Do animals understand the concept of fairness?

"It's not fair."

Those familiar words of indignation span all ages, from the child who covets a playmate's toy to the adult who learns a co-worker earns more money doing the same job.

Humans have a keen sense of inequity and are quick to protest when they encounter it. This rejection of inequity is said to have played a role in the evolution of human cooperation, since monkeys also appear to get angry when they receive unequal treatment.

One study detected distinct signals in the primate brain that, scientists believe, indicate they recognize bias. There also is that humorous, well-publicized video of a monkey flinging cucumber slices back at a researcher after seeing the monkey in the next cage get a grape for performing the same task.

Some scientists wonder, though, do animals actually grasp the concept of fairness, or are other factors at work?

Primate research from Germany suggests that "social disappointment" with humans may play a role. The study found that long-tailed macaques were more likely to reject an inferior reward from a human than from an automatic feeding machine, meaning they can distinguish between the two and react to the difference.

Understanding such reactions is important "in the context of learning more about human evolution," said study co-author Rowan Titchener, a doctoral student at the Georg-August-Universität Göttingen. If primates, including humans, share certain behaviors, "it means it has likely evolved in our last common ancestor, and was potentially advantageous for survival," she said.

The research, which appeared in Royal Society Open Science in March, looked at four different experimental conditions: In one set, a subject monkey received less-preferred food (fennel) from a human experimenter or an automated food dispenser. In the other set, the subject monkey received fennel, while the partner monkey in an adjacent cage got grapes, a better treat, from a human experimenter or the machine.

The researchers found that the subject monkeys more often refused the low-value food from the humans but accepted the same low-value food from the machine. This happened both when the monkey was alone or with the partner monkey.

"If the monkeys were reacting due to a sense of inequity, we would have seen frustration only when the other monkey was getting a better reward," said Titchener, who is also a researcher in cognitive ethology at the German Primate Center — Leibniz Institute for Primate Research (DPZ). "Instead, we saw food refusal consistently with the human, as compared to the machine."

She thinks the monkeys understood that the human's goal was to provide low-value food, and that "the machine is inanimate — it has no goal," she said. "The monkeys have no social expectations of a vending machine and are therefore not disappointed."

Sarah Brosnan, distinguished university professor of psychology, philosophy and neuroscience, and co-director of the Language Research Center at Georgia State University, whose early research in capuchin monkeys found a clear rejection of "unequal pay," said the German primate study added another dimension to previous findings.

That the monkeys focused on the human "suggests that this is a social response," said Brosnan, who was not involved in the German research.

"To use a crude analogy, if someone issues me a smaller paycheck than you for the same work, I’m going to be upset with them, but if the printer has an error and prints my check for less, I’m not going to feel that it was inequitable," she said.

Frans de Waal, director of the Living Links Center and C. H. Candler professor of psychology at Emory University, who conducted many of the early fairness experiments in monkeys — including the one with the cucumber-flinging monkey — said the response of the macaques in the German study was "remarkable."

Macaques have not shown an aversion to inequity until now; they are hierarchical, he said, which may indicate an acceptance of inequality. "The reaction is mostly to human distribution, but at least there is a reaction," said de Waal, who was not involved in the German research.

He said he did not know what the German study's findings mean for the "reaction patterns of more cooperative, less hierarchical species" such as capuchin monkeys "and if the findings of this study can be extended."

"Capuchin monkeys, which were in the original study, have been tested with an empty cage next to them and react more strongly if high-value food goes to a partner than to an empty cage," de Waal said, "so social comparison still seems a good explanation" for their behavior.

The German study is in line with previous research about chimpanzees by Jan Engelmann, assistant professor of psychology at the University of California at Berkeley.

"The striking thing to me is that macaques seem to form special expectations toward other social beings, for example, to be treated nicely by a human being, which they do not form toward machines," said Engelmann, who was not part of the German study.

He said it also was interesting for "machine-human interactions."

"Differentiating between machines and other social animate beings seems to be deeply rooted in our evolution," Engelmann said. The macaques "seem to understand that handing over the bad food is an expression of ill-will by the human experimenter, but not by the machine," he said.

Titchener said that to understand the behavior of the macaques, it would be helpful to know "what it is about the human that the animals are reacting to, that is, what characteristics of the human are important."

Stefanie Keupp, a postdoctoral scientist in the German Primate Center's Cognitive Ethology Laboratory, and lead author of the study, cautioned that animal behavior research has limits.

"We cannot ask our nonhuman primate subjects how they perceive an experimental situation, we can only observe their behavior," she said, and "need to avoid falling into the trap of viewing animal behavior without context, through a human lens."

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