Just as my office would not stay empty for long were I to move out, nature's real estate changes hands all the time. Potential homes range from holes drilled by woodpeckers to empty shells on the beach. A typical example of what economists call a vacancy chain is the housing market among hermit crabs. To protect its soft abdomen, each crab carries its house around, usually an abandoned gastropod shell. The problem is that the crab grows, whereas its house does not. Hermit crabs are always on the lookout for new accommodations. The moment they upgrade to a roomier shell, other crabs line up for the vacated one.
One can easily see supply and demand at work here, but because it plays itself out on a rather impersonal level, few would view the crab version as related to human economic transactions. The crab interactions would be more interesting if the animals struck deals along the lines of you can have my house if I can have that dead fish. Hermit crabs are not deal makers, though, and in fact have no qualms about evicting homeowners by force. Other, more social animals do negotiate, however, and their approach to the exchange of resources and services helps us understand how and why human economic behavior may have evolved.
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CLASSICAL ECONOMICS views people as profit maximizers driven by pure selfishness. As 17th-century English philosopher Thomas Hobbes put it, Every man is presumed to seek what is good for himselfe naturally, and what is just, only for Peaces sake, and accidentally. In this still prevailing view, sociality is but an afterthought, a social contract that our ancestors entered into because of its benefits, not because they were attracted to one another. For the biologist, this imaginary history falls as wide off the mark as can be. We descend from a long line of group-living primates, meaning that we are naturally equipped with a strong desire to fit in and find partners to live and work with. This evolutionary explanation for why we interact as we do is gaining influence with the advent of a new school, known as behavioral economics, that focuses on actual human behavior rather than on the abstract forces of the marketplace as a guide for understanding economic decision making. In 2002 the school was recognized by a shared Nobel Prize for two of its founders: Daniel Kahneman and Vernon L. Smith.
The Evolution of Reciprocity
ANIMALS AND PEOPLE occasionally help one another without any obvious benefits for the helper. How could such behavior have evolved? If the aid is directed at a family member, the question is relatively easy to answer. Blood is thicker than water, we say, and biologists recognize genetic advantages to such assistance: if your kin survive, the odds of your genes making their way into the next generation increase. But cooperation among unrelated individuals suggests no immediate genetic advantages. Ptr Kropotkin, a Russian prince, offered an early explanation in his book Mutual Aid, published in 1902. If helping is communal, he reasoned, all parties stand to gain--everyone's chances for survival go up. We had to wait until 1971, however, for Robert L. Trivers, then at Harvard University, to phrase the issue in modern evolutionary terms with his theory of reciprocal altruism.
Trivers contended that making a sacrifice for another pays off if the other later returns the favor. Reciprocity boils down to I'll scratch your back, if you scratch mine. Do animals show such tit for tat? Monkeys and apes form coalitions; two or more individuals, for example, gang up on a third. And researchers have found a positive correlation between how often A supports B and how often B supports A. But does this mean that animals actually keep track of given and received favors? They may just divide the world into buddies, whom they prefer, and nonbuddies, whom they care little about. If such feelings are mutual, relationships will be either mutually helpful or mutually unhelpful. Such symmetries can account for the reciprocity reported for fish, vampire bats (which regurgitate blood to their buddies), dolphins and many monkeys.
Just because these animals may not keep track of favors does not mean they lack reciprocity. The issue rather is how a favor done for another finds its way back to the original altruist. What exactly is the reciprocity mechanism? Mental record keeping is just one way of getting reciprocity to work, and whether animals do this remains to be tested. Thus far chimpanzees are the only exception. In the wild, they hunt in teams to capture colobus monkeys. One hunter usually captures the prey, after which he tears it apart and shares it. Not everyone gets a piece, though, and even the highest-ranking male, if he did not take part in the hunt, may beg in vain. This by itself suggests reciprocity: hunters seem to enjoy priority during the division of spoils. To try to find the mechanisms at work here, we exploited the tendency of these apes to share--which they also show in captivity--by handing one of the chimpanzees in our colony a watermelon or some branches with leaves. The owner would be at the center of a sharing cluster, soon to be followed by secondary clusters around individuals who had managed to get a major share, until all the food had trickled down to everyone. Claiming another's food by force is almost unheard of among chimpanzees--a phenomenon known as respect of possession. Beggars hold out their hand, palm upward, much like human beggars in the street. They whimper and whine, but aggressive confrontations are rare. If these do occur, the possessor almost always initiates them to make someone leave the circle. She whacks the offenders over the head with a sizable branch or barks at them in a shrill voice until they leave her alone. Whatever their rank, possessors control the food flow.
We analyzed nearly 7,000 of these approaches, comparing the possessor's tolerance of specific beggars with previously received services. We had detailed records of grooming on the mornings of days with planned food tests. If the top male, Socko, had groomed May, for example, his chances of obtaining a few branches from her in the afternoon were much improved. This relation between past and present behavior proved general. Symmetrical connections could not explain this outcome, as the pattern varied from day to day. Ours was the first animal study to demonstrate a contingency between favors given and received. Moreover, these food-for-grooming deals were partner-specific--that is, May's tolerance benefited Socko, the one who had groomed her, but no one else.
This reciprocity mechanism requires memory of previous events as well as the coloring of memory such that it induces friendly behavior. In our own species, this coloring process is known as gratitude, and there is no reason to call it something else in chimpanzees. Whether apes also feel obligations remains unclear, but it is interesting that the tendency to return favors is not the same for all relationships. Between individuals who associate and groom a great deal, a single grooming session carries little weight. All kinds of daily exchanges occur between them, probably without their keeping track. They seem instead to follow the buddy system discussed before. Only in the more distant relationships does grooming stand out as specifically deserving reward. Because Socko and May are not close friends, Socko's grooming was duly noticed.
A similar difference is apparent in human behavior, where we are more inclined to keep track of give-and-take with strangers and colleagues than with our friends and family. In fact, scorekeeping in close relationships, such as between spouses, is a sure sign of distrust.
Biological Markets
BECAUSE RECIPROCITY requires partners, partner choice ranks as a central issue in behavioral economics. The hand-me-down housing of hermit crabs is exceedingly simple compared with the interactions among primates, which involve multiple partners exchanging multiple currencies, such as grooming, sex, support in fights, food, babysitting and so on. This marketplace of services, as I dubbed it in Chimpanzee Politics, means that each individual needs to be on good terms with higher-ups, to foster grooming partnerships and--if ambitious--to strike deals with like-minded others. Chimpanzee males form coalitions to challenge the reigning ruler, a process fraught with risk. After an overthrow, the new ruler needs to keep his supporters contented: an alpha male who tries to monopolize the privileges of power, such as access to females, is unlikely to keep his position for long. And chimps do this without having read Niccol Machiavelli.
With each individual shopping for the best partners and selling its own services, the framework for reciprocity becomes one of supply and demand, which is precisely what Ronald No and Peter Hammerstein, then at the Max Planck Institute for Behavioral Physiology in Seewiesen, Germany, had in mind with their biological market theory. This theory, which applies whenever trading partners can choose with whom to deal, postulates that the value of commodities and partners varies with their availability. Two studies of market forces elaborate this point: one concerns the baby market among baboons, the other the job performance of small fish called cleaner wrasses.
Like all primate females, female baboons are irresistibly attracted to infants--not only their own but also those of others. They give friendly grunts and try to touch them. Mothers are highly protective, however, and reluctant to let anyone handle their precious newborns. To get close, interested females groom the mother while peeking over her shoulder or underneath her arm at the baby. After a relaxing grooming session, a mother may give in to the groomer's desire for a closer look. The other thus buys infant time. Market theory predicts that the value of babies should go up if there are fewer around. In a study of wild chacma baboons in South Africa, Louise Barrett of the University of Liverpool and Peter Henzi of the University of Central Lancashire, both in England, found that, indeed, mothers of rare infants were able to extract a higher price (longer grooming) than mothers in a troop full of babies.
Cleaner wrasses (Labroides dimidiatus) are small marine fish that feed on the external parasites of larger fish. Each cleaner owns a station on a reef where clientele come to spread their pectoral fins and adopt postures that offer the cleaner a chance to do its job. The exchange exemplifies a perfect mutualism.
The cleaner nibbles the parasites off the client's body surface, gills and even the inside of its mouth. Sometimes the cleaner is so busy that clients have to wait in line. Client fish come in two varieties: residents and roamers. Residents belong to species with small territories; they have no choice but to go to their local cleaner. Roamers, on the other hand, either hold large territories or travel widely, which means that they have several cleaning stations to choose from. They want short waiting times, excellent service and no cheating. Cheating occurs when a cleaner fish takes a bite out of its client, feeding on healthy mucus. This makes clients jolt and swim away.
Research on cleaner wrasses by Redouan Bshary of the Max Planck institute in Seewiesen consists mainly of observations on the reef but also includes ingenious experiments in the laboratory. His papers read much like a manual for good business practice. Roamers are more likely to change stations if a cleaner has ignored them for too long or cheated them. Cleaners seem to know this and treat roamers better than they do residents. If a roamer and a resident arrive at the same time, the cleaner almost always services the roamer first. Residents have nowhere else to go, and so they can be kept waiting. The only category of fish that cleaners never cheat are predators, who possess a radical counterstrategy, which is to swallow the cleaner. With predators, cleaner fish wisely adopt, in Bshary's words, an unconditionally cooperative strategy.
Biological market theory offers an elegant solution to the problem of freeloaders, which has occupied biologists for a long time because reciprocity systems are obviously vulnerable to those who take rather than give. Theorists often assume that offenders must be punished, although this has yet to be demonstrated for animals. Instead cheaters can be taken care of in a much simpler way. If there is a choice of partners, animals can simply abandon unsatisfactory relationships and replace them with those offering more benefits. Market mechanisms are all that is needed to sideline profiteers. In our own societies, too, we neither like nor trust those who take more than they give, and we tend to stay away from them.
Fair Is Fair
TO REAP THE BENEFITS of cooperation, an individual must monitor its efforts relative to others and compare its rewards with the effort put in. To explore whether animals actually carry out such monitoring, we turned again to our capuchin monkeys, testing them in a miniature labor market inspired by field observations of capuchins attacking giant squirrels. Squirrel hunting is a group effort, but one in which all rewards end up in the hands of a single individual: the captor. If captors were to keep the prey solely for themselves, one can imagine that others would lose interest in joining them in the future. Capuchins share meat for the same reason chimpanzees (and people) do: there can be no joint hunting without joint payoffs.
We mimicked this situation in the laboratory by making certain that only one monkey (whom we called the winner) of a tray-pulling pair received a cup with apple pieces. Its partner (the laborer) had no food in its cup, which was obvious from the outset because the cups were transparent. Hence, the laborer pulled for the winner's benefit. The monkeys sat side by side, separated by mesh. From previous tests we knew that food possessors might bring food to the partition and permit their neighbor to reach for it through the mesh. On rare occasions, they push pieces to the other.
We contrasted collective pulls with solo pulls. In one condition, both animals had a pull bar and the tray was heavy; in the other, the partner lacked a bar and the winner handled a lighter tray on its own. We counted more acts of food sharing after collective than solo pulls: winners were in effect compensating their partners for the assistance they had received. We also confirmed that sharing affects future cooperation. Because a pair's success rate would drop if the winner failed to share, payment of the laborer was a smart strategy.
Sarah F. Brosnan, one of my colleagues at Yerkes, went further in exploring reactions to the way rewards are divided. She would offer a capuchin monkey a small pebble, then hold up a slice of cucumber as enticement for returning the pebble. The monkeys quickly grasped the principle of exchange. Placed side by side, two monkeys would gladly exchange pebbles for cucumber with the researcher. If one of them got grapes, however, whereas the other stayed on cucumber, things took an unexpected turn. Grapes are much preferred. Monkeys who had been perfectly willing to work for cucumber suddenly went on strike. Not only did they perform reluctantly seeing that the other was getting a better deal, but they became agitated, hurling the pebbles out of the test chamber and sometimes even the cucumber slices. A food normally never refused had become less than desirable.
To reject unequal pay--which people do as well--goes against the assumptions of traditional economics. If maximizing benefits were all that mattered, one should take what one can get and never let resentment or envy interfere. Behavioral economists, on the other hand, assume evolution has led to emotions that preserve the spirit of cooperation and that such emotions powerfully influence behavior. In the short run, caring about what others get may seem irrational, but in the long run it keeps one from being taken advantage of. Discouraging exploitation is critical for continued cooperation.
It is a lot of trouble, though, to always keep a watchful eye on the flow of benefits and favors. This is why humans protect themselves against freeloading and exploitation by forming buddy relationships with partners--such as spouses and good friends--who have withstood the test of time. Once we have determined whom to trust, we relax the rules. Only with more distant partners do we keep mental records and react strongly to imbalances, calling them unfair.
We found indications for the same effect of social distance in chimpanzees. Straight tit for tat, as we have seen, is rare among friends who routinely do favors for one another. These relationships also seem relatively immune to inequity. Brosnan conducted her exchange task using grapes and cucumbers with chimpanzees as well as capuchins. The strongest reaction among chimpanzees concerned those who had known one another for a relatively short time, whereas the members of a colony that had lived together for more than 30 years hardly reacted at all. Possibly, the greater their familiarity, the longer the time frame over which chimpanzees evaluate their relationships. Only distant relations are sensitive to day-to-day fluctuations.
All economic agents, whether human or animal, need to come to grips with the freeloader problem and the way yields are divided after joint efforts. They do so by sharing most with those who help them most and by displaying strong emotional reactions to violated expectations. A truly evolutionary discipline of economics recognizes this shared psychology and considers the possibility that we embrace the golden rule not accidentally, as Hobbes thought, but as part of our background as cooperative primates.
THE AUTHOR
FRANS B. M. DE WAAL is C. H. Candler Professor of Primate Behavior at Emory University and director of the Living Links Center at the university's Yerkes National Primate Research Center. De Waal specializes in the social behavior and cognition of monkeys, chimpanzees and bonobos, especially cooperation, conflict resolution and culture. His books include Chimpanzee Politics, Peacemaking among Primates, The Ape and the Sushi Master and the forthcoming Our Inner Ape.