Author's personal copy Anim Cogn DOI 10.1007/s10071-015-0934-5
ORIGINAL PAPER
Does affective information influence domestic dogs’ (Canis lupus familiaris) point-following behavior? Ross Flom1 • Peggy Gartman1
Received: 29 June 2015 / Revised: 13 October 2015 / Accepted: 22 October 2015 Ó Springer-Verlag Berlin Heidelberg 2015
Abstract Several studies have examined dogs’ (Canis lupus familiaris) comprehension and use of human communicative cues. Relatively few studies have, however, examined the effects of human affective behavior (i.e., facial and vocal expressions) on dogs’ exploratory and point-following behavior. In two experiments, we examined dogs’ frequency of following an adult’s pointing gesture in locating a hidden reward or treat when it occurred silently, or when it was paired with a positive or negative facial and vocal affective expression. Like prior studies, the current results demonstrate that dogs reliably follow human pointing cues. Unlike prior studies, the current results also demonstrate that the addition of a positive affective facial and vocal expression, when paired with a pointing gesture, did not reliably increase dogs’ frequency of locating a hidden piece of food compared to pointing alone. In addition, and within the negative facial and vocal affect conditions of Experiment 1 and 2, dogs were delayed in their exploration, or approach, toward a baited or sham-baited bowl. However, in Experiment 2, dogs continued to follow an adult’s pointing gesture, even when paired with a negative expression, as long as the attention-directing gesture referenced a baited bowl. Together these results suggest that the addition of affective information does not significantly increase or decrease dogs’ point-following behavior. Rather these results demonstrate that the presence or absence of affective expressions influences a dogs’ exploratory behavior and the
& Ross Flom
[email protected] 1
Department of Psychology, Brigham Young University, Provo, UT 84602, USA
presence or absence of reward affects whether they will follow an unfamiliar adult’s attention-directing gesture. Keywords Emotional expressions Point following Object choice Domestic dogs Social referencing
Introduction Communication is essential for the survival of nearly all species. Communication promotes the obtainment of resources, the avoidance of predation, and in higher order mammals promotes social and cognitive development. Human infants, for example, are communicative from birth, and the sharing of affect between an adult and newborn represents the earliest form of human communication (Fridlund 1994; Gibson and Pick 2003). Domestic dogs (Canis lupus familiaris), through processes of domestication and convergent evolution, are adept at using a number of human communicative gestures (e.g., pointing and direction of gaze) in locating a piece of food or a novel object and typically do so with little to no training (see Kaminski et al. 2012; Lakatos et al. 2009, 2012; Miklo´si et al. 1998; Udell et al. 2008 for examples of canine sensitivity to human pointing). Given that emotion or affect is ubiquitous to human communication, and represents the first form of adult–infant communication, coupled with the fact that domestic dogs are sensitive to, and can use, a variety of human communicative behaviors, it is logical to examine whether and how dogs respond to human emotional and communicative cues. The purpose of the current study is to examine the effects of an adult’s positive and negative facial and vocal expressions on domestic dogs’ point-following behavior in locating a hidden reward or treat.
123
Author's personal copy Anim Cogn
Just as dogs are sensitive to and follow a variety of pointing gestures, not surprisingly dogs are also sensitive to and discriminate a variety of human facial expressions. Specifically, Nagasawa et al. (2011) examined and found evidence demonstrating that dogs discriminate their owner’s face from a stranger’s face and that dogs also discriminate their owner’s smiling face from their owner’s expressionless face. While dogs discriminate human faces, it has also been shown that they discriminate between their owner’s happy and sad facial expressions (Morisaki et al. 2009) and respond differently to human’s positive and negative affective behaviors (Merola et al. 2012a, b). Together, it is clear that dogs are adept at discriminating faces and that they show a preference for a positive expression (smiling) over an expressionless face. More recently, and germane to the current study, research has begun to examine whether dogs comprehend a human’s affective expression as referential and whether dogs engage in social referencing. Using a modified social referencing procedure (e.g., Walden and Ogan 1988), Merola et al. (2012a) examined whether domestic dogs referentially look to their owner and whether the owner’s affective facial–vocal expression affects the dog’s exploratory behavior. In this experiment, dogs were presented with a small operating fan with streamers attached (a neutral and ambiguous object) as the owner communicated a positive or negative affective facial–vocal expression toward the fan. Their results revealed that the majority of the dogs (83 %) alternated their direction of gaze between their owner and the fan and thus showed evidence of referential communication. Their results also revealed a somewhat attenuated pattern of behavioral regulation, i.e., social referencing, when provided with positive or negative affective facial and vocal cues. Specifically, those dogs exposed to their owner’s negative affect showed reduced rates of locomotion (behavioral freezing) when the owner approached and touched the fan. In addition, and unlike experiments with humans, when dogs were provided with positive affective expressions they did not increase their frequency of exploration (Merola et al. 2012a). More broadly, the results of Merola et al. (2012a) are important, as they are among the first to show that when confronted with a novel object dogs seek information from their owner about that object, i.e., referential communication. The results of Merola et al. (2012a), however, do not unequivocally demonstrate that dogs use their owner’s affective cues in guiding their exploratory behavior, i.e., social referencing. A more recent experiment further examined whether domestic dogs use an adult’s affective expression in a referential manner in exploring one of the two boxes (Buttelmann and Tomasello 2013).
123
Buttelmann and Tomasello (2013) examined whether (1) dogs comprehend an unfamiliar adult’s emotional expression as directed toward an unseen object and (2) whether the emotional expression affects dogs’ choice of a box. In one condition, an adult opened a box containing a piece of sausage and while looking inside conveyed a happy facial and vocal expression and then looked into another box containing wood shavings and conveyed a neutral expression (happy–neutral condition). In a second condition, the adult looked into a box containing a piece of sausage and again conveyed a happy facial and vocal expression and then looking into another box containing a piece of garlic and conveyed a disgusted facial and vocal expression (happy–disgust condition). The results of Buttelmann and Tomasello (2013) showed that dogs performed at chance in the happy–neutral condition by choosing each box with roughly equal frequencies. In the happy–disgust condition, however, dogs reliably chose the box paired with the happy expression. In the happy–disgust condition, it is difficult to discern whether dogs approached one box because it was paired with the positive affect or if they approached it because they avoided the bowl paired with the negative affect. Finally, and as noted by Buttelmann and Tomasello (2013, p. 142), while dogs did use emotional expressions to find hidden food, their results may have been attenuated within the happy–neutral condition because dogs may have difficulty in discriminating between the happy and neutral expressions. Taken together, the results of Buttelmann and Tomasello (2013), and those of Merola et al. (2012a), demonstrate that dogs do use their owner’s, or a stranger’s, affective expression in a referential manner and also provide some evidence that the adult’s affective expression affected dogs’ exploratory behavior (i.e., social referencing). Expanding upon the results of Buttelmann and Tomasello (2013), Merola et al. (2014) further examined dogs’ understanding of human affective expressions as referential. In this experiment, Merola et al. (2014) compared dogs’ frequency of exploring an unfamiliar, and affectively ambiguous, infant toy hidden behind a barrier when either the dog’s owner or a stranger communicated the affective expression toward the toy. In addition, and like Buttelmann and Tomasello (2013), Merola et al. (2014) compared dogs’ exploratory behavior when the dog was provided a positive–negative affective pairing (positive affect directed toward one location and negative affect directed toward the other location), or a positive–neutral affective pairing, however, and unlike Buttelmann and Tomasello (2013), dogs in Merola et al. (2014) were also provided a negative–neutral pairing. Results of Merola et al. (2014) revealed that within the positive–negative affective condition, and when the owner, but not a stranger, provided positive affective information, dogs
Author's personal copy Anim Cogn
reliably explored the novel toy hidden behind the barrier. In the positive–neutral affective condition, dogs also searched behind the barrier for the toy when the owner communicated the positive affect. However, in the negative–neutral condition, when the owner communicated the negative affective expression, dogs did not reliably search behind the barrier associated with the neutral affective expression. Together, these studies provide converging evidence that dogs will explore an unfamiliar object when one object is associated with a positive expression and the other object is associated with a negative affective expression and the affective information is conveyed by their owner (Merola et al. 2014) or a stranger (Buttelmann and Tomasello 2013). However, dogs will only approach an unfamiliar object when it is paired with positive affective information and the other object is paired with neutral affective information and the owner conveys the affective information. Thus, dogs do use another’s emotional expression in a referential manner and dogs do, in a limited way, use another’s affective expression in guiding their exploratory behavior. Current experiment The current experiment examines the question of how an unfamiliar adult’s affective behavior, when paired with a pointing gesture, influences canines’ point-following behavior. Previous studies have demonstrated dogs reliably follow a human’s pointing gestures and that an adult’s affective expressions influence dogs’ exploratory behavior; however, it is not known whether, or how, an adult’s affective behavior influences dogs’ point-following behavior. In Buttelmann and Tomasello (2013) and Merola et al. (2012a, 2014), the adult’s affective gesture was paired with the adult’s head and eye orientation, but not pointing, in reference to a box, fan, or object located behind a barrier. Moreover, when adults typically communicate with dogs, they often pair affective information with various communicative gestures—including pointing. Thus in two experiments we examined the effects of an unfamiliar adult’s positive and negative affective expressions, while paired a pointing gesture, on dogs’ point-following behavior. Similar to prior studies, dogs in the current study were provided with a two-alternative choice task (e.g., Buttelmann and Tomasello 2013; Hare et al. 2002; Soproni et al. 2002) where an experimenter either looked and pointed silently, looked and pointed while conveying a positive or happy affective facial and vocal expression, or looked and pointed while conveying a negative or disgusted affective expression toward one of the two bowls. Finally, and unlike other studies (e.g., Buttelmann and Tomasello 2013; Merola et al. 2014), only one object or location, rather than both locations or objects, was referenced.
Experiment 1: effects of affect on canine point following Methods Participants Forty-five domestic dogs (Canis lupus familiaris) of various breeds participated and were included in the analyses. Dogs were recruited from fliers placed at pet stores and local veterinary clinics. While some dogs had received obedience training, no dog had participated in more specialized training (i.e., search and rescue, hunting/retrieving). Dogs were randomly assigned to each of the three conditions (N = 15 silent, N = 16 positive, and N = 14 negative condition). ‘‘Appendix’’ lists the number of dogs by breed. Twenty-three dogs were female. Dogs were between 1 and 11 years of age (M = 5.4 years, SD = 2.5 years). All dogs lived in homes with their owners and were considered pets. Dogs were required to pass a series of warm-up trials described below and were further required to complete 10 of the 12 experimental trials. No dog was excluded for failure to complete the warm-up trials. Eight additional dogs, however, were tested, and their data were excluded. Six dogs were excluded as they became distracted during testing (N = 3 for failure to sit and allow an experimenter to hold the dog by a short leash or collar, N = 2 for failure to look to the experimenter providing the cue, and N = 1 for becoming upset by the departure of their owner). Two dogs were tested and were excluded as they displayed a side bias as they went to the left side of the testing room and not toward a bowl on all experimental trials (see Wells 2003 for a discussion of side bias in dogs). Stimuli and apparatus The experiment was conducted in a 4 9 9 m enclosure that was surrounded by a 2-m-high opaque partition (see Fig. 1). Two stainless steel food containers, approximately 10 cm in diameter and 6 cm deep, were used. The owners were given a choice of 2–3 possible dog treats that were used in baiting and scent marking the bowls. Owners were allowed to pick their dog’s treat in order to decrease the likelihood of any difference in behavior/responding being due to a dog not liking a specific treat. The target dish was baited with a 1oz dog treat for each trial. Prior to beginning the warm-up trials, each bowl was scent marked with the preferred dog treat by crushing and then smearing the dog treat on the inner sides and bottom of each bowl. Scent marking was done for each dog and was done to reduce the possibility of dogs using olfaction in locating the treat during warm-up or experimental phase.
123
Author's personal copy Anim Cogn
of a female adult actress conveying a positive–happy and a negative–disgusted affective expression. The video clips were used and validated with humans in similar experiment (Flom and Bahrick 2007) and were consistent with Ekman and Friesen’s (1975) characterizations of affective expressions as conveyed in facial expressions. After watching each clip 3–4 times, each experimenter then practiced conveying each expression until they felt comfortable in terms of how they conveyed the affective expressions and the pointing gesture. Positive affective expressions consisted of saying, ‘‘Oh wow, that’s great’’ in a higher and more varied pitch, raised eyebrows, wider mouth and eye opening, and a smiling facial expression. Negative vocal expressions consisted of saying ‘‘Oh wow, that’s awful’’ in a lowered and less varied pitch, lowered eyebrows, squinted eyes, and downward turned corners of the mouth. Procedure Each dog participated in four warm-up trials and 12 experimental trials. In order to increase the likelihood that the dogs were motivated to perform the food choice task, only those dogs that had not eaten within the past 4 h and ‘‘passed’’ all four warm-up trials were included. Warm-up phase Fig. 1 Layout of testing area
A handheld stopwatch was used in recording dogs’ latency to begin exploration. Tape markings on the floor were used to mark the location of the bowls and the chairs. A strip of tape positioned .5 m in front of the experimenter’s chair who held each dog was used to code dogs’ latency to begin exploration. Each session was videorecorded using a Canon Vixia HF R21 HD video camera, and recorded events were used in subsequent coding. Experimenters Four different experimenters (two females and two males) were used. One experimenter provided the affective (facial and vocal) cues and pointing gesture to the dog. A second experimenter held the dog by the collar or short leash and recorded the dog’s latency to begin exploration. A third experimenter baited/sham baited the bowls. The fourth experimenter waited with the owner. Each of the four experimenters rotated through the four different roles/positions. Experimenters were randomly assigned to each task/role with the constraint that each experimenter performed each task/role with roughly similar frequencies within each condition described below. Experimenters were trained how to convey the affective expression (happy and disgust) by watching a 30-s video clip
123
In the current study, experimenters looked and pointed toward a baited bowl during the warm-up phase, whereas other studies often do not include pointing within the warm-up phase. We included pointing during the warm-up phase because we are particularly interested in the effects of adult’s communicated affective expression on dogs’ point-following behavior in locating a hidden treat. If pointing was not included within the warm-up phase, and dogs did not reliably follow or search for a hidden reward during the experimental phase, it would be ambiguous as to whether the results were due to the affective expression or because the dogs failed to follow the adult’s pointing gesture. Thus, pointing was included during the warm-up phase to acclimate the dog to the task and testing environment, including the unfamiliar experimenter, and to examine whether each dog reliably followed the experimenter’s pointing gesture. Each dog was positioned/seated approximately 2.5 m equidistant from the two bowls, and the bowls were placed 2 m apart. The experimenter providing the cue sat on a stool, centered equidistance between the two bowls. During each trial, the second experimenter held the dog by the collar and the third experimenter placed a 1oz portion of a treat into one bowl in full view of the dog. The other bowl, while scent marked, remained empty and was not sham baited during the warm-up trials.
Author's personal copy Anim Cogn
Following baiting and the departure of the third experimenter, the first experimenter (the cuer) called the dog by name and made sure the dog was looking at him or her. Once the dog had established eye contact, the cuer silently looked and pointed using their outstretched arm and index finger toward the baited bowl for 5 s. After the cuer ceased gesturing, the experimenter holding the dog then released the dog. The procedure was then repeated for the bowl on the opposite side. After successfully completing the two ‘‘open-bowl’’ warm-up trials, the third experimenter again baited one of the two bowls and now covered each bowl with a 20 9 28 cm (800 9 1100 ) sheet of cardstock. In each warm-up trial, the dog, the experimenter cueing the dog, and the experimenter holding the dog observed the baiting process as well as the covering of the bowls. During the warm-up trials, if a dog failed to initially approach either bowl within 20 s, the trial ended. In addition, warm-up trials continued until each dog successfully passed a total of four warm-up trials (two with the bowls covered and two uncovered). If a dog failed 5 or more warm-up trials, the data from the dog were excluded. No dog failed to meet these criteria, and all dogs reliably followed the experimenter’s pointing gesture during the warm-up phase and did so in five trials or fewer. Following a 2- to 3-min break, the experimental session began. Experimental phase The experimental phase consisted of three between-subject conditions. Within each condition, each participant received a total of twelve 20-s trials. The lateral positioning of the baited bowl was counterbalanced into one of the two random orders within each condition and across participants. Dogs were randomly assigned to one of the three experimental conditions and counterbalanced order of the baited bowl.
dog’s name, initiating eye contact with the dog, alternating his/her gaze between the bowl and the dog and pointed with the adjacent arm/finger toward the baited bowl. In the silent condition, the experimenter did not give any affective cue (facial or vocal) toward the baited bowl and ignored the sham-baited bowl. After the experimenter had looked and pointed toward the baited bowl and alternated their gaze between the bowl and the dog for 5 s, the experimenter then looked in their lap and the experimenter holding the dog then released the dog. Each dog was given 20 s to approach or touch a bowl with his or her paw or snout. If the dog selected the baited bowl, it was permitted to eat the treat. If the dog selected or approached the shambaited bowl, it was not provided with any treat or reward. After the dog had made their choice and/or eaten the treat, the second experimenter retrieved and repositioned the dog and the next trial was commenced. This same procedure continued for the remaining trials. Positive affect and pointing toward the baited bowl The positive affect condition was identical to the silent condition in all respects with the exception that the experimenter providing the cue conveyed a positive facial and vocal expression while looking and pointing toward the baited bowl. Critically, in the positive affect condition (as well as the negative affect condition), the experimenter directed their communicative and affective behavior toward the baited bowl and not toward the dog. Negative affect and pointing toward the sham-baited bowl During this condition, the cueing experimenter used a negative affective facial and vocal expression while looking and pointing toward the sham-baited bowl. In this condition, the negative affective expression was one of disgust rather than prohibition.
Silent pointing toward baited bowl Coding and analyses In this condition, as in the warm-up trials, each dog was seated and held by an experimenter. After the dog was positioned and seated, the third experimenter baited and covered one bowl and then sham baited and covered the other bowl. The order of baiting and sham baiting was counterbalanced across trials for each dog. The first experimenter (i.e., cuer), but not the experimenter holding the dog, or the dog, observed which bowl was baited and which bowl was sham baited. Baiting by a third experimenter was done to avoid having the experimenter providing the cue touch or otherwise ‘‘enhance’’ either bowl. After the bowls were baited and sham baited and covered, this experimenter left the testing enclosure. The experimenter providing the cues began each trial by calling the
Each dog’s choice was scored live during the experiment by the experimenter who held the dog and again from the videotapes by naı¨ve observers. This same experimenter who held the dog also recorded, using a handheld stopwatch, each dog’s latency to begin exploration or approach toward a bowl. A correct response in the look and point silent condition, as well as in the look and point with a positive affective expression condition, was defined as approaching or selecting the baited bowl referenced by the experimenter. In the look and point condition paired with a negative affective expression, a correct response, however, was defined as selecting the baited but non-referenced bowl (i.e., avoiding the sham-baited bowl that was referenced
123
Author's personal copy Anim Cogn
and was paired with the experimenter’s negative or disgusted affective expression). In other words, and across all conditions, a correct response is defined as the dog’s frequency of locating the hidden reward. Latency to leave the experimenter that held the dog was also calculated. Latency was calculated by starting a stopwatch when the experimenter holding dog released the dog and stopping the stopwatch when two of the dog’s paws crossed a. 5 M tape boundary in front of the experimenter that held the dog. Reliability was coded for 51 % of the sample (N = 23) by three naı¨ve observers from the videotapes. Reliability for latency to begin exploration was assessed by using a Pearson r correlation and was .91 (SD = .04). We also recoded the experimenter’s behavior to assess whether the experimenter looked toward the correct bowl and provided the appropriate attention-directing gesture. Reliability for looking to the correct bowl, and the appropriate attentiondirecting gesture, was assessed by Cohen’s Kappa and was 100 % between the experimenter and the three observers’ rating of the bowl selected by the dog. The affective expressions of experimenters were also assessed. This was accomplished by having seventeen undergraduate observers, who were naı¨ve to hypotheses and purposes of the experiment, rate three trials of each of three affective expressions (including neutral) from each of the four experimenters (36 trials in total). Trials were selected at random from different videotaped sessions with different dogs. The expressions were rated by having the naı¨ve observers select which affect they thought was being conveyed by the experimenter (happiness, sadness,
Fig. 2 Dogs’ mean (SD) frequency of locating the hidden treat/reward by condition and experiment out of 12 trials. N = the number of dogs, by condition and experiment, whose frequency of selecting the baited bowl was [10 out of 12 trials using a two-tailed binomial. Latency to explore is the mean duration (in seconds) dogs took to leave the experimenter holding them and begin to explore or approach one of the two bowls. **P \ .01. *P \ .05
123
surprise, disgust, anger, no emotion, and don’t see it) and its intensity (using a scale from 1 to 7). The average percent agreement regarding the affective expression displayed was 99 % for happy (range 99–100), 98 % for disgust (range 96–100), and 100 % for neutral. The average intensity rating was 6.7 (SD = .41) for happy, 6.4 (SD = 1.6) for disgust, and 1.3 for neutral (SD = .58). Results and discussion The dependent variable was the number of times dogs found, or approached, the baited bowl within each of the three conditions. For each trial, a correct response was scored as a one and an incorrect and no-response was scored as a zero. The maximum possible correct for any one dog is 12 (finding the treat on every trial). Dogs’ frequency of finding or locating the treat by condition is presented in Fig. 2. Data were initially subjected to a between-subject 2 (trial order) 9 4 (experimenter) analysis of variance (ANOVA) with frequency of finding or selected the baited bowl as the dependent variable. Results of this initial analysis failed to reach significance for trial order, experimenter, or any interactions (all P [ .1). A one-way ANOVA examined dogs’ frequency of choosing the baited bowl by condition. The main effect of condition reached significance, F (2, 42) = 62.2, P = .001, partial eta squared = .58. Scheffe´’s post hoc comparisons revealed a significant difference in correct responses between the negative affective condition (M = 2.6, SD = 1.5), and the silent condition (M = 9.9, SD = 1.9), as well as the positive affective condition
Author's personal copy Anim Cogn
(M = 10.0, SD = 2.3). The difference between the positive and the silent condition did not reach significance (P [ .10). A two-tailed binomial test was also performed to examine whether the total number of dogs in each condition exceeds chance (see Fig. 2). Using a two-tailed binomial, 10 out of 12 trials exceed chance (P \ .05). In the silent condition, 12 out of 15 dogs selected the baited bowl on 10 or more of 12 trials. In the positive condition, 9 out of 16 dogs selected the baited bowl on 10 or more of 12 trials. In the negative condition, no dog selected the baited bowl on more than 10 trials—within this condition the greatest frequency of selecting the baited bowl was four dogs which approached the baited bowl on 6 of the 12 trials. A secondary dependent variable was dogs’ latency to leave the experimenter that held them and begin exploring or approaching one of the two bowls. Latency to explore was defined as the duration of time (in seconds) between when the experimenter released the dog and when the dog began to move away from the experimenter that held the dog (defined as two paws crossing a strip of tape .5 M away from the experimenter that held them). A one-way ANOVA examined dogs’ latency to explore by condition. The main effect of condition reached significance, F (2, 42) = 19.7, P = .001, partial eta squared = .48. Scheffe´’s post hoc comparisons revealed a significant difference in latency between the negative affective condition (M = 4.5 s, SD = 1.5), and the silent condition (M = 2.2 s, SD = 1.1), as well as the positive affective condition (M = 2.1 s, SD = .81). The difference between the positive and the silent condition did not reach significance (P [ .10). Thus, dogs within the negative affective condition took longer to ‘‘leave’’ the experimenter that held them and explore or move toward either bowl. Two additional analyses were also performed. The first examined whether there is a correlation between age of the dog and their frequency of selecting the correct bowl. This correlation (Pearson r = -.14, P = .36) did not reach significance. Finally, we examined whether there is an effect of trial block. Examining trial block (trials 1–6 and 7–12) is important to assess learning. The results of trial block failed to reach significance (P [ .10). Thus, we failed to observe any learning effects or a correlation between age and dogs’ frequency of selecting the baited bowl. Given the diversity of dogs, including mixed breeds (see ‘‘Appendix’’), we lacked sufficient power to examine the effects of breed on dog’s point-following behavior. These results are consistent with previous research as they demonstrate that dogs reliably follow an experimenter’s looking and pointing gesture to locate a hidden treat/reward (e.g., Kaminski et al. 2012; Lakatos et al. 2012). These results also demonstrate when an experimenter’s looking and pointing gesture is paired with a
positive affective expression dogs continued to locate the hidden reward/treat at a level that exceeded chance. The difference between the look and point silent condition and the look, point, and positive affect condition did not reliably differ. Thus the addition of a communicated positive facial and vocal affective expression did not reliably increase dogs’ frequency of locating a hidden treat compared to pointing alone. When the experimenter looked and pointed toward an empty bowl and conveyed an expression of disgust toward the empty bowl, dogs did not reliably select the baited bowl (i.e., the non-referenced bowl). Several dogs did, however, continue to follow the experimenter’s pointing gesture toward the empty and shambaited bowl. Because dogs did not show a clear preference for either the non-baited but referenced bowl, or the baited and non-referenced bowl, the data suggest that dogs did not use olfaction. In other words, had olfaction been a primary cue then dogs’ performance should have exceeded chance in each condition (i.e., always selecting the baited bowl) without regard to where the experimenter was pointing. The fact that dogs’ frequency of locating the reward, or treat, did not reliably differ between the silent compared to the positive condition is not surprising. The lack of a reliable difference between these two conditions is likely a ceiling effect as it is well established that dogs are adept at following the pointing gesture of an unfamiliar adult in locating a hidden reward. The results of the negative facial and vocal affective condition are more ambiguous. It is possible within the negative affect condition that dogs failed to follow the adult’s pointing gesture because it did not direct the dog toward a reward. In other words, one possibility is that dogs did not follow the pointing gesture because they were not rewarded for doing so. Another possibility is that dogs simply do not follow a pointing gesture when paired with a negative facial and vocal affective expression. If the first possibility is correct, i.e., a lack of reward, then when the negative affective expression and pointing gesture is directed toward a baited bowl, so that the dog is rewarded for following the gesture, then dogs’ frequency of locating the treat should mirror the performance of those dogs in the positive and silent conditions of Experiment 1. If, however, dogs attenuated point following is due to dogs not wanting to follow a pointing gesture paired with a negative expression, which is possible given their longer latency to leave the experimenter in Experiment 1, then dogs’ performance should mirror their performance in the negative affect condition of Experiment 1—even when following the pointing gesture leads to a reward. The purpose of Experiment 2 was to examine these two possibilities. Experiment 2 was identical to negative affect condition of Experiment 1 in all aspects except that the referenced bowl was baited rather than sham baited.
123
Author's personal copy Anim Cogn
Experiment 2: negative affect and pointing toward a baited bowl Methods Participants Fifteen domestic dogs (Canis lupus familiaris) of various breeds participated (‘‘Appendix’’ shows the number of dogs by breed). Dogs were recruited in a manner identical to Experiment 1. Dogs were between 1 and 9 years of age (M = 5.1 years SD = 2.2 years). Eight dogs were male. One additional dog was tested, and its data were excluded for failure to approach any bowl during the experimental phase. Stimuli, apparatus, and procedure All stimuli and apparatus were identical to Experiment 1. All procedures, including counterbalancing and trial orders in Experiment 2, were identical to Experiment 1. Experiment 2 differed from the negative affect condition in Experiment 1 as the experimenter looked, pointed, and conveyed a negative affective facial and vocal expression (disgusted) toward a baited bowl.
which is similar to the positive condition of Experiment 1 where 9 out of 16 dogs selected the baited bowl on 10 more trials. As in Experiment 1, a one-way ANOVA was used to examine dogs’ latency to leave the experimenter that held them. The main effect of condition again reached significance, F (3, 56) = 13.4, P = .001, partial eta squared = .42. Scheffe´ post hoc comparisons revealed a significant difference between the latency for the negative baited condition (Exp. 2) (M = 4.2 s, SD = 1.8) and the positive (M = 2.1 s, SD = .81) and silent (M = 2.2 s, SD = 1.1) conditions of Experiment 1. However, the latencies for the negative baited condition (M = 4.2 s, SD = 1.8) of Experiment 2 and the negative non-baited condition (M = 4.5 s, SD = 1.5) of Experiment 1 did not reliably differ (P [ .10). Taken together, the results of Experiment 2 reveal that there is merit to both explanations for dogs’ performance during negative facial and vocal affective condition of Experiment 1. Specifically, the experimenter’s negative affect did reduce, or delay, the dog’s exploration away from the experimenter that held them, but it did not reduce their frequency of locating the treat as long as the other experimenter’s attention-directing gesture referenced a baited bowl.
Results and discussion
General discussion
All coding procedures were identical to Experiment 1. The dependent variable was again the number of times dogs approached (i.e., chose) the baited bowl. Dogs’ frequency of choosing the baited bowl is presented in the right panel of Fig. 2. Data were again subjected to a between-subject 2 (trial order) 9 4 (experimenter) analysis of variance (ANOVA) with frequency of selecting the baited bowl as the dependent variable. Results of this initial analysis failed to reach significance for trial order, experimenter, or any interactions (all Ps [ .1). A one-way ANOVA examined dogs’ frequency of choosing the baited bowl by condition—including the conditions of Experiment 1. The main effect of condition reached significance, F (3, 56) = 44.5, P = .001, partial eta squared = .70. Scheffe´ post hoc comparisons revealed a significant difference between the negative baited condition (Exp. 2) (M = 9.3, SD = 2.2), and the negative nonbaited condition of Experiment 1 (M = 2.6, SD = 1.5). In addition, dogs’ frequency of selecting the baited bowl during Experiment 2 did not differ from the positive or the silent condition during Experiment 1 (both Ps [ .1). We also examined the number of dogs choosing the correct bowl in Experiment 2 exceeded chance, i.e., 10 or more out of 12 (see Fig. 2). The results revealed that 8 out of 15 dogs in Experiment 2 selected the baited bowl on 10 more trials
The purpose of these two experiments was to explore the effects of an unfamiliar adult’s positive and negative facial and vocal expressions, when paired with a pointing gesture, on dogs’ frequency of locating a hidden reward. Broadly, these results replicate previous research showing dogs reliably follow a human’s pointing gesture (Hare and Tomasello 1999; Miklo´si et al. 1998; Miklo´si and Soproni 2006; Soproni et al. 2001). These results also extend the results of prior studies in several ways. First, the addition of an experimenter’s positive affect did not increase dogs’ frequency of locating a hidden treat/reward compared to looking and pointing in silence. The fact that the silent and positive affect conditions did not reliably differ is not surprising as the results of these two conditions revealed that dogs were nearly at ceiling as they correctly chose the baited bowl on average 10 out 12 trials and is consistent with prior research (e.g., Hare and Tomasello 1999; Riedel et al. 2008). Second, and in both Experiments, the inclusion of an experimenter’s negative/disgusted affective expression delayed dogs’ exploration or approach of either bowl. The results of Experiment 2 further reveal that while the negative facial and vocal affect delays dogs’ exploration, dogs do follow an experimenter’s pointing gesture, even when paired with a negative affective expression, as long as the experimenter
123
Author's personal copy Anim Cogn
references a baited bowl. In addition, dogs’ frequency of approaching the negatively referenced but baited bowl in Experiment 2 did not differ from either the positive affective condition or the looking and pointing in silence condition of Experiment 1. Together, these results demonstrate that an unfamiliar adult’s affective behavior has a nuanced effect on dogs’ point-following behavior in locating a hidden reward. To our knowledge, this is the first study that directly assesses how communicated affect, when paired with a pointing gesture, influences dogs’ point-following behavior. The fact that we demonstrated that dogs delay their exploration when an unfamiliar adult provides a negative facial and vocal affective expression is convergent with the results of Merola et al. (2012a) who also demonstrated that dogs showed increased rates of behavioral freezing when their owner presented a negative or fearful affective expression. Unlike Merola et al. (2012a, 2014), however, who showed that dogs do not increase their exploration when their owner provided a positive affective expression, our results show that dogs do approach an unfamiliar object when an unfamiliar adult provides a positive facial and vocal expression. This difference is likely due to the fact that Merola et al. (2012a, 2014) used an ambiguous object (a fan), whereas our object (food bowl) was not ambiguous and contained a reward/dog treat. While our results show affective expressions influence dogs’ point-following behavior, our results also reveal that the presence or absence of a reward further influences dogs’ point-following behavior. For example, Bentosela et al. (2008) found when dogs that were once rewarded for gazing toward an experimenter and then were no longer rewarded, or the quality of the reward was reduced, there was a steady decline in dogs’ gazing toward the experimenter across trials. Likewise, within the negative affect condition of Experiment 1 our results suggest dogs’ frequency of locating the correct bowl was reduced because the gesture did not direct the animal toward a reward. Taken together, our results demonstrate that negative affect does affect dogs’ exploration; however, dogs will follow an unfamiliar adult’s attention-directing gesture toward a target location as long as that target location contains a reward. More broadly, what do these results demonstrate within the context of canine social referencing? As traditionally described (e.g., Sorce et al. 1985; Walden and Ogan 1988), social referencing occurs when one uses another’s emotional expression in guiding their exploratory behavior toward an ambiguous object or event. In other words, the affective information is used to disambiguate the previously ambiguous object. In the current experiment, it is clear that the negative affect did influence the dogs’ behavior in terms of when they left the experimenter that held them, thus providing evidence that dogs at least
discriminated the negative affect from the silent and positive affect conditions. The results do leave open the possibility, however, that the dogs interpreted the affective expression as being ‘‘about the experimenter’’ providing the cue rather than in reference toward one of the two bowls. In other words, in Experiment 1 dogs were willing to walk toward the experimenter and one of the bowls when provided a positive affective expression and reward, but dogs were delayed in their exploration in Experiments 1 and 2 when provided negative facial and vocal affective expressions. Therefore, one possibility for future research would be to have the experimenter look and point while conveying an affective expression toward one of two locations and then have that experimenter leave the area. If dogs comprehended the affective expression to be in reference to the experimenter, then dogs would approach either bowl with equal frequencies once the experimenter left. If, however, dogs comprehended the affect in reference to one of the bowls or objects, then dogs would approach the bowls or objects with different frequencies and would thus show that the affect was in reference to the object/bowl rather than the experimenter. While dogs in the current experiment showed behavioral evidence of discriminating the positive and negative affective expressions, it is not unequivocal that the dogs in the current study showed social referencing. The results of current study, along with recent research by Merola et al. (2013, 2014), provide additional avenues for future research relevant for our understanding of dogs’ proclivity for social referencing. For instance, Merola et al. (2013) have shown that pet dogs, compared to water rescue trained dogs of the same breed, approached a novel and ambiguous object more often than their water rescue trained peers. In other words, in both the current study and in Merola et al. (2013), pet dogs used the positive affective information from an unfamiliar adult in approaching an unfamiliar object. Thus future research is needed that continues to examine how different types of dog training, familiarity of the experimenter, and perhaps the breed and age of the dog influence their frequency of social referencing (see Merola et al. 2014 for a similar point). Another possibility for future research is canines’ capacity for deductive reasoning. For example, and within the current experiment, in both the silent and positive affective conditions of Experiment 1, dogs could gain access to the treat by following the pointing gesture; however, within the negative affective condition of Experiment 1, dogs could only gain access to the treat by not following the pointing gesture. Thus gaining access to the treat in the negative affect condition requires dogs to (1) infer that the negative affect is in reference to the empty bowl and (2) by a process of exclusion deduce that the treat is
123
Author's personal copy Anim Cogn
in the other bowl. While there is evidence for one dog, ‘‘Rico,’’ which has shown deductive reasoning, or reasoning by exclusion, in a word learning task, it is not clear that dogs in general are capable of such problem solving (Aust et al. 2008; Kaminski et al. 2004). If dogs in the current study did learn to employ such reasoning in locating the treat, then one might have observed an effect of trial block where dogs’ performance is greater on the second block of trials compared to the first block of six trials which we did not. Thus another possibility for future research is to examine whether dogs reason by exclusion within the context of social referencing. Humans use a variety of physical and affective behaviors when they communicate—including when they communicate with dogs. These results add to a growing literature demonstrating that dogs reliably use an unfamiliar adult’s physical cues in locating a hidden treat. These results further demonstrate that the presence of an adult’s affective expression has a nuanced affect on dogs’ point-following behavior. More broadly, these results highlight the fact that dogs are sensitive to various human social communicative behaviors; however, the results also suggest that dogs may rely on physical cues more than subtle or non-ostensive cues. In addition, these results suggest the need for continued research examining whether, and under what conditions, dogs’ perceive a human’s affective behavior as referential and how it affects dogs’ exploratory behavior. Finally because humans and canines have coexisted and communicated for thousands of years, where human–canine communication includes a variety of communicative behaviors, including the sharing of affect, continued research is needed that unpacks the dynamic interplay of these communicative behaviors. Acknowledgments All procedures performed in these experiments were in accordance with the ethical standards of the BYU Institutional Animal Care and Use Committee. These data were submitted in partial support of the second author’s MS thesis from Brigham Young University. This research was supported by a Brigham Young University undergraduate mentoring grant awarded to the first author. The authors gratefully acknowledge Sean and Ana Aaron, Andrew Dorsett, Chantelle Fitting, Darren Guenther, James Parker, and Will West, for their assistance in data collection. A portion of this data was presented at the 50th annual meeting of the Animal Behavior Society, July 2013. Compliance with ethical standards Conflict of interest of interest.
Appendix See Table 1.
123
The authors declare that they have no conflict
Table 1 Participant breed Experiment 1 n = 45
Breed
1
Greyhound
1
English Bulldog
2
Bernese Mt. dog
2
Husky
3
Australian Shepherd
3
Collie
3
German Shepherd
5
Pit bull
6
Golden Retriever
9
Border Collie
10
Labrador and Lab Mix
Experiment 2 n = 15
Breed
1
Australian Shepherd
1
Boxer
1 2
Husky Border Collie
2
Golden Retriever
3
Doberman
5
Labrador and Lab Mix
References Aust U, Range F, Steurer M, Huber L (2008) Inferential reasoning by exclusion in pigeons, dogs, and humans. Anim Cogn 11:587–597 Bentosela M, Barrera G, Jakovcevic A, Elgier A, Mustaca A (2008) Effect of reinforcement, reinforcer omission and extinction on a communicative response in domestic dogs (Canis familiaris). Behav Process 78:464–469 Buttelmann D, Tomasello M (2013) Can domestic dogs (Canis familiaris) use referential emotional expressions to locate hidden food? Anim Cogn 16:137–145 Ekman P, Friesen WV (1975) Unmasking the face. A guide to recognizing emotions from facial clues. Prentice-Hall, Englewood Cliffs, New Jersey Flom R, Bahrick L (2007) The effects of multimodal stimulation on infants’ discrimination of affect: an examination of the intersensory redundancy hypothesis. Dev Psychol 43:238–252 Fridlund A (1994) Human facial expression: an evolutionary view. Academic Press, San Diego, CA Gibson EJ, Pick AD (2003) Ecological approach to perceptual learning and development. Oxford University Press, New York Hare B, Tomasello M (1999) Domestic dogs (Canis familiaris) use human and conspecific social cues to locate hidden food. J Comp Psychol 113:173–177 Hare B, Brown M, Williamson C, Tomasello M (2002) The domestication of social cognition in dogs. Science 298:1634–1636
Author's personal copy Anim Cogn Kaminski J, Call J, Fischer J (2004) Word learning in a domestic dog: evidence for ‘‘fast mapping. Science 304:1682–1683 Kaminski J, Schulz L, Tomasello M (2012) How dogs know when communication is intended for them. Dev Sci 15:222–232 ´ (2009) A comparative Lakatos G, Soproni K, Do´ka A, Miklo´si A approach to dogs’ (Canis familiaris) and human infants’ comprehension of various forms of pointing gestures. Anim Cogn 12:621–631 ´ (2012) Comprehension and Lakatos G, Ga´csi M, Topa´l J, Miklo´si A utilisation of pointing gestures and gazing in dog–human communication in relatively complex situations. Anim Cogn 15:201–213 Merola I, Prato-Previde E, Marshall-Pescini S (2012a) Social referencing in dog-owner dyads? Anim Cogn 15:175–185 Merola I, Prato-Previde E, Marshall-Pescini S (2012b) Dogs social referencing towards owners and strangers. PLoS One 7(10):e47653 Merola I, Marshall-Pescini S, D’Aniello B, Prato-Previde E (2013) Social referencing: water rescue trained dogs are less affected by the strangers message. App Anim Behav Sci 147:132–138 Merola I, Prato-Previde E, Lazzaroni M, Marshall-Pescini S (2014) Dogs’ comprehension of referential emotional expressions: familiar people and familiar emotions are easier. Anim Cogn 17:373–385 ´ , Soproni K (2006) A comparative analysis of animals’ Miklo´si A understanding of the human pointing gesture. Anim Cogn 9:81–93 ´ , Polga´rdi R, Topa´l J, Csa´nyi V (1998) Use of experiMiklo´si A menter-given cues in dogs. Anim Cogn 1:113–121
Morisaki A, Takaoka A, Fujita K (2009) Are dogs sensitive to the emotional state of humans? J Vet Behav Clin Appl Res 4:49 Nagasawa M, Murai K, Mogi K, Kikusui T (2011) Dogs can discriminate smiling faces from blank expression. Anim Cogn 14:525–533 Riedel J, Schumann K, Kaminski J, Call J, Tomasello M (2008) The early ontogeny of human-dog communication. Anim Behav 75:1003–1014 Soproni K, Miklo´si A, Topa´l J, Csa´nyi V (2001) Comprehension of human communicative signs in pet dogs (Canis familiaris). J Comp Psychol 115:122–126. doi:10.1037/0735-7036.115.2. 122 ´ , Topa´l J, Csa´nyi V (2002) Dogs’ (Canis Soproni K, Miklo´si A familaris) responsiveness to human pointing gestures. J Comp Psychol 116:27–34 Sorce J, Emde R, Campos J, Klinnert M (1985) Maternal emotional signaling: its effect on the visual cliff behavior of 1-year-olds. Dev Psychol 21:195–200 Udell MAR, Giglio RF, Wynne CDL (2008) Domestic dogs (Canis familiaris) use human gestures but not nonhuman tokens to find hidden food. J Comp Psychol 122:84–93 Walden TA, Ogan TA (1988) The development of social referencing. Child Dev 59:1230–1240 Wells DL (2003) Lateralised behaviour in the domestic dog, Canis familiaris. Behav Process 61:27–35
123
