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Do chimpanzees care about fairness? The jury’s out

A stranger gets a pot of money and offers you a share of it. If you accept the offer, both of you walk away with your proposed shares. If you reject, you both leave with nothing.

This is the ultimatum game—a classic psychological experiment used to study fair play. If both players behave completely selfishly, the proposer might offer as little as possible, while the responder should accept any offer as long as it’s not zero. That way, both of them walk away with something. In practice, responders typically reject any offers less than 20 percent. They care enough about fairness to do themselves out of money in order to punish unfair partners. Meanwhile, proposers from industrialised countries, who are wary of social norms and the potential for punishment, tend to offer between 40 and 50 percent of the pot.

But what about chimpanzees? Do our closest relatives also share our attitudes to equality? Darby Proctor from Georgia State University thinks so. She modified the ultimatum game so that chimps and human children could play it in the same way. In both cases, when proposers needed to cooperate with responders, they became more likely to offer an equal split, rather than trying to hog the rewards for themselves. The conclusion: “humans and chimpanzees show similar preferences regarding reward division, suggesting a long evolutionary history to the human sense of fairness.”

But her study has prompted stern criticism from scientists who have also tested chimps at the ultimatum game and found the opposite. In their studies, our fellow apes did not make fair offers and accepted anything as long as it was greater than zero.

This debate reflects a growing divide between scientists who study chimpanzees, but it is more than an academic spat. It speaks to a fundamental question about our evolution: is our sense of fairness a uniquely human trait, or one that we share with our closest kin?

Old male chimp, by Prabir Kumar Bhattacharyya

The experiments

Keith Jensen, Josep Call and Michael Tomasello were the first to play the ultimatum game with chimps. In their experiments, two chimps sat in adjacent cages, facing a contraption with two sliding trays. Each tray contained one dish on the proposer’s side and another on the responder’s side, and the two dishes carried varying numbers of raisins. The proposer made an offer by using a rope to pull one of the two trays half-way over. The responder could accept this offer by pulling the tray the rest of the way, allowing them both to eat their respective raisins. Alternatively, they could reject the offer by doing nothing, leaving both animals unfed.

The team found that the proposers were likely to choose the tray that gave them the most raisins, and the responders tended to accept any offer, no matter how unbalanced. They wrote that “in this context, one of humans’ closest living relatives… does not share the human sensitivity to fairness.” And in a second study, the team found that our other close relatives—the bonobos—behaved in a similar way.

But Proctor was unimpressed by the team’s set-up. She felt that the “complex mechanical apparatus” was unlike anything that humans use when we play ultimatum games, and may have been too complicated for the chimps to understand. And while humans usually play for money, which is exchanged for other rewards, the chimps were playing for food, which is immediately rewarding.

In her version of the ultimatum game, two chimps play for tokens that are exchanged for six bananas laid out in front of them. A human experimenter offers two tokens to the proposer chimp, one signifying an equal banana split and the other signifying an unequal 5:1 divide. The proposer picks one token and passes it to a responder in an adjoining cage. They can drop the token to reject the offer, or pass it back to the experimenter to accept.

Proctor played the game with three pairs of chimps, one of which swapped roles as proposer and responder. She found that two of the proposers chose the equal-split token more often than expected by chance. And all four of them chose that token more often in the ultimatum game than in a straight preference test, when their choice dictated their reward irrespective of what a responder did. Proctor concluded that when chimps need to cooperate to get a reward—that is, when the proposer depends on the responder—they change their behaviour to favour the fairer option. Young children, aged two to seven, behaved in the same way.

Margot, an orphaned chimpanzee from a sanctuary in Cameroon. By Daniel Bergin

So what does that mean?

The obvious criticism is that Proctor’s study only included six chimps, and only the two animals who played both roles offered the equal token more often than expected by chance. Proctor admits that the numbers were small, but says that these were the only chimps that passed her rigorous pre-tests and clearly understood the nature of the game.

But Jensen disputes Proctor’s claim. He is glad that another team tried to replicate his results, since “one can only conclude so much from one or two studies,” but says that Proctor’s experiment was no ultimatum game. The most important aspect of the ultimatum game is not what the proposer does, but how the responder reacts,” he says. The proposer’s offers are strategic rather than a sign of fairness—they’re a reaction to what the responder might do. It’s the responder’s ability to reject unequal offers that drives fairness in the game.

And among Proctor’s chimps, no responder ever refused an offer, even the many unfair ones. That’s even less rejection than in Jensen’s study. “Not rejecting unfair offers is puzzling if chimps are really playing the ultimatum game,” says Call. “I see that as a fatal flaw,” adds Jensen. At best, it confirms his original experiment by showing that the responders are insensitive to unfairness and only motivated by getting bananas. At worst, it shows that they didn’t understand the task.

Proctor counters that she did extensive tests to be as sure as possible that the chimps understood what the tokens meant. She admits that she did not explicitly train the chimps that they could refuse offers, but says, “This actually makes our results more striking. Without experiencing a refusal, proposers changed their behaviour to be more equitable. They may be responding to the potential for refusals as do adult humans.”

Jensen doesn’t buy it. “There isn’t the tiniest shred of evidence that proposers understood that responder could reject their offers, and no demonstration that responders understood anything of the possible consequences of their choices,” he says.

David Rand, a psychologist from Harvard University who has used the ultimatum game in human studies, agrees with Jensen’s criticisms. While Proctor’s set-up does look like an ultimatum game, “it looks like maybe the chimps didn’t understand the game structure,” he says.

Jensen thinks that this confusion arose because Proctor’s task is not as simple as she claims. Unlike human ultimatum games, where players interact with each other, Proctor’s chimps spent as much time exchanging tokens with humans. “Passing a token is just an intermediate step to getting food from experimenters, something they are highly trained to do,” says Jensen. He doubts that this set-up, which involved tokens exchanging hands three times, is truly simpler than his tray-pulling machine.

The verdict

As Proctor notes, there are many reasons to suspect that chimps care about equality. They help one another, share food, and cooperate extensively to hunt, fight, patrol, defend, and more. But it’s difficult to interpret wild anecdotal behaviour, which is why experiments are valuable.

None of the existing studies is perfect. In all the chimp ultimatum games, the animals could only reject offers passively, by not pulling a tray or not handing over a token; in human games, rejection is an active choice. In the chimp games, the animals could see each other, and played multiple rounds with the same partners; in human games, partners usually play single rounds anonymously to stop social dynamics and reputations from clouding the results.

Given these shared weaknesses, Proctor’s team is right that Jensen’s studies don’t prove that chimps are insensitive to fairness even though they support that hypothesis. After all, absence of evidence is not evidence for absence. But equally, the problems in Proctor’s study prevent it from confirming that chimps are sensitive to fairness. Until more research is done, we’re at an impasse.

Reference:  Proctor, Williamson, de Waal & Brosnan. 2013. Chimpanzees play the ultimatum game. PNAS http://dx.doi.org/10.1073/pnas.1220806110

Note: This study was “contributed” to PNAS by co-author Frans de Waal, a publishing route where members of the National Academy of Sciences can nominate their own peer-reviewers. I try to avoid papers that use this track but did most of the reporting before I noticed, so here’s the piece anyway.

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The development of fairness – egalitarian children grow into meritocratic teens

Children_fairnessTwo children, Anne and Carla, have worked together to make a cake and they have to split it between them. Anne says that she’s the bigger cake aficionado and deserves the lion’s share. But Carla demands the bigger slice since she did most of the cooking. A nosy third party, Brenda, argues that the only fair call would be for the two girls to split the cake equally. Which is the right path?

There’s no obvious right answer and different people will probably side with different viewpoints. Dilemmas like this have been the subject of much philosophical debate, and they’re a common part of everyday life. How do you allocate pay rises between your staff? How should the UK’s new government split its budget among its various departments?

According to Norwegian scientist Ingvild Almås, our attitudes to such questions change during our childhood and adolescence, as we start changing our opinions on what counts as ‘fair’. Children tend to shun any form of inequality – they’d agree with Brenda. But as they enter the turmoil of adolescence, they become more meritocratic and are happier to divide wealth according to individual achievements, as Carla suggested. As their teens draw to a close, they (like Anne) pay greater heed to efficiency, making choices of maximum benefit to the group.


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Clean smells promote generosity and fair play; dark rooms and sunglasses promote deceit and selfishness

The English language is full of metaphors linking moral purity to both physical cleanliness and brightness. We speak of “clean consciences”, “pure thoughts” and “dirty thieves”. We’re suspicious of “shady behaviour” and we use light and darkness to symbolise good and evil. But there is more to these metaphors than we might imagine. The mere scent of a clean-smelling room can take people down a virtuous road, compelling them to choose generosity over greed and charity over apathy. Meanwhile, the darkness of a dimmed room or a pair of sunglasses can compel people towards selfishness and cheating.

These new results are the latest from psychologist Chen-Bo Zhong. Back in 2006, he showed that people who brought back memories of past wrong-doings were more likely to think of words related to cleaning, or to physically crave cleaning products. He called this the “Lady Macbeth effect”. Subsequently, another group found that it works the other way too. People judge moral transgressions more leniently if they had previously washed their hands or if they had been primed with words related to cleanliness, like ‘pure’ or ‘immaculate’.

Now, Zhong, together with Katie Liljenquist and Adam Galinsky, have expanded on these studies by showing that clean smells can make people behave more virtuously. They ushered 28 volunteers into a room that was either unscented or that had been lightly sprayed with a citrus air freshener. In either case, they had to play a trust game, where a “sender” has a pot of money and chooses how much they want to invest with a “receiver”. The investment is tripled and the receiver decides how much to give back.

The volunteers were all told that they had been randomly chosen as receivers. Their anonymous partner had invested their entire $4 pot with them, which had been tripled to $12. Their job was to decide how much to give back. On average, they returned a measly $2.81in the unscented rooms but a more equitable $5.33 in the scented ones. The single spray of citrus nearly doubled their tendency to reciprocate.

In a second experiment, the trio again ushered 99 students into either a scented or unscented room. They were given a pack of miscellaneous tasks, including a flyer requesting volunteers for a charity called Habitat for Humanity. Those in the citrus-scented rooms were more likely to be interested in volunteering, and almost four times more willing to donate money to the cause.


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Prejudice vs. biology – testosterone makes people more selfish, but only if they think it does

What do you think a group of women would do if they were given a dose of testosterone before playing a game? Our folk wisdom tells us that they would probably become more aggressive, selfish or antisocial. Well, that’s true… but only if they think they’ve been given testosterone.

Hulk.jpgIf they don’t know whether they’ve been given testosterone or placebo, the hormone actually has the opposite effect to the one most people would expect – it promotes fair play. The belligerent behaviour stereotypically linked to testosterone only surfaces if people think they’ve been given hormone, whether they receive a placebo or not. So strong are the negative connotations linked to testosterone that they can actually overwhelm and reverse the hormone’s actual biological effects.

If ever a hormone was the subject of clichés and stereotypes, it is testosterone. In pop culture, it has become synonymous with masculinity, although women are subject to its influence too. Injections of testosterone can make lab rats more aggressive, and this link is widely applied to humans. The media portrays “testosterone-charged” people as sex-crazed and financially flippant and the apparent link with violence is so pervasive that the use of steroids has even been used as a legal defence in a US court.

Christoph Eisenegger from the University of Zurich tested this folk wisdom by enrolling 60 women in a double-blind randomised controlled trial. They were randomly given either a 0.5 milligram drop of testosterone or a placebo. He only recruited women because previous research shows exactly how much testosterone you need to have an effect, and how long it takes to do so. We don’t know that for men.

The women couldn’t have known which substance they were given, but Eisenegger asked them to guess anyway. Their answers confirmed that they couldn’t tell the difference between the two drops. But they would also confirm something more startling by the trial’s end.

Each woman was paired with a partner (from another group of 60) and played an “Ultimatum game” for a pot of ten Swiss francs. One woman, the “proposer”, decided how to allocate it and her partner, “the responder” could choose to accept or refuse the offer. If she accepts, the money is split as suggested and if she refuses, both players go empty-handed. The fairest split would be an equal one but from the responder’s point of view, any money would be better than nothing. The game rarely plays out like that though – so disgusted are humans with unfairness that responders tend to reject low offers, sacrificing their own meagre gains to spite their proposers.

Overall, Eisenegger found that women under the influence of testosterone actually offered more money to their partners than those who received the placebo. The effect was statistically significant and it’s exactly the opposite of the selfish, risk-taking, antagonistic behaviour that stereotypes would have us predict.

Those behaviours only surfaced if women thought they had been given testosterone. Those women made lower offers than their peers who believed they had tasted a placebo, regardless of which drop they had been given. The amazing thing is that this negative ‘imagined’ effect actually outweighed the positive ‘real’ one. On average, a drop of testosterone increased a proposer’s offer by 0.6 units, but belief in the hormone’s effects reduced the offer by 0.9 units.

The difference between these values is not statistically significant, so we can’t conclude that the negative effect outweighs the positive one, but the two are certainly comparable. Either way, it is a staggering result. It implies that the biological effect of a behaviour-altering hormone can be masked, if not reversed, by what we think it does. It’s somewhat similar to the nocebo effect, where people experience unwanted side effects from a drug because they believe that such effects will happen.



How can we explain these results? Certainly, Eisenegger accounted for the volunteers’ levels of testosterone before the experiment, as well as their levels of cortisol (a stress hormone), their mood and their feelings of anxiety, anger, calmness or wakefulness. None of these factors affected his results.

It’s possible that people who are naturally inclined towards selfish, aggressive or dominant behaviour would find it easier to rationalise their actions if they felt that they were under the spell of testosterone. However, these personality traits weren’t any more common among the recruits who thought they were given testosterone than those who thought they had a placebo.

Instead, Eisenegger suggests that testosterone’s negative stereotype provided some of the women with a licence to misbehave. Their beliefs relieved them from the responsibility of making socially acceptable offers because they thought they would be driven to make greedy ones.

At first, this work seems to contradict the results from earlier studies, which suggest that high testosterone levels are linked with risk-taking, selfishness and aggression. But these studies can’t tell us whether the former causes the latter. Indeed, another randomised trial that I’ve blogged about before found that doses of testosterone didn’t affect a woman’s selflessness, trust, trustworthiness, fairness or attitude to risk. This study also used an Ultimatum game but it only analysed the behaviour of the responder rather than the proposer.

The alternative hypothesis says that testosterone plays a much subtler role in shaping our social lives. When our social status is challenged, testosterone drives us to increase our standing; how we do that depends on the situation. Traders might take bigger financial risks, while prisoners might have a dust-up.  Eisenegger thinks that this is the right explanation, and his results support his view. In his experiment, women who received testosterone would be more inclined towards acts that boosted their social status, and the best way of doing that was to make a fair offer.

The message from this study is clear, and Eisenegger sums it up best himself:

“Whereas other animals may be predominantly under the influence of biological factors such as hormones, biology seems to exert less control over human behaviour. Our findings also teach an important methodological lesson for future studies: it is crucial to control for subjects’ beliefs because the [effect of a pure substance] may be otherwise under- or overestimated.”

Reference: Nature doi:10.1038/nature08711

More on hormones and placebo:


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Genes affect our likelihood to punish unfair play

This article is reposted from the old WordPress incarnation of Not Exactly Rocket Science. The blog is on holiday until the start of October, when I’ll return with fresh material.

As a species, we value fair play. We’re like it so much that we’re willing to eschew material gains in order to punish cheaters who behave unjustly. Psychological games have set these maxims in stone, but new research shows us that this sense of justice is, to a large extent, influenced by our genes.

When it comes to demonstating our innate preference for fair play, psychologists turn to the ‘Ultimatum Game‘, where two players bargain over a pot of money. The ‘proposer’ suggests how the money should be divided and the ‘receiver’ can accept of refuse the deal. If they refuse, neither player gets anything and there is no room for negotiation. In a completely rational setting, the proposer should offer the receiver as little as possible, and the receiver should take it – after all, a very little money is better than none at all.

Of course, that’s not what happens. Receivers typically abhor unfair offers and would rather that both parties receive no money than accept a patronisingly tiny amount. Across most Western countries, proposers usually offer the receivers something between 40% and 50% of the takings. Any offers under 10% are almost always rejected.

The uniformity of responses across Western countries suggests that culture has a strong effect on how people play the game, but until now, no one had looked to see how strongly genes asserted their influence. Bjorn Wallace and colleagues from the Stockholm School of Economics decided to do just that, and they used the classic experiment for working out heritability – the twin study.


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Do testosterone and oestrogen affect our attitudes to fairness, trust, risk and altruism?

Blogging on Peer-Reviewed ResearchSome people go out of their way to help their peers, while others are more selfish. Some lend their trust easily, while others are more suspicious and distrustful. Some dive headlong into risky ventures; others shun risk like visiting in-laws. There’s every reason to believe that these differences in behaviour have biological roots, and some studies have suggested that they are influenced by sex hormones, like testosterone and oestrogen.

Roulette.jpgIt’s an intriguing idea, not least because men and women have very different levels of these hormones. Could that explain differences in behaviour between the two sexes? Certainly, several studies have found links between people’s levels of sex hormones and their behaviour in psychological experiments. But to Niklas Zethraeus and colleagues from the Stockholm School of Economics, this evidence merely showed that the two things were connected in some way – they weren’t strong enough to show that sex hormones were directly influencing behaviour.

To get a clearer answer, Zethraeus set up a clinical trial. He recruited 200 women, between 50-65 years of age, and randomly split them into three groups – one took tablets of oestrogen, the second took testosterone tablets and the third took simply sugar pills.

After four weeks of tablets, the women took part in a suite of psychological games, where they had the chance to play for real money. The games were designed to test their selflessness, trust, trustworthiness, fairness and attitudes to risk. If sex hormones truly change these behaviours, the three groups of women would have played the games differently. They didn’t.

Their levels of hormones had changed appropriately. At the end of the four weeks, the group that dosed up on oestrogen had about 8 times more than they did at the start, but normal levels of testosterone. Likewise, the testosterone-takers had 4-6 time more testosterone and free testosterone (the “active” fraction that isn’t attached to any proteins) but normal levels of oestrogen. The sugar-takers weren’t any different. Despite these changes, the women didn’t play the four psychological games any differently.


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Dogs frown on unfair rewards

Blogging on Peer-Reviewed ResearchIf a colleague of yours was rewarded for their work while you received nothing for your (similarly sized) efforts, you would probably be quite peeved. Now it seems that man’s best friend also shares our disdain for unfairness.

Humans are notorious for our dislike of injustice. It rankles us to see others being rewarded or penalised unfairly. We not only have the capacity to recognise when someone else is being rewarded beyond their efforts, but the inclination to punish them for it, often at personal expense. But other species behave in the same way – recent studies have found that capuchin monkeys and chimpanzees also have the ability to compare their payoffs and efforts to those of their peers, and they too frown on unequal rewards.

Now, Friederike Range from the University of Vienna has found that dogs may also share the distaste for inequity that primates seem to have, although to a much simpler degree. Together with colleagues from Austria, Range compared the reactions of pairs of dogs as they were rewarded with food for giving their paws to a human partner.

When both dogs were rewarded with a piece of dark bread, both offered their paws for the vast majority of 30 trials. But if one was rewarded and the other not, the spurned animal stopped cooperating at some point and on average, they only offered their paw in two-thirds of the trials. They were also visibly more distressed, scratching themselves, yawning and avoiding the gazes of their partners. And when they did play along, they did so more hesitantly, making Range ask for their paws more often before they gave in.



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The right side of fair play


Blogging on Peer-Reviewed ResearchA stranger walks up to you and a friend and offers to give you both £100. As always, there is a catch – your friend must choose how to split the money between you. Accept his offer, and you both keep your respective shares; reject it, and you both come away empty-handed. Now imagine your friend offered you a single pound. What do you do? Most people would reject the offer to spite the friend. Even though you would financially better off if you accepted, you friend’s proposal is unfair and rather insulting. Clearly, economic status is not the only thing at stake here.

old-bailey.jpgPsychologists use this ‘Ultimatum Game‘ to investigate the role of justice in human interactions and the results are very consistent. Usually, people who are offered a quarter of the stake or less will reject it, even if the sum is several months’ income (a rare case of justice triumphing over capitalism!)

Human beings seem to be strongly motivated by a social sense of justice. Those that play fairly are rewarded, and those that don’t, like you friend here, are punished. Now, Daria Knoch and colleagues at the University of Zurich have discovered that this desire for justice is influenced by a small part of the brain – the dorsolateral prefrontal cortex or DLPFC – which constantly suppresses our more selfish urges.


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Children learn to share by age 7-8

Blogging on Peer-Reviewed Research Yesterday, I wrote about selfless capuchin monkeys, who find personal reward in the act of giving other monkeys. The results seemed to demonstrate that monkeys are sensitive to the welfare of their peers, and will make choices that benefit others without any material gain for themselves. Today, another study looks at the same processes in a very different sort of cheeky monkey – human children.

Sharingsweets.jpgHumans are notable among other animals for our vast capacity for cooperation and empathy. Our concern about the experiences of other people, and our natural aversion to unfair play are the bedrocks on which our societies and moral codes are built. But are we born with this penchant for equality or does it develop as we grow up?

To find out, Ernst Fehr from the University of Zurich played a series of three decision-making games with 229 children between the ages of 3 and 8. The study used similar methods to those employed by Frans de Waal in his experiments on capuchins, but with some notable differences. For a start, the choices were anonymous. In each trial, a child had to decide between two ways of distributing sweets between themselves and a second child, who was only ever represented by a photo.


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Selfless monkeys find personal reward in helping others

Blogging on Peer-Reviewed ResearchThere are some who say that helping others is its own reward, and many biologists would agree. The fact that selfless acts give us a warm glow is evident from personal experience and neurological studies, which find that good deeds trigger activity in parts of the brain involved in feelings of reward. But feeling food by being good isn’t just the province of humans – monkeys too get a kick out of the simple act of giving to their fellow simians.

Capuchins.pngAt the Yerkes National Primate Research Center, Frans de Waal‘s team of scientists have been investigating the selfless side of eight brown capuchin monkeys. Each monkey was given a choice between two differently coloured tokens. Both would earn it a rewarding piece of apple but only one token would net a slice for a second monkey sitting in an adjacent transparent compartment.

The chooser would benefit equally no matter what choice they made, so if they were completely cold to the needs of their peers, you would expect them to pick both tokens with equal frequency. Otherwise, the “prosocial” token which benefited a second monkey would be the favoured pick. Everything else begin equal, would the monkeys take the welfare of their fellows into account?


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Why cooperation is hard for people with borderline personality disorder

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Social lives are delicate things. We’ve all had situations where friendships and relationships have been dented and broken, and we’re reasonably skilled at repairing the damage. This ability to keep our social ties from snapping relies on being able to read other people, and on knowing a thing or two about what’s normal in human society.

Fatalattraction.jpgFor instance, we appreciate that cheating fosters ill-will, while generosity can engender trust. So cheaters might try to win back their companions with giving gestures. These little exchanges are the glue that bind groups of people into happy and cooperative wholes. Now, a new study uses psychological games and brain scans to show what happens when they go amiss.

Brooks King-Casas at Baylor College of Medicine used a simple game to compare the social skills of healthy volunteers with those of people diagnosed with psychiatric condition called borderline personality disorder (BPD). People who suffer from BPD show erratic mood-swings and find it difficult to trust and understand the motives of others. As a result, they suffer from fraught personal relationships with friends, colleagues and partners.

So it was in the games. Each one was played by two players, an investor and a trustee, over the course of 10 rounds. The investor was given a princely sum of $20 and could split as much of it as they liked with the trustee. This investment was tripled and the trustee could then decide how much to return to the investor. Trust and cooperation is essential if both players are to benefit. The investor can make the most money by trusting the trustee with a sizeable share, on the assumption that some of it will find its way back. If the trustee violates that agreement, they are likely to get smaller investments in future rounds.