Subjects

The subjects were 39 (24 male, 15 female; 33 spayed or neutered) household dogs living in the Twin Cities area in Minnesota that were volunteered by their owners. Two dogs (non-therapy dogs) were excluded from analyses because they showed signs of aggression during baseline monitoring, and were thus considered too dangerous to be included further in the experiment. One dog was excluded because it was deaf (therapy dog), and thus was not subjected to the auditory component of the experimental manipulation. One dog in the distress condition was excluded because the owner chose to end the trial before the five-minute trial length had been completed due to the dog’s distress (therapy dog). Finally, one dog in the control condition was excluded because its owner did not follow instructions and encouraged the dog to open the door, which led to opening (non-therapy dog). This left 34 dogs (21 male, 13 female; 29 spayed or neutered). The dogs were adults (M = 6.71 years old, SD = 2.62), ranging from 1.5 to 12 years old. By weight, they ranged from 8 to 160 lbs (M = 45.57 lbs, SD = 29.84). There were a variety of breeds, although the most common types of dog were mixed breeds (n = 13) followed by golden retrievers (n = 3; see Table 1 for all breeds by condition). Nearly half of the dogs (n = 16) were nationally-certified therapy dogs (n = 6 Therapy Dog International; n = 9 Pet Partners, n=1 certification type not reported), while the other dogs (n = 18) were non-therapy pet dogs. There were no differences between conditions (distress or control) with regard to age or weight, all ts < 1.2, all ps > 0.24, or sex, χ2(1, N = 34) = 0.13, p = 0.72. There were also 34 human participants (32 female, 2 male), the owners that accompanied the dogs during the experiment. The human participants ranged from 19 to 75 years old, with a mean age of 49.56 years old (SD = 12.23). Subjects were recruited by word of mouth or from an ad in a daily college-wide email newsletter. All methods were approved by both the Institutional Animal Care and Use Committee and the Institutional Review Board at Macalester College.

Table 1 Breeds by condition Full size table

Apparatus and materials

A behavioral and demographic survey was used to obtain information about the owner’s age, gender, and dog-owning history, and the dog’s age, sex, breed, health history, and training. They also completed the C-BARQ behavioral questionnaire to measure general behavioral history of aggression and anxiety (Hsu & Serpell, 2003).

A Polar H7 Heart Rate Monitor was used to record the dog’s HRV (Polar Electro, Kempele, Finland). The data from the monitor were transmitted via Bluetooth to an iPhone app (Heart Rate Variability Logger, Marco Altini). The HRV data were analyzed using ARTiiFACT software (Kaufmann et al., 2011).

The testing arena was a rectangular room with a small square room adjacent to the main chamber (see Fig. 1). There was a chair in the square room and a small door separating the small room from the main one. The door (96.5 cm wide × 122 cm tall × 2.54 cm thick) was made of gray-painted wood with a sheet of clear Plexiglas (55.9 cm × 106.7 cm) spanning the interior of the door to make a window. This door was attached to the door frame by three magnets positioned vertically along the hinged side of the door. The other side of the door was loosely connected to the other side of the door frame with three weak magnets positioned vertically, such that contact by a dog’s nose or paw allowed the door to easily swing open into the small room. Pilot trials of dogs not taking part in the study indicated that dogs of varying sizes could easily open the door.

Fig. 1 Schematic representation of the testing arena for the prosocial helping task Full size image

The impossible task was performed in a small room that was across the hall from the prosocial task testing space. The apparatus was a piece of wood (60.96 cm × 53.3 cm × 0.6 cm) covered in white fleece to prevent splinter injuries. The wood had Velcro on the edges of its bottom side that allowed it to be securely attached to the carpeted floor of the room. At the center of the wood plank on the top side, the lid of a glass jar was glued upside-down, such that the jar could be screwed upside-down into its lid and be rendered immovable. This allowed food to be placed onto the lid with the jar screwed over it, such that it was visible but unreachable.

Prosocial helping task

Owners were instructed to restrict their dog’s access to food for four hours prior to testing to ensure consistency and motivation in the impossible task (D’Aniello et al., 2015). Dogs and owners were taken to a small classroom where a heart rate monitor was placed on the dog. Veterinary lubricant was applied to the monitor to enable conductivity before it was placed just left of center on the dog’s chest, and was held by a band that was wrapped snugly around the dog’s rib cage to hold it in place. The connection between the monitor and the app was established, and a 10-min period of baseline heart rate data were collected while the owner completed the behavioral survey in the same room. Once the baseline heart rate data had been recorded, the owner went with one of the experimenters into the testing arena and was instructed on their role in the prosocial helping task while a second experimenter calmly held the dog’s leash. After approximately 2 min of instructions to the owner, the prosocial task began.

The procedure is a modified protocol of trapped-other rat experiments (Ben-Ami Bartal et al., 2011). The dog’s owner was seated in the chair in the small square room, and the small door was closed such that they were separated from the main chamber by the door. Dogs were assigned to either the distress or control condition, and only participated in that one condition. This assignment was done by categorizing each dog into one of four groups based on size (small or large to ensure that group differences were not based on physical ability to open the door) and whether the dog was a therapy dog or not. In each of these categories, condition assignment alternated, such that within each of the four groups there were an approximately equal number of dogs assigned to each condition. Each owner received instructions on what vocalizations to make based on their condition assignment. In the control condition, the owner said “Help” in a control tone every 15 s, and hummed “Twinkle Twinkle Little Star” between each vocalization. In the distress condition, the owner said “Help” in a distressed tone at 15-s intervals at approximately the same volume as in the control condition, and made crying sounds between each vocalization. In both conditions, the owner hid their hands from their dogs by placing them under their legs to prevent unintended communication with hand gestures, and maintained their gaze slightly above the dog’s eye level to decrease variation in the amount of eye contact between conditions.

To begin the trial, the dog was brought into the room and positioned at the opposite end of the room from their owner and facing toward their owner. The experimenter released the dog’s leash and left the room, at which point the trial started. The trial ended if the dog touched the door and detached its magnets from the door frame, thus opening the door. In trials where the dog did not open the door, the experiment was terminated after 5 min. Each dog was allowed to reunite with their owner for a short period of time following the prosocial helping trial, regardless of whether they opened the door. Each trial was video recorded, and the videos were used to calculate opening rate and coded for distress behaviors.

Impossible task

Following the prosocial helping task, the dog’s owner left the room with an experimenter and proceeded to the next stage of the experiment while another experimenter stayed with the dog. In the impossible task (Marshall-Pescini et al., 2008), the dog’s owner and a stranger each stood on one side behind the testing apparatus, which was positioned in the middle of the room on the floor. The side of the apparatus (left or right) that the owner stood on was counterbalanced across subjects. The owner and stranger both stared diagonally across the room and remained still throughout the experiment. Once the room was set up, the dog was brought in and held in the back of the room by an experimenter, approximately 0.5 m away from the testing apparatus, such that the dog could see the apparatus and the two people standing behind it.

The main experimenter started by giving the dog a treat to show them that there was an opportunity for food. Then, a treat was placed on the lid at the center of the wood plank, and the dog was released to go get the food. After it had eaten the treat, the dog was retrieved and brought back to its starting position. For the next three treats, the food was placed onto the lid of the jar, and the jar was placed gently on top of the lid such that it could be easily tipped over to retrieve the food underneath. The dog was released to retrieve each piece of food, and if it did not knock over the jar rapidly, the experimenter encouraged the dog to move the jar in order to retrieve the food. Most dogs required at least one trial of encouragement. No dog was allowed to progress to the final trial until it had moved the jar to get to the food underneath three times; this ensured that dogs had started to acquire a jar-moving behavior in order to receive a food reward. In the final trial, the food was placed on the lid and the jar was screwed into place over it. The set-up looked identical to the previous trials but this time the jar could not be moved even if the dog applied force to it. Once the jar was put in place, the dog was released and the two experimenters exited the room, such that the dog was alone in the room with their owner and the stranger. The trial lasted 60 s, during which time videos were recorded for later analyses of gaze direction. After the trial period had passed, the experimenters re-entered the room and removed the jar so that the dog could eat the treat underneath. The heart rate monitor was then removed from the dog, and the owner was debriefed about the purpose of the experiment.

Behavioral ethogram

Dogs were videotaped for the duration of the baseline heart rate recording, and the prosocial helping and impossible task rooms were each videotaped from two different angles. In the prosocial helping room, one angle captured the dog’s face when they were facing the door and looking at their owner, and the other captured their movement through the experimental room. The video cameras could not be set up to capture the entire experimental arena, so the amount of time that the dog was visible in the video was also recorded for each trial. Because evaluation of vocalizations required auditory cues from the video, the video coder for the prosocial task was not able to be blind to condition (since the owner’s vocalizations were also audible on the video) nor opening (since the length of the video indicated whether the dog opened or not, as all dogs that did not open had 300-s videos while openers had shorter videos). Experimenters blind to the condition and opening status completed the ethogram for the baseline stress and impossible task behavioral coding. In the impossible task, one camera faced the owner and stranger from the front, and the other was set up to record a side view of the experimental room. Videos of the impossible task were coded to compare gazes toward the owner and stranger as well as task-oriented behaviors such as digging at or attempting to move the jar to get to the food underneath.

Behavioral coding was used to quantify dogs’ distress during the baseline and experimental portions of the study. An ethogram was used to code videos for behavioral measures of stress during baseline and testing. Eight variables were recorded: vocalizing (barking or whining that was audible on the video, duration), panting (duration), sniffing the floor (duration), urogenital checkout (sniffing or licking, count), shaking off (count), yawning (count), scratching oneself (count), and flicking the tongue (count) which are all considered typical stress behaviors in dogs (as reviewed by Mariti et al., 2012). The individual totals of stress behaviors (count and duration) were summed to yield a total stress score for each dog. Approximately 25% of videos for behavioral coding for stress and the impossible task were re-coded by a blind coder. In cases, where major discrepancies appeared, coders sat down to reexamine the video to determine where the discrepancies were and came to a joint conclusion. Inter-rater correlations for total stress behaviors during baseline, r(9) = 0.88, p = 0.002, prosocial task, r(10) = 0.98, p < 0.001, for the percentage of gaze at the owner r(10) = 0.92, p < 0.001, were all very high.

Data processing

The C-Barq survey reports averages of scores on several questions to form categories (e.g., owner-directed aggression, stranger-directed fear, etc.). We created a further category for general anxiety. We summed the subcategories of fear of dogs, fear of strangers, non-social fear, touch sensitivity, and separation-related problems under this anxiety measure.

In order to ensure that trial length and differences in visibility in the videos did not confound the behavioral distress measure, stress scores from the ethograms were divided by the total amount of time, in seconds, that the dog was visible in the video to yield a score of stress per second for each dog. The baseline behavioral recording period was 10 min for every dog except for four, for which the videos were truncated due to equipment failure or experimenter error, whereas the testing behavioral recording period was equivalent to the length of the trial (either the latency to opening, or 300 s for dogs that did not open). One dog was excluded from analyses on baseline stress behaviors because their video did not save, and thus stress behaviors could not be analyzed. Videos of the impossible task were coded for the amount of time that the dog spent gazing either at the owner or stranger, or performing task-oriented behaviors. The percentage of gaze directed at the owner was calculated by dividing the amount of time spent gazing at the owner over the total amount of time the dog spent gazing at either the owner or the stranger.

There were four dogs that were excluded from heart rate analyses because a reliable connection was not able to be established during baseline, or because the reading dropped during the prosocial helping task. Analyses on HRV were performed on a total of 30 dogs (14 in the distress condition, 16 in the control condition). All heart rate data were analyzed using Artiifact (Kaufmann et al., 2011). For the baseline sampling, only the most consistent five-minute section of the file was used in analyses. If the entire file was consistent, 180–480 s were used. For the trial phase, the entire file was used unless there was enough inconsistency in a section to deem it unusable, in which case as much of the file as possible was selected. All inter-beat interval data points above 2,000 ms were classified as artefacts and were removed from the sample through cubic spline interpolation prior to analyses using ARTiiFACT software (Craig, Meyers-Manor, Anders, Sütterlin, & Miller, 2017). The VLF band was set at 0.06 Hz, the LF band was set at 0.24 Hz, and the HF band was set at 1.06 Hz, which have been found to be typical for canine heart rate measures (Houle & Billman, 1999). Although the software produces a variety of other HRV measures, including mean HR, SDNN, RMSDD, NN50, VLF, LF, HF, and LF/HF ratio, pNN50 was used to quantify HRV in analyses because it is less sensitive to sample length than the other measures and has been used as a good measure of HRV in dogs (Craig et al., 2017). pNN50 is a measure of the percentage of successive RR intervals that differ from each other by more than 50 ms, and thus a high pNN50 corresponds to high HRV.