Thursday, November 1, 2012

Do Dogs Display Guilt after Eating Forbidden Hot Dogs? It Depends How the Data Is Massaged

An advertisement in a Budapest newspaper sought participants in a study about pet dogs.  The ad specified that the only owners who need reply were those whose dog (1) was older than eight months, (2) had lived with the owner for at least six months, (3) could remain calm if left alone in an unfamiliar room for three minutes, and (4) had not participated in food-reward studies. Also, owners had to say that if they prohibited their dog from eating food in a room, they would be unsure whether the command would be obeyed if they left the room. 

Generally, the experiment involved recording the greeting behavior of the dog after a brief separation from the owner, followed by the owner telling the dog not to eat some hot dog pieces on a plate and leaving the room.   The owner returned to the room, but could not see the plate with the hot dogs behind a barrier, and had to assess whether the dog’s behavior indicated that it had eaten or not eaten the food. 

Most owners (40 of 54) correctly stated what their dog had done while they were out of the room. Nevertheless, the researchers eliminated a number of the responses on various grounds, after which there was no longer statistical support sufficient to conclude that owners could actually recognize guilty behavior in their dogs.   

Dog Behavior

The research was conducted by Julie Hecht, Adam Miklosi, and Marta Gacsi of the Department of Ethology of Eötvös Loránd University in Budapest.  All three authors are among the most renowned dog behavior people now working, and all have been cited in prior blogs, as well as in both of my dog books. 

Their discussion begins with the behavioral aspects of domestication, where they note:

“Among scientists, the emotional experience of social, non-human animals remains a contentious topic.  While primary emotions, like anger and fear, serve an evolutionary function to adapt and respond to social and environmental demands, the precursors for the experience of secondary emotions, like embarrassment, pride and guilt, are not widely attributed to non-human animals.”

Dog owners, however, believe that dogs experience guilt, and they believe this more of dogs than of any other companion animals.  One study (Morris et al., 2008) concluded that 74% of dog owners claim to recognize guilt in their dogs; the next-highest attribution, at 36%, is found in horse owners.

The scientists describe guilt as “a self-conscious, evaluative emotion associated with a self-perceived violation against an established rule to which one has agreed to adhere.”  Guilt is useful in reinforcing social relationships and behaviors, and is associated with actions such as constricting posture, moving the head down and averting gaze, which have been described in non-human primates.  Wolves sometimes demonstrate such behaviors.  The scientists cite Alexandra Horowitz’s conclusion that “when dogs display these behaviors in particular interspecific social contexts, owners interpret the behavior to signify knowledge of transgression and therefore indicative of guilt.”  Horowitz, however, found that the “guilty look” was, in fact, “a response to owner scolding, not an appreciation of a misdeed.”  (Horowitz, 2009)

Objectives of the Study

Hecht and her colleagues wanted to explore two questions:
  • Is there a difference in dog presentation of ABs [associated behaviors of guilt] when greeting their owners between dogs that disobeyed a social rule in owners’ absences and dogs that did not disobey?
  • By relying solely on dog greeting behavior, can owners determine, upon returning to a room, whether their dog transgressed?
The scientists found 64 pet dogs whose owners filled out a questionnaire.  The questionnaires revealed that owners mentioned 11 associated behaviors of guilt (“guilt behaviors”), which were:
  •  lowering body 
  •  tail down 
  •  moving away from owner 
  •  freezing 
  •  turning 
  •  head away from owner 
  •  lowering head and lack of jumping 
  •  putting ears back 
  •  averting eyes 
  •  approaching low and slow 
  •  lack of barking
Video recordings indicated that jumping was not revealed during scolding.

The questionnaires revealed that 91.8% of owners claimed that their dogs sometimes showed guilt behavior, and that this behavior indicated that the dog knew it had done something wrong. Of these, 59.2% acknowledged that a dog’s guilty behavior caused them to scold the dog less.  This is consistent with previous studies concluding that attributing human-like emotions to non-human animals affects how humans interact with these animals.  (Anyone who remembers childhood knows that acting guilty often reduced the punishment.)

Dogs were of many breeds, slightly more females than males, though many more women dog owners participated than men, 47 against 6.  This curiously high imbalance should have been explained.  

Phases of the Experiment

(1) In the first phase of the experiment, the dog, the owner, and the experimenter entered the test room.  The dog was off-leash and free to explore. The room contained a table that was low enough to make it easy for the dog to see anything on it. The experimenter and owner left the room for three minutes. The owner re-entered the test room but, instead of interacting with the dog, the owner stood at the door and described the dog’s behavior to the experimenter, who remained in the hallway but could hear the owner through the closed door.  The owner then put the leash on the dog and they both left the room. 

(2) In the first food phase, the owner, the experimenter, and the dog entered the test room and the dog was taken off leash.  The owner held a plate with two pieces of hot dogs.  The owner and experimenter pretended to eat from the plate for thirty seconds to “create the desired social context—that the food was for humans and not dogs”—then the owner put the plate on the table without saying anything to the dog.  If the dog ate any of the hot dog pieces in the next thirty seconds, the owner scolded the dog for up to ten seconds while the experimenter turned her back (to give the owner privacy, which it was hoped would make the owner act natural while scolding).   

(Two questions we have at this point: When did the owner know that he or she would be able to scold for the dog eating, which had not been prohibited?  If this was known before the dog ate, there might already have been a degree of prohibition from the owner’s body language.  Also, if a dog is regularly punished for eating human food, would not the “social context” of the experimenter and the owner pretending to eat from the plate effectively create a command?)

Regardless of whether the dog had eaten or not, the owner next picked up the plate and the experimenter and the owner walked around the edge of the room.  If the dog had eaten, the experimenter replaced the hotdog from her waist pouch, and the owner and experimenter again pretended to eat from the plate. Then the owner put the food back on the table, but this time specifically warned the dog not to eat it.  If the dog ate the food anyway, the owner scolded it. (So some dogs had been scolded twice by this point.)

(3) In the next food phase, the owner put the food on the table and told the dog not to eat it, then both the owner and experimenter left the room.  The dog was left alone for three minutes.  The owner then re-entered the room but could not see the table because of a small barrier that prevented a view from near the door.  The owner had been instructed to decide, based on the dog’s greeting behavior, whether it ate the food during the three-minute absence by saying “yes,” “no,” or “not sure.”  The experimenter asked the owner (from the hallway), “Why do you think this?” to get as much detail as possible regarding the dog’s behavior.  If the dog had eaten, the owner could scold.  If not, the owner could praise. 

(4) In a final phase, the opening non-food phase to watch the initial greeting behavior of the owner and the dog was repeated. 

What the Researchers Saw

The researchers examined whether dogs that had eaten differed from dogs that had not in the part of the experiment which occurred as owners entered the room after having previously warned the dogs not to eat the hot dog pieces.  The researchers who scored the dogs’ behaviors at this point were themselves unaware of whether the dogs had or had not eaten the hot dog pieces, as were the owners at the moment the greeting occurred.  The researchers could detect no difference between eaters and non-eaters in their display of guilt behaviors. 

Nevertheless, some differences in greeting behavior were detected by the researchers.  Dogs generally showed fewer guilt behaviors when greeting owners than when being scolded, which seems consistent with Horowitz’s observations.  Dogs that did eat when their owners were out of the room showed more guilt behaviors in greeting after the owner returned than they had in the first phase when separated from their owners with no food involved. Thus, these dogs showed more guilt behaviors after violating a command than they did in the baseline established by the first greeting in the experiment.    

The researchers also detected that dog which did not eat in their owners’ absence showed fewer guilt behaviors in the final phase (4) than they had when greeting their owners after (3). Thus, dogs that many people would call “good dogs” because they did not eat, nevertheless showed more guilt behaviors when they had the opportunity to be bad than they did when they did not have this opportunity at the end of the experiment.  This might suggest these good dogs were fearful of being punished for what they did not do, or just better trained.   There was no discussion of the level of training previously received by the dogs in the experiment. In either case, guilt behaviors as observed by the researchers were not randomly distributed throughout the greetings in the experiment.   

Owners’ Responses

When asked if a dog had eaten in the owner’s absence, 4 owners were unsure but 58 said “yes” or “no.”  Of those 58, 40 were correct and 14 incorrect. Thus, overall, owners were successful in determining whether dogs had or had not violated a command not to eat. 

Nevertheless, the researchers did not think that this confirmed that owners could correctly assess whether a dog had eaten or not because some owners perhaps had a bias based on a dog’s prior behavior in the experimental context.  They first eliminated results of owners who seemed to have a bias towards thinking one way or the other based on their mentioning the dog’s history inside the experiment.  The results after this adjustment were still better than chance.  If, however, the researchers looked only at owners whose dogs ate while the owner and the experimenter were in the room but before the prohibition on eating the hot dog pieces had been explicitly stated, but did not eat after the prohibition was stated and the owner and experimenter were still in the room, the result was no better than chance.  This selection of the data excludes dogs that did not eat because they were unsure if there was a command in place, or accepted that there was a command from the pretend eating of the owner and the experimenter, or from body language of the owner if the owner knew that he or she was going to scold if the dog ate, regardless of the lack of explicit command.

Whether selecting a specific slice of the data proves that dog owners cannot really tell guilt in dogs is not clear to us, and the scientists do not in the end claim that it is.  After all, as noted before, the researchers did find, in their analysis of the videotapes, that dogs that ate when their owners were out of the room showed more guilt behaviors in greeting after the owner returned than they had in the first phase when separated from their owners with no food involved.   The researchers acknowledge that their experimental design left some possibilities open, and further testing will be necessary to say more.   

Design Issues

As dog people, we are concerned about several aspects of the experiment.  It is not stated when the dogs last ate.  Were they allowed normal food intake?  Was there a period in which they were not allowed to eat? Contrary to popular belief, not all dogs like hot dogs.  If a dog ate a hot dog piece when the owner and experimenter were in the room, it might not have been interested in trying again.  Does this make its response more valid, as determining the owner’s ability to sense guilt, than if it disliked hot dogs enough not to eat during any of the opportunities? 

The interpretation of a dog’s actions by its owner might also be subject to more detailed analysis.  What guilt behaviors did each individual owner specify?  Could those specified by an individual owner have indicated the owner recognized some behavior associated with guilt, while the dog’s overall behavior, on the 11 guilt behaviors as assessed by the researchers from the videotapes, was more neutral? 

Additionally, it must be noted that some owners, in our experience, list other behaviors as inducing guilt including jumping on furniture, urinating, or scratching the floor, some or all of which may have existed in the experiment during the time the experimenters and owners were out of the room, as this was not discussed in the report. Arguably, physiological changes should also be recorded. 

Perhaps Only Some Dogs Show Guilt

One of us (JE) grew up with two Cocker spaniels, Blackie and Sandy.  My mother always insisted that she could tell when Sandy had done something he was not supposed to do because he would display guilt.  Blackie, in her opinion, did not feel guilty about anything.  As a child, I always assumed that she was right about this, and I believe that Blackie was punished more because of the feeling that he was recalcitrant. 

Guilt seldom had anything to do with being left alone in the house because dogs of Pullman, Washington, in that era were more often outside than inside.  Our dogs were not in the house except in the worst weather and had an insulated doghouse that had been built by the same contractor who built our house.  Guilt was usually about digging something up in my mother’s flower garden or eating something from the outdoor flagstone fireplace grill.  Blackie, in particular, had a curious love of carrots and could dig up two or three a day, which annoyed my father when it began.  Soon he was not punished for this, however, as once my father accepted Blackie's love of carrots, several rows of the vegetable were planted for his use alone.  
Perhaps Blackie had a bit of the wolf left in him.  He was the one who learned how to get away by (1) wrapping a leash around a tree and pulling back and forth until the leash broke, (2) climbing over the 6-foot high steel hog fence that my father strung so the dogs would have a large yard, and (3) digging under this fence after my father strung barbed wire across the top to prevent Blacky from climbing over it.  After that my father gave up and any time a bitch was in heat in Pullman we’d have to wait for the irate owner to call and tell us where Blackie was hanging out.  Sometimes Blackie was kept in the house for a few days if the owner of the female was sufficiently angry. 

Sandy never disobeyed the rules and never went off in search of females that might want some attention. My mother and I cried for days after he was hit by a car when I was ten years old.  Blackie died a natural death at 16, a year after we moved to Fresno. 

Defining Guilt in Dogs

Whether my mother was right about Sandy showing guilt I cannot say. Hecht and her colleagues observe that “an ambiguous social situation generated by repeated scoldings and greetings—not uncommon for experiments investigating guilty behavior—could affect the behavioral displays in question in a complex way.”  Perhaps this acknowledges that there are more things in dog heaven and earth than meet the scientist’s eye. How “repeated” must scoldings be to affect the results of an experiment like this?  I suspect Sandy and Blackie were only punished two or three times a year. 

Guilt is a somewhat loaded concept, and in many uses includes an element of remorse.  Such is not established, and not intended, in this research.  The researchers describe guilt as “a self-conscious, evaluative emotion associated with a self-perceived violation against an established rule to which one has agreed to adhere.”  Perhaps this could be rephrased to say that guilt is a self-conscious evaluative emotion associated with an understood violation of a rule to which an animal has been trained or expected to adhere.  The dog does not feel remorse, but rather anticipates disapproval or punishment based on not adhering to a command.  Some of the results arguably support this.  The study at least establishes that perception of guilt behaviors is more than a simple anthropomorphic projection we put onto the behavior of our dogs. (Whether remorse in humans is partly an internalization of punishments once received I leave to the psychoanalysts.)

Conclusion 

Thinking that dogs have human thoughts and emotions that they may not in fact have, i.e., anthropomorphism, as argued by James Serpell (2003) and others, probably existed very early in the human-canine relationship, and may be fundamental to the success of domestication.  It explains something about why many of us see dogs as members of our families and societies.  Homer’s account of a hunting hound recognizing his master in Book 17 of The Odyssey contains elements of anthropomorphism.  The dog, Argus, has not seen his master for two decades but is not strong enough to crawl to him.  Odysseus cannot pet the dog for fear that Penelope's suitors will recognize him and kill him.  He has to hide a tear, but perhaps tries to speak to the dog indirectly by asking the swineherd, who is serving as his guide, why such a finely built dog is left to lie on a dung heap. 

As Homer knew, there is room for guilt on the human side of a relationship between a man and a dog. To this day, I feel guilt on remembering how I ignored Blackie when I was a teenager, trying against hope to fit into the California culture that was new and frightening to a maladjusted misfit, paying no attention to my long faithful dog as he prepared to die.  I failed him, but the memory of that failure has become part of my conscience, and I hope has made me a better dog owner as an adult.  To put it another way, Blackie is still part of me.  That is one of the things our pets do for us. 

This blog was written by John Ensminger and L.E. Papet. 

Hecht, J., Miklosi, A., and Gacsi, M. (2012). Behavioral Assessment and Owner Perceptions of Behaviors Associated with Guilt in Dogs.  Applied Animal Behavior Science, 139, 134-142.

Additional References:
  1. Horowitz, A. (2009). Disambiguating the Guilty Look: Salient Prompts to a Familiar Dog Behaviour. Behavioral Process 81, 447-452.
  2. Keltner, D. (1995). Signs of Appeasement: Evidence for the Distinct Displays of Embarrassment, Amusement, and Shame. Journal of Personality and Social Psychology, 68, 441-454.
  3. Morris, P.H., Doe, C. and Godsell, E. (2008). Secondary Emotions in Non-Primate Species?  Behavioural Reports and Subjective Claims by Animals Owners. Cognition and Emotion, 22(1), 3-20.  
  4. Serpell, J. A. (2003). Anthropomorphism and Anthropomorphic Selection—Beyond the “Cute
    Response.” Society and Animals, 11(1), 83–100.

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