.

The info on lines 271-280 should come in line 268 right after “first in presence and then in absence of their owner”.

We moved the information regarding each trial up. Now at lines 241-250.

Lines 406-408: I think the paper benefits if this info is presented earlier (see comment above).

The presence of the experimenter in the room in Experiment 1 but not in Experiment 2 is already mentioned at lines 135-139, 199-201, 374, 385-386, hence multiple times and earlier than this point.

Results

I think there are too many graphs/tables in this section. Please think reducing the number of figures – maybe create two big figures (one for Experiment 1 and one for Experiment 2) with several panels. Moreover, I would suggest moving the tables to supplementary material.

We combined figures as suggested. Now there are only two figures for Experiment 1 and one figure for Experiment 2. Moreover, we moved the Tables to the Supporting Information and uploaded them separately from the main manuscript in the S1 File.

Discussion

My only comment to this section is that I missed seeing the present results compared/contrasted with those from Previde and Valsecchi (2007) [6, 17], the only other published study comparing attachment in shelter vs ‘family’ dogs.

Thank you for this comment. We added that indeed our in line with that previous study. We added this information at lines 531-540.

Attachment

Submitted filename: response_to_reviewers.docx

Decision Letter 1

I Anna S Olsson

29 Nov 2021

PONE-D-21-22971R1Secure base effect in former shelter dogs and other family dogs: strangers do no provide security in a problem-solving taskPLOS ONE

Dear Dr. Cimarelli,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

The reviewer has provided detailed suggestions for how to make the writing more stringent, and as the editor I have a few additional comments on wording, all of which is presented below.

Please submit your revised manuscript by Jan 13 2022 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

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We look forward to receiving your revised manuscript.

Kind regards,

I Anna S Olsson, Ph.D.

Academic Editor

PLOS ONE

Journal Requirements:

Please review your reference list to ensure that it is complete and correct. If you have cited papers that have been retracted, please include the rationale for doing so in the manuscript text, or remove these references and replace them with relevant current references. Any changes to the reference list should be mentioned in the rebuttal letter that accompanies your revised manuscript. If you need to cite a retracted article, indicate the article’s retracted status in the References list and also include a citation and full reference for the retraction notice.

Additional Editor Comments:

Line 1 "do not" (the letter t is missing)

Line 31 "affects" (the letter s is missing)

Line 132 Replace "[26]'s" with the author name followed by [26]

Line 168 What are the GSP guidelines? I'm not familiar with them, and googling gave me a reference to a trade term.

Line 249 Start a new paragraph at "The dog passed the pre-test"

Line 315 The term "partner" has as far as I can see not been defined previously. I could deduce that it was the person present with the dog in the test situation, but I suggest you define the term here or in the methods section, where you introduce the social conditions around the set-up

Line 486 Replace "would have had an effect" with "had an effect"

Line 489 Replace "calls attention that" with "highlight that" or "calls attention to that"

Line 593 "teachers" (the letter s is missing)

[Note: HTML markup is below. Please do not edit.]

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #1: (No Response)

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Yes

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: I Don't Know

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

**********

6. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: I would like to thank the authors for the changes and clarifications provided and for the detailed responses to my comments. I think the manuscript has improved substantially. I would just like some minor issues to be addressed before I can say the paper is ready for being published. I detail my suggestions and questions in what follows.

Terms

The terms “constant family dogs” and “former shelter dogs” make the text too verbose sometimes. I understand why the authors choose these terms but, personally, for a matter of easiness of reading, I would use “family dogs” and “shelter dogs”. This is just a suggestion, and I am ok with the authors deciding to stick to the current terms.

Aims of study

I would suggest that the authors keep the presentation of the aims of the study more consistent throughout the paper. I do not mind, and actually think it is helpful for the reader, if a very similar wording (or even the same) is used.

In the end of the Introduction (lines 163-165), the authors state two aims:

- “to compare the secure base effect of owners to the social support strangers may provide dogs with”

- “to investigate how having lived in a shelter may influence stranger acceptance and bonding with the owner.”

Latter, in the beginning of the Discussion (lines 452-456), despite the authors stating the study had two main aims, I personally see three. Namely:

- “to investigate whether strangers could serve as a secure base for pet dogs”

- to investigate “to what extent they would do so less than owners would”

- “to examine whether the secure base effect provided by owners (and potentially by strangers) would differ between dogs with a past in the shelter and dogs who have always lived with the same owner.”

Line 122: I would suggested reorganizing to something like:

However, in the first study using this paradigm [26], some methodological limitations did not allow to fully compare to what extent owners and strangers could serve as a secure base for dogs. Specifically, while there was a condition in which the owner would be encouraging the dog, no corresponding condition existed for the stranger. Although results showed that dogs spent more time manipulating the object when the owner was encouraging them as compared to when the stranger was silent, and no differences were found between the silent owner and the silent stranger conditions, the possibility is still open that also an encouraging unfamiliar human could facilitate dogs’ manipulation, when compared to the owners.

Line 140-147: Here I would suggest stating which the hypothesis are for each Experiment. -- lines 140-144 refer to results to be obtained in Experiment 1 and lines 145-157 refer to results to be obtained in Experiment 2.

Line 148-162: This second part is still a bit confusing. As far as I understand, the authors are presenting three hypothesis, namely:

1. dogs might be very flexible and could be able to build new bonds easily, even when adults, resulting in no differences between constant family and former shelter dogs.

2. dogs’ re-homing past might have an effect on their social development and as such…

2.1. “Having lived in a shelter negatively affects the future development of a secure attachment bond or

2.1. “Having lived in a shelter increases the likelihood of accepting strangers as social partners

3. former shelter dogs might form a secure attachment bond with their owners comparable to the one formed by other family dogs, but be generally more anxious than constant family dogs

…but the way it is currently written does not leave it clear.

Still in Line 154: “In the first case, former shelter dogs would manipulate and explore less in the presence of the owner than other family dogs.” – what about Owner-Stranger differentiation? One would expect a less strong O-S differentiation, no?

Line 200 - I suggest introducing here the concept “coordinating experimenter” and using it every time from here on.

Line 202 - Why not referring here to the towel as well? Doesn’t this section refer to the Experimental Setup for both the pre-test and the test? Moreover, in the Materials section, the authors present the materials for both pre-test and test.

Line 218: Consider writing “held by the owner on a leash” instead of “held by the owner thanks to the leash”. Moreover, was the dog watching the coordinating experimenter from the hallway or inside the room?

Please clarify throughout the section Experimental Design and General Procedure when were the doors opened or closed. For example, in line 221 “The experimenter and the dog waited outside the testing room in the hallway” – was Door 1 opened or closed?

Line 280 - When the authors write “Similarly to the study by [26], “Manipulation” was coded whenever the dog was touching the toy with its muzzle or paw” it seems that it was just for this behavior and not the following ones. Please clarify if the remaining coded behaviors were also coded “similarly to [26]”.

Line 506-509: “It is difficult to tell whether former shelter dogs’ exploring to a similar extent in presence of the owner and of the stranger was due to lower stress when the owners were absent or more support when they were present.”

This idea is hard to follow. Maybe the problem is the fact that it is not clear whether these comparisons (“lower stress when the owners were absent” and “more support when they were present”) refers to a comparison between shelter dogs and family dogs or if it refers to a within-group comparison (i.e., owner-stranger comparison for shelter dogs). Namely, when the authors say that these dogs could be showing lower stress in the absence of the owner, does this mean lower as compared to what family dogs would show, or lower as compared to the other condition (owner present)?

It is also confusing because, as far as I understand, exploration in this paragraph seems to be interpreted both as a sign of distress and a sign of secure-base effect. In this same example, when the authors are trying to interpret the absence of differences in exploration in shelter dogs, it seems that the first hypothesis (lower stress when the owners were absent) is based on distress-related exploration and the second hypothesis (more support when they were present) is based on exploration related to a secure-base effect provided by the owner.

I truly feel this section needs clarification.

Typos:

Abstract line 31: remove “s” in “affects”.

Line 350: I believe the authors mean “Experiment 1”

Line 453: I suggest removing the “would” at the end of the sentence

**********

7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: Yes: Ana Catarina Vieira de Castro

[NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files.]

While revising your submission, please upload your figure files to the Preflight Analysis and Conversion Engine (PACE) digital diagnostic tool, https://pacev2.apexcovantage.com/. PACE helps ensure that figures meet PLOS requirements. To use PACE, you must first register as a user. Registration is free. Then, login and navigate to the UPLOAD tab, where you will find detailed instructions on how to use the tool. If you encounter any issues or have any questions when using PACE, please email PLOS at figures@plos.org. Please note that Supporting Information files do not need this step.

PLoS One. 2021 Dec 22;16(12):e0261790. doi: 10.1371/journal.pone.0261790.r004

Author response to Decision Letter 1


2 Dec 2021

Response to reviewers - PLOS ONE manuscript [PONE-D-21-22971R1]

Dear Editor,

Please find below the answers to each of your and the reviewers’ points. Our answers are reported in bold below each point.

Thank you very much for your work and valuable contribution to improve the present manuscript.

Kind regards,

Giulia Cimarelli, PhD

Additional Editor Comments:

Line 1 "do not" (the letter t is missing)

Corrected.

Line 31 "affects" (the letter s is missing)

Corrected.

Line 132 Replace "[26]'s" with the author name followed by [26]

Corrected.

Line 168 What are the GSP guidelines? I'm not familiar with them, and googling gave me a reference to a trade term.

Good Scientific Practice. We corrected it.

Line 249 Start a new paragraph at "The dog passed the pre-test"

Done.

Line 315 The term "partner" has as far as I can see not been defined previously. I could deduce that it was the person present with the dog in the test situation, but I suggest you define the term here or in the methods section, where you introduce the social conditions around the set-up

Added at line 273 and 289.

Line 486 Replace "would have had an effect" with "had an effect"

Corrected.

Line 489 Replace "calls attention that" with "highlight that" or "calls attention to that"

Corrected.

Line 593 "teachers" (the letter s is missing)

Corrected.

Comments to the Author

6. Review Comments to the Author

Reviewer #1: I would like to thank the authors for the changes and clarifications provided and for the detailed responses to my comments. I think the manuscript has improved substantially. I would just like some minor issues to be addressed before I can say the paper is ready for being published. I detail my suggestions and questions in what follows.

Terms

The terms “constant family dogs” and “former shelter dogs” make the text too verbose sometimes. I understand why the authors choose these terms but, personally, for a matter of easiness of reading, I would use “family dogs” and “shelter dogs”. This is just a suggestion, and I am ok with the authors deciding to stick to the current terms.

Thank you for your suggestion, we thought about it but we don’t want to confuse the reader: by simply mentioning shelter and family dogs, the risk is that the reader will interpret shelter dogs as still being host in the a shelter, while all dogs in our sample are indeed family dogs, but one group has a past in a shelter. We would like to stick with the terminology used so far, even if a but verbose.

Aims of study

I would suggest that the authors keep the presentation of the aims of the study more consistent throughout the paper. I do not mind, and actually think it is helpful for the reader, if a very similar wording (or even the same) is used.

In the end of the Introduction (lines 163-165), the authors state two aims:

- “to compare the secure base effect of owners to the social support strangers may provide dogs with”

- “to investigate how having lived in a shelter may influence stranger acceptance and bonding with the owner.”

Latter, in the beginning of the Discussion (lines 452-456), despite the authors stating the study had two main aims, I personally see three. Namely:

- “to investigate whether strangers could serve as a secure base for pet dogs”

- to investigate “to what extent they would do so less than owners would”

- “to examine whether the secure base effect provided by owners (and potentially by strangers) would differ between dogs with a past in the shelter and dogs who have always lived with the same owner.”

Thank you. We modified the end of the Introduction (Lines 165-168) to more clearly state the 3 aims of the study and be more in line with the rest of the manuscript, as the reviewer suggested: “Overall, the present study allows us to test whether strangers could serve as a secure base for pet dogs and to compare the secure base effect of strangers to the one provided by owners. Moreover, the present study aims at investigating how having lived in a shelter may influence stranger acceptance and bonding with the owner.” Moreover, we changed that the study aims are three and not two as previously stated at line 464.

Line 122: I would suggested reorganizing to something like:

However, in the first study using this paradigm [26], some methodological limitations did not allow to fully compare to what extent owners and strangers could serve as a secure base for dogs. Specifically, while there was a condition in which the owner would be encouraging the dog, no corresponding condition existed for the stranger. Although results showed that dogs spent more time manipulating the object when the owner was encouraging them as compared to when the stranger was silent, and no differences were found between the silent owner and the silent stranger conditions, the possibility is still open that also an encouraging unfamiliar human could facilitate dogs’ manipulation, when compared to the owners.

Thank you! Indeed the structure of the paragraph is simpler and clearer. We modified as the reviewer suggested.

Line 140-147: Here I would suggest stating which the hypothesis are for each Experiment. -- lines 140-144 refer to results to be obtained in Experiment 1 and lines 145-157 refer to results to be obtained in Experiment 2.

Yes, we added in brackets to what experiment each prediction is referred to (Lines 146 and 149).

Line 148-162: This second part is still a bit confusing. As far as I understand, the authors are presenting three hypothesis, namely:

1. dogs might be very flexible and could be able to build new bonds easily, even when adults, resulting in no differences between constant family and former shelter dogs.

2. dogs’ re-homing past might have an effect on their social development and as such…

2.1. “Having lived in a shelter negatively affects the future development of a secure attachment bond or

2.1. “Having lived in a shelter increases the likelihood of accepting strangers as social partners

3. former shelter dogs might form a secure attachment bond with their owners comparable to the one formed by other family dogs, but be generally more anxious than constant family dogs

…but the way it is currently written does not leave it clear.

Thank you. We corrected that indeed the hypotheses are 3 (Line151) and we added list item letters for the in-sentence list. This should make the structuring clearer (paragraph at lines 150-164).

Still in Line 154: “In the first case, former shelter dogs would manipulate and explore less in the presence of the owner than other family dogs.” – what about Owner-Stranger differentiation? One would expect a less strong O-S differentiation, no?

Yes, we added “and a less strong owner-stranger differentiation”.

Line 200 - I suggest introducing here the concept “coordinating experimenter” and using it every time from here on.

Thanks for you suggestion, we added it and used it throughout the text.

Line 202 - Why not referring here to the towel as well? Doesn’t this section refer to the Experimental Setup for both the pre-test and the test? Moreover, in the Materials section, the authors present the materials for both pre-test and test.

Yes, we added it at line 206.

Line 218: Consider writing “held by the owner on a leash” instead of “held by the owner thanks to the leash”.

Corrected.

Moreover, was the dog watching the coordinating experimenter from the hallway or inside the room?

From the hallway, we added it at line 223.

Please clarify throughout the section Experimental Design and General Procedure when were the doors opened or closed. For example, in line 221 “The experimenter and the dog waited outside the testing room in the hallway” – was Door 1 opened or closed?

Closed. We added details regarding whether the door was open or closed throughout the whole section.

Line 280 - When the authors write “Similarly to the study by [26], “Manipulation” was coded whenever the dog was touching the toy with its muzzle or paw” it seems that it was just for this behavior and not the following ones. Please clarify if the remaining coded behaviors were also coded “similarly to [26]”.

All behaviours were coded following [26]. We specified this at line 291 and we used semicolons instead of colons to list the different variables.

Line 506-509: “It is difficult to tell whether former shelter dogs’ exploring to a similar extent in presence of the owner and of the stranger was due to lower stress when the owners were absent or more support when they were present.”

This idea is hard to follow. Maybe the problem is the fact that it is not clear whether these comparisons (“lower stress when the owners were absent” and “more support when they were present”) refers to a comparison between shelter dogs and family dogs or if it refers to a within-group comparison (i.e., owner-stranger comparison for shelter dogs). Namely, when the authors say that these dogs could be showing lower stress in the absence of the owner, does this mean lower as compared to what family dogs would show, or lower as compared to the other condition (owner present)? It is also confusing because, as far as I understand, exploration in this paragraph seems to be interpreted both as a sign of distress and a sign of secure-base effect. In this same example, when the authors are trying to interpret the absence of differences in exploration in shelter dogs, it seems that the first hypothesis (lower stress when the owners were absent) is based on distress-related exploration and the second hypothesis (more support when they were present) is based on exploration related to a secure-base effect provided by the owner.

I truly feel this section needs clarification.

Only within the former shelter group. And yes, exploration could be either a sign of distress or of a secure base effect. We modified the sentence to make this clearer “If exploration was a sign of distress also in the case of former shelter dogs, then a similar duration of exploration in the presence of the owner and of the stranger might be either due to low stress when the owner is absent (stranger condition) or to received support when the owner is present (owner condition).” We additionally simplified the rest of the paragraph (lines 515-527).

Typos:

Abstract line 31: remove “s” in “affects”.

Corrected.

Line 350: I believe the authors mean “Experiment 1”

Corrected.

Line 453: I suggest removing the “would” at the end of the sentence

Corrected.

Attachment

Submitted filename: response_to_reviewers_02122021.docx

Decision Letter 2

I Anna S Olsson

10 Dec 2021

Secure base effect in former shelter dogs and other family dogs: strangers do not provide security in a problem-solving task

PONE-D-21-22971R2

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Acceptance letter

I Anna S Olsson

13 Dec 2021

PONE-D-21-22971R2

Secure base effect in former shelter dogs and other family dogs: strangers do not provide security in a problem-solving task

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