From capuchin tantrums to #caninecog: The importance of fairness

Many parents of three- and four-year old children learn very quickly that tantrums can be averted by dividing a cookie into two parts when the child “wants” two cookies or using two cups that are the same size when serving drinks. These tricks mediate the sense of equity or “fairness” that even young humans feel so strongly.

This sense of fairness appears to be shared by a number of non-human species including a variety of primates (apes and monkeys), birds, rats, and even cleaner fish.

In 2003, Sarah Brosnan and Frans De Waal published a paper on the responses of capuchin monkeys to an inequitable outcome in which two monkeys, paired together as partners, initially received equal payoffs (a piece of cucumber), followed by unequal payoffs (i.e., one of the monkeys received a grape while the other still received the cucumber) in a token exchange task with a human.  Hint: a cucumber pales in comparison to a grape.

Aside from the fact that this paper was one of the first of its kind to document inequity aversion in non-human animals, its true claim to fame was the video that went viral of the capuchin’s response to the cucumber when her partner received a grape (presented in De Waal’s 2013 Ted talk):

What is inequity aversion?

As illustrated in the clip above, inequity aversion is defined by negative responses to unequal payoffs like the grape vs. the cucumber.  Jim McGetrick and Friederike Range recently published a review of the research on inequity aversion in dogs in the special issue of Learning & Behavior that gave rise to the #caninecog digital event. I focus on their article in this post. McGetrick and Range first argue that when humans forego material payoffs to achieve equity, they are in essence promoting cooperation and protecting others from being exploited.

Two forms of inequity aversion are recognized: disadvantageous and advantageous. When individuals reject inequity that is disadvantageous to themselves, they are displaying disadvantageous inequity aversion (i.e., the monkey that received the cucumber and not the grape). By contrast, if individuals reject inequity that is advantageous to themselves but disadvantageous to their partners, they are engaging in advantageous inequity aversion (i.e., if the monkey that received the grape had been as upset as the monkey that received the cucumber).

Most of the research conducted with non-human subjects, including dogs, tests the disadvantageous version of inequity aversion.

McGetrick and Range reviewed the current literature on canine responses to inequity aversion. In their review, they compared and contrasted the strengths and weaknesses of the basic tasks used to test inequity aversion in dogs.  They also discussed the possible mechanisms for. and factors affecting, the findings that supported the presence of a primitive form of inequity aversion in dogs.  They ended with a discussion about the ultimate function of this behavior, assuming that the assumptions about inequity aversion in dogs were true.

Testing Inequity Aversion in Dogs

Two types of tasks have been utilized to test inequity aversion in dogs: the paw task and the buzzer task. Both are illustrated below:

In the paw task (left panel), two dogs sitting side-by-side are requested alternately to give a paw to the experimenter. On equitable trials, both dogs receive the same food reward. On inequitable trials (2 variations: quality of food or reward/no reward), one dog received either a high quality reward (i.e., sausage) or a food reward of some kind while the other dog received either a low quality reward (i.e., bread) or no food reward at all.  In an earlier study by Range and colleagues, the dogs presented their paws less often when no reward was provided, as compared to when the rewards were equitable. Interestingly, the quality of reward did not produce any reduction in paw giving responses, suggesting that the different reward types were either not perceived or noticed by the dogs.

In the buzzer task (right panel), rather than presenting a paw on command, the dogs had to press a buzzer on command. This paradigm was used by Essler and colleagues in 2017. The delivery of food rewards was very similar to the two previous studies, and the results supported the previous research that indicated that a primitive form of inequity aversion exists in dogs.

Despite these corroborating results, other studies failed to find evidence for inequity aversion for pet dogs in the same buzzer task described above (Brucks and colleagues, 2017), and in a study using a different testing paradigm in which pet dogs had to choose between fair and unfair trainers when their partner was absent and no food reward was given (see Horowitz, 2012 for more details). McGetrick and Range argue that these studies help identify potential areas for future research, including the mechanisms and factors influencing the exhibition of inequity aversion by dogs.

What’s driving inequity aversion and what is not?

Cognitive skills

To recognize and act upon an inequity aversion, researchers have argued that individuals need to be able to compare the relation between their own efforts and rewards along with their partners’ experience while also being able discriminate between numbers, quantity, and quality. Being able to experience negative emotions or engage in inhibitory control (i.e., able to stay with original choice despite feedback received or greater impulsivity) also appear to be important processes in inequity aversion.

Other factors

Research with primates and birds has suggested that factors such as sex, dominance rank, relationship quality/length, personality, age, and effort affect the expression of inequity aversion. For dogs, relationship quality with partner, dominance rank, testing paradigm, dog breed, and experiences with humans may affect the presence or absence of aversion inequity.

Alternative explanations that have been ruled out

Based on the myriad controls utilized in the literature on dog inequity aversion, a number of alternative explanations have been ruled out. First, the presence of the reward is not driving the inequity aversion in dogs since all rewards were always visible to both dogs. Second, food expectations and their possible violation were controlled by most protocols used. Third, frustration caused by a downshift in rewards was controlled in the dog studies by presenting high quality rewards before the key inequity conditions and making sure those conditions were not tested first. Finally, social disappointment by the dogs because the human experimenter failed to reward them as expected from their dog partners’ reward was less likely because of the pattern of responses exhibited by the dogs in the two types of inequity conditions (low value reward or no reward).

Ultimately, what’s the point?

Inequity aversion, even a primitive form, is thought to be an important mechanism in promoting cooperation between individuals who are not related. Through experiences involving inequitable outcomes, individuals may be able to test other individuals to assess their willingness to cooperate.

Evidence from inequitable conditions indicated that dogs were less likely to tolerate co-feeding with or proximity by the partner dogs, suggesting that the inequity aversion had affected the dogs’ “beliefs”.

Ultimately, inequity aversion in dogs may exist to promote cooperation or it may not, and instead may be a vestigial behavior that will eventually be selected out. Clearly much more research is needed before the final word is out on dogs.

In the meantime, in the spirit of our young children, be sure to feed both dogs the sausage or the bread and never give one dog the sausage and the other dog nothing, unless of course you wish to elicit some howling and whimpering.

Article focused on in this post:

McGetrick, J., & Range, F. (2018). Inequity aversion in dogs: a review. Learning & Behavior, 6, 479 – 500. DOI: 10.3758/s13420-018-0338-x.

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