Empathy and Fairness: Psychological Mechanismsfor Eliciting and Maintaining Prosocialityand Cooperation in Primates

Shinya Yamamoto • Ayaka Takimoto

Published online: 9 August 2012

� Springer Science+Business Media, LLC 2012

Abstract In the past, prosociality has been considered a hallmark of humans;

however, recently, accumulating data have empirically revealed that non-human

animals also show prosocial behavior. In situations in which animals cannot predict

return benefits, prosocial behavior is probably driven by other-regarding motivation.

A sense of fairness and empathy continue to draw attention as the most plausible

candidates for the psychological mechanisms underlying such prosocial behavior. In

this article, we first introduce comparative studies on prosocial behavior in non-

human primates and discuss similarities and differences between humans and non-

human primates. Then, we discuss the role of a sense of fairness and empathy. In

this paper, we hypothesize that empathy may promote prosocial behavior, whereas a

sense of fairness may play a role as a stabilizer, but not as a promoter of prosocial

behavior in non-human animals. We further hypothesize that prosocial behavior

motivated by sympathetic concerns can survive only with a sense of fairness, the

inhibitory system for unnecessarily excessive expression of prosocial behavior.

Without a sense of fairness, empathic animals might be exploited by free-riders,

which might lead to the extinction of cooperation. Therefore, the interplay of a

sense of fairness and empathy are both important to maintaining prosocial behavior

and cooperation. This hypothesis seems to be supported by comparative studies with

non-human primates and also by neural studies with humans.

S. Yamamoto (&)

Primate Research Institute, Kyoto University, 41 Kanrin, Inuyama, Aichi 484-8506, Japan

e-mail: shinyayamamoto1981@gmail.com

A. Takimoto

Graduate School of Letters, Kyoto University, Yoshida-honmachi, Sakyo, Kyoto 606-8501, Japan

A. Takimoto

Japan Society for the Promotion of Science, 8 Ichibancho, Chiyoda, Tokyo 102-8472, Japan

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DOI 10.1007/s11211-012-0160-0

Keywords Prosociality � Cooperation � Helping � Fairness � Inequity aversion �Empathy � Understanding of others

Introduction

In this pair of special issues, ‘‘Justice in animals,’’ a sense of fairness that appears in

the form of a behavioral response of inequity is the central discussion topic. Why

has fairness drawn so much attention? It may be because fairness is closely related

to human cooperation and prosociality. Although, in classic economic theories

people are assumed to be exclusively motivated by their own self-interest,

researchers have noticed that in actuality, humans are also strongly motivated by

other-regarding preferences, or interest in others’ outcomes. From this perspective,

fairness has become the focus of modern economic theories explaining human

prosociality (Fehr & Schmidt, 1999). If this is the case in humans, it may also be

true in other species that have recently been shown to demonstrate prosocial

behavior. Thus, non-human animals as well as humans have become a target for

investigation of a sense of fairness, and researchers have devoted efforts to finding

the evolutionary link among prosociality, cooperation, and fairness (Brosnan, 2011).

We place prosociality at the center of the discussion in this article. Prosocial

behavior refers to ‘‘voluntary actions that are intended to help or benefit another

individual or group of individuals’’ (Eisenberg & Mussen, 1989). This definition

refers to the consequences of a donor’s actions rather than the motivations behind

those actions. These behaviors include a broad range of activities, such as: sharing,

comforting, rescuing, and helping. If there is a cost to the actor, then the behavior

can be labeled as altruistic behavior; therefore, prosocial behavior includes altruistic

behavior (Yamamoto & Tanaka, 2009a).

Previously, the evolution of prosocial behavior was mainly explained from an

ultimate perspective, i.e., the cost–benefit balance of the behavioral consequence.

Recently, however, prosocial behavior has been analyzed from the proximate

viewpoint of psychological mechanisms (Brosnan, 2011; de Waal, 2008; Preston &

de Waal, 2002). From an ultimate perspective, it is argued that prosocial behavior

might subsequently bring some benefits to the actor, such as through reciprocal

interaction (Trivers, 1971) and helping kin (Hamilton, 1964). However, the

underlying motivations are not necessarily based on self-interest. When an

individual cannot predict any return benefit, the prosocial behavior must be driven

by other-regarding motivations (de Waal, 2008; de Waal & Suchak, 2010).

Empathy, the ability to share the feelings and emotions of others, as well as a sense

of fairness, are considered to be the most plausible underlying psychological

mechanisms of this other-regarding behavior.

Here, we also define another closely related term, ‘‘cooperation.’’ This word has

acquired two different meanings, which has caused some confusion among

researchers in different fields. In some disciplines, such as primatology and

ethology, this term is often used as ‘‘collective action’’: the behavior of two or more

individuals acting together to achieve a common goal, typically in hunting context

(Busse, 1978; Boesch & Boesch, 1989) and bar- or rope-pulling cooperative tasks

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(Chalmeau, 1994; Crawford, 1937; Hirata & Fuwa, 2007). With this definition,

cooperation can be achieved by only self-regarding motives. In other research,

‘‘cooperation’’ is used in the analysis of individual behavior: an individual acts

cooperatively only if it benefits the long-term fitness (in terms of survival and

reproduction) of both itself and the recipient of its actions, even at the expense of its

own short-term fitness (Hamilton, 1964; Krebs and Davies, 1987; Maynard-Smith,

1982). Melis and Semmann (2010) adopted this term in broader sense along with

this line: behaviors which provide a benefit to a recipient or are beneficial to both

the actor and the recipient. In this usage, by definition, cooperation is compatible

with prosocial behavior. In this article, we follow this latter definition, and use

‘‘cooperation’’ when discussing reciprocal cooperation (i.e., reciprocal prosocial or

altruistic behavior). When we refer to cooperation based on the former meaning, we

use ‘‘collective action.’’

Previously, prosocial behavior, a sense of fairness, and empathy were considered

to be some of the hallmarks of humans. However, recently there has been

accumulating evidence for the existence of these traits in non-human animals as

well. In this article, we first introduce empirical studies suggesting similarities and

differences between humans and non-human animals in prosocial behavior and

mechanisms related to fairness and empathy. Following this, we discuss how each

of the two psychological traits, a sense of fairness and empathy, impact prosocial

behavior; finally, we also discuss the possible link between fairness and empathy.

Comparison of Studies on Prosociality with Human and Non-human Animals

Many non-human species in different taxa have recently been shown to demonstrate

prosocial behavior in the wild and captivity (de Waal, 2008; Dugatkin, 1997:

Kappeler & van Schaik, 2006; see also Price & Brosnan, 2012, previous issue and

Brauer & Hanus, 2012, current issue). Recently, two experimental paradigms have

been developed to empirically test non-human animals’ prosociality: one is a

prosocial choice paradigm and the other is a targeted helping (or instrumental

helping) paradigm.

In the prosocial choice paradigm, an animal is presented with opportunities to

provide benefits to others at little or no cost to themselves (Fig. 1a). The animal can

choose one of two options: one produces rewards to him/herself and a conspecific

partner (prosocial choice), and the other benefits only him/herself (selfish choice).

Whether the animal chooses the prosocial or selfish choice, he or she can obtain the

same amount of reward; therefore, giving a benefit to the partner by choosing the

prosocial option is not costly, although it may require a little labor (e.g., pulling a

bar connected to the food tray). This prosocial choice test is now one of the most

prevalent test paradigms applied to various species and has revealed considerable

species differences (Table 1). A prosocial tendency, i.e., the tendency for an actor to

choose the prosocial choice more frequently when the partner is present than absent,

has been observed in New World monkeys (capuchin monkeys: de Waal,

Leimgruber, & Greenberg, 2008; Lakshminarayanan & Santos, 2008; Takimoto &

Fujita, 2011; Takimoto, Kuroshima, & Fujita, 2010, common marmosets: Burkart,

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Fehr, Efferson, & van Schaik, 2007, cottontop tamarins: Cronin, Kori, & Showdon,

2010, but see also Cronin, Schroeder, Rothwell, Silk, & Snowdon, 2009; Stevens,

2010), and Old World monkeys (long-tailed macaques: Massen, van den Berg,

Spruijt, & Sterck, 2010). Bonobos, one of our closest living evolutionary relatives,

also showed prosociality in another experimental setting where they could choose to

share or not to share food with a conspecific partner (Hare & Kwetuenda, 2010).

Surprisingly, chimpanzees have demonstrated ‘‘indifference’’ to the others’ payoff

in most of the previous studies using this test paradigm, not discriminating

between the prosocial and the selfish options (Brosnan et al., 2009; Jensen, Hare,

Fig. 1 Two test paradigms fortesting animals’ prosocialbehavior. a Prosocial choice testanimals were presented with twooptions: one is just self-rewarding, and the other benefitsboth the actor and the partner. Inthis picture, a subject (right) ischoosing prosocial option (back)in which both the subject and therecipient received a high-valuereward (photograph by AyakaTakimoto). b Targeted helpingtest animals were tested whetherthey help others in predicament.In this picture, a chimpanzee(front) is giving a tool uponrequest to the partner who canthereafter use the tool to getotherwise out-of-reach reward.(photograph by ShinyaYamamoto)

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Call, & Tomasello, 2006; Silk et al., 2005; Vonk et al., 2008; Yamamoto & Tanaka,

2010; but see also Horner, Cartera, Suchak, & de Waal, 2011).

The targeted helping paradigm examines whether animals help other animals in

predicaments that they cannot resolve on their own (Fig. 1b). Results to date using

this paradigm have been seemingly incompatible with those using the prosocial

choice tests (Table 1). Besides humans, chimpanzees are the most helpful animals

in the targeted helping paradigm (Melis et al., 2010; Warneken & Tomasello, 2006;

Warneken, Hare, Melis, Hanus, & Tomasello, 2007; Yamamoto, Humle, & Tanaka,

2009, 2012). However capuchin monkeys, who have shown prosociality in the

prosocial choice paradigm, have demonstrated limited performance in the targeted

Table 1 Comparative studies with non-human primate species with two different prosocial test para-

digms and inequity aversion tests

Prosocial choice Targeted helping Inequity aversion

Chimpanzees Na Ph Pj

Bonobos Pb – ?k

Orangutans – – Nl

Long-tailed macaques Pc – Pm

Capuchin monkeys Pd Ni Pn

Cottontop tamarins Pe/Nf – Po

Common marmosets Pg – –

Squirrel monkeys – – Np

P mainly positive results, N mainly negative results

? difficult to interpret the result, – no empirical studya Brosnan et al. (2009), Jensen et al. (2006), Silk et al. (2005), Vonk et al. (2008), Yamamoto and Tanaka

(2010), but see also Horner et al. (2011)b Hare and Kwetuenda (2010)c Massen et al. (2010)d de Waal et al. (2008), Lakshminarayanan and Santos (2008), Takimoto and Fujita (2011), and

Takimoto et al. (2010)e Cronin et al. (2010)f Cronin et al. (2009) and Stevens (2010)g Burkart et al. (2007)h Melis et al. (2010), Warneken and Tomasello (2006), Warneken et al. (2007), and Yamamoto et al.

(2009)i Barnes et al. (2008) and Skerry et al. (2011)j Brosnan et al. (2005) and Brosnan, Talbot, et al., (2010)k Brauer et al. (2009); bonobos demonstrated highest rejection rate compared to chimpanzees and

orangutans, although this difference was not significant (possibly due to the small sample size; see the

discussion in Brosnan (2011)l Brauer et al. (2009) and Brosnan et al. (2011)m Massen et al. (2011)n Brosnan and de Waal (2003), Fletcher (2008), and van Wolkenten et al. (2007)o Neiworth et al. (2009)p Talbot et al. (2011)

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helping paradigm (Barnes, Martinez, Langer, Hill, & Santos, 2008; Skerry, Sheskin,

& Santos, 2011). Although there are a relatively small number of empirical studies

in which this paradigm has been used with non-human animal species, some studies

have suggested that targeted helping is observed only in limited number of animals,

such as some great apes, dolphins, and elephants (de Waal, 2008).

What is the difference between the two test paradigms? What psychological or

cognitive abilities are required in each test? In the prosocial choice test, if the

subjects are other-regarding, they only need to discriminate the reward distributions

between the two options. Therefore, the prosocial choice test is a useful device to

evaluate whether animals have other-regarding preferences and whether they can

discriminate between the reward distributions for themselves and the partner.

Meanwhile, to complete a targeted helping task, animals have to understand their

partner’s goals. This paradigm requires of animals more elaborate cognitive abilities

in terms of understanding others, i.e., perspective-taking. Capuchin monkeys’

results seem to fit with this explanation. They have shown prosociality in the

simpler prosocial choice test (de Waal et al., 2008; Lakshminarayanan & Santos,

2008; Takimoto & Fujita, 2011; Takimoto, Kuroshima, & Fujita, 2010), but not so

much in the targeted helping test (Barnes et al., 2008; Skerry et al., 2011). It has

been suggested that capuchin monkeys are not so skillful in perspective-taking

compared to chimpanzees (Hare, Call, Agnetta, & Tomasello, 2000; Hare, Addessi,

Call, Tomasello, & Visalberghi, 2003).

Interestingly, however, chimpanzees have demonstrated the opposite: they have

shown prosociality in the targeted helping tests (Melis et al., 2010; Warneken &

Tomasello, 2006; Warneken et al., 2007; Yamamoto et al., 2009, 2012), but rarely

in the prosocial choice tests (Brosnan et al., 2009; Jensen et al., 2006; Silk et al.,

2005; Vonk et al., 2008; Yamamoto & Tanaka, 2010; but see also Horner et al.,

2011). One of the most plausible explanations would be that chimpanzees may

recognize others’ goals (Call, Hare, Carpenter, & Tomasello, 2004), but may not

take them into account unless directly requested to help. Yamamoto et al. (2012)

empirically demonstrated that chimpanzees can understand the partner’s goals and

flexibly adjust their targeted helping in accordance with what the partner needs. In

their experiments, they presented chimpanzees with seven objects, one of which

could be used as a tool by the partner who was in an adjacent booth facing one of

two different tool-use tasks. In this setting, the helpers selected and transferred an

appropriate tool upon request, although not without such a request, when they could

visually assess the partner’s situation. Interestingly, when the visual information

about the partner’s situation was interrupted, the helpers still tried to respond to the

partner’s request (a gesture made by stretching out an arm), but could not select an

appropriate tool. These results suggested the following: (1) chimpanzees can

understand others’ goals just by visual assessment, (2) in spite of this, chimpanzees

seldom help others proactively, and (3) chimpanzees try to help others upon request

even when they do not understand the exact goals of others. The importance of the

recipients’ request has also been suggested from other empirical studies (Jaeggi,

Burkart, & van Schaik, 2010; Melis et al., 2010; Warneken & Tomasello, 2006;

Warneken et al., 2007; Yamamoto et al., 2009). In some prosocial choice tests,

however, the request did not affect (Vonk et al., 2008) or even decreased (Horner

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et al., 2011) the chimpanzees’ prosocial choice, which suggests that a request works

conditionally and sometimes plays an opposite role, as a harassment which might

undermine the prosociality of the partner.

Considering the characteristics of chimpanzee helping, humans appear to be

unique in their proactive targeted helping. Sometimes people help others upon

observing them in trouble, even without being requested. This may be possible

because of humans’ well-developed theory-of-mind abilities, such as understanding

others’ desires and shared intentionality. However, as is sometimes seen in real life,

unsolicited helping runs the risk of resulting in wasted labor, as the recipient may

not need or appreciate the help. Why have humans evolved such a risky helping

style? Reputation and indirect reciprocity may have strongly influenced its evolution

(Nowak & Sigmund, 2005; Ohtsuki & Iwasa, 2006). Even if the recipient does not

appreciate their proactive help, the helper may obtain a good reputation from third-

party individuals and then from the society to which they belong. It can be easily

argued that in such a society, people behave prosocially even without being solicited

(Yamamoto & Tanaka, 2009a). This indirect reciprocity system ensures future

benefit for prosocial individuals in the ultimate perspective, which means that

people are not necessarily conscious of this system.

Prosociality and Fairness

As stated above, prosociality and fairness are supposed to be closely linked.

Especially in humans, the strong preference for fairness, in collaboration with the

reputation system, leads to our social norms, which strongly promote prosocial

behavior (Fehr & Fischbacher, 2004). Fairness can be behaviorally presented as

inequity aversion, which is categorized into two types: advantageous and

disadvantageous inequity aversion. The former is a negative response to an

inequitable outcome in which an individual earns more than a comparison

individual, while the latter means that an individual resists an opposite inequitable

situation, in which they receive less than another (Fehr & Schmidt, 1999). People

demonstrate both the types of inequity aversion. This means that people are willing

to give up some material payoff to benefit others and to move in the direction of

more equitable outcomes (advantageous inequity aversion). This human inclination

strongly supports proactive prosocial behavior.

Now the question is whether this happens in non-human animals or not. At this

moment, there is no empirical evidence for reputation or social norms having a

strong effect on prosocial behavior in primates other than humans. Although

chimpanzees (Subiaul, Vonk, Okamoto-Barth, & Barth, 2008; Russell, Call, &

Dunbar, 2008; but not capuchin monkeys: Brosnan & de Waal, 2009) seem to

evaluate other’s behavior, there is no evidence that they adjust their prosocial

behavior by recognizing that they are evaluated by others (i.e., audience effect). In

addition, although there has been accumulating evidence for a sense of fairness in

non-human animals (for review, see Brosnan, 2009, 2011), the animals have

normally demonstrated only disadvantageous inequity aversion (Brosnan & de

Waal, 2003; Brosnan, Schiff, & de Waal, 2005; Fletcher, 2008; Massen et al., 2011;

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Neiworth, Johnson, Whillock, Greenberg, Brown, 2009; van Wolkenten, Brosnan,

& de Waal, 2007), and there is little evidence for advantageous inequity aversion

(Brosnan, Talbot, Ahlgren, Lambeth, & Schapiro, 2010; see also Brosnan, 2012,

previous issue; Christen & Glock, 2012, this issue). Therefore, a sense of fairness in

non-human animals may not directly promote prosocial behavior in them. Actually,

the absence or scarcity of proactive prosocial behavior, especially in chimpanzees,

may partly be explained by these facts, i.e., the lack of social norm and

advantageous inequity aversion. In this section, we will focus on disadvantageous

inequity aversion in non-human animals, and discuss another possible role of this

type of sense of fairness and how it influences prosocial behavior.

First of all, there appears to be a considerable phylogenetic link between

prosociality and inequity aversion. Chimpanzees and capuchin monkeys have been

the most examined. These two species have shown both a greater tendency to reject

inequitable outcomes (Brosnan & de Waal, 2003; Brosnan et al., 2005; Brosnan,

Talbot, et al., 2010; Fletcher, 2008; van Wolkenten et al., 2007; but see also Jensen

et al., 2007a) and greater prosocial tendencies in either the prosocial choice tests or

the helping tests than have many other species (de Waal et al., 2008; Lakshmin-

arayanan & Santos, 2008; Melis et al., 2010; Takimoto & Fujita, 2011; Takimoto

et al., 2010; Warneken & Tomasello, 2006; Warneken et al., 2007; Yamamoto et al.,

2009, 2012). Cottontop tamarins have also demonstrated both traits (prosociality:

Cronin et al., 2010, inequity aversion: Neiworth et al., 2009), although there have

been contradictory results on prosociality (Cronin and Snowdon, 2008; Cronin et al.,

2009; Stevens, 2010). Long-tailed macaques (Macaca fascicularis) have demon-

strated a prosocial tendency (Massen et al., 2010), even though they are known as a

despotic species with a steep linear hierarchy (Thierry, 2000). Accordingly, they

also showed aversion to disadvantageous inequity (Massen et al., 2011). Orangutans

(Pongo pygmaeus), which are not known to cooperate to a great degree in the wild,

possibly due to their more solitary social organization (van Schaik & van Hooff,

1996), did not show any inequity aversion (Brauer, Call, & Tomosello, 2006;

Brosnan, Flemming, Talbot, Mayo, & Stoinski, 2011). However, the link between

prosociality and fairness requires further investigation, because some studies with

captive orangutans have suggested that they do show reciprocal cooperation

(Dufour, Pele, Neumann, Thierry, & Call, 2008).

We next consider the link between prosociality and fairness from the perspective

of its mechanism. Although it is assumed that a sense of fairness is beneficial as a

mechanism for stabilizing cooperation (Fehr & Schmidt, 1999), there can be

competition in nature between fairness and prosociality (Brosnan, Hauser, et al.,

2010). Prosocial behavior may lead to unequal payoffs between the actor and the

recipient (Fig. 2). Consider the prosocial choice test. The actor has the choice of

either the prosocial or the selfish option. Either option produces the same reward to

the actor; therefore, the actor could benefit the partner at no cost. Nevertheless, the

actor has to spend labor on this task (e.g., pulling a bar), whereas the partner does

nothing. In this situation, selecting the prosocial option results in disadvantageous

inequity in terms of effort, although the reward is equal. Animals that are sensitive

to disadvantageous inequity have to overcome at least such temporal inequity. In

fact, there has been a study suggesting this competition. In an experiment entailing

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the competing demands of prosociality and equity, capuchin monkeys ceased

prosocial behavior when this other-rewarding behavior resulted in considerable

disadvantageous inequity in rewards (Brosnan, Hauser, et al., 2010).

One possibility is that non-human animals can recognize reward differences

between themselves and others, but are not sensitive to an imbalance in effort. Many

studies that suggested inequity aversion in non-human animals (e.g., Brosnan & de

Waal, 2003; Brosnan et al., 2005; Brosnan, Talbot, et al., 2010; Fletcher, 2008) have

focused on the imbalance in rewards between the target subject and his or her

partner, but did not consider the influence of the reward/effort balance on the

partner’s side. A smaller number of studies (Massen et al., 2011; van Wolkenten

et al., 2007) manipulated the amount of effort required of the targeted subjects who

would get a lesser reward and found that an increased amount of effort increased the

subjects’ aversion to the reward inequity; however, this result can be interpreted as a

sign that the subjects responded just to their own increased amount of labor, and that

this effort-effect might not be based on comparisons with the partner. So far, there

has been no empirical study that shows non-human animals are sensitive to inequity

in effort between themselves and their partner (cf. Fontenot, Watson, Roberts, &

Fig. 2 Response to equity and inequity of prosocial behavior and a sense of fairness. Top when there isequity between self and others, prosocial behavior generates disadvantageous inequity situation (light-gray arrow), and therefore, a sense of fairness may work the other way (dark-gray arrow). Middle whenthere is advantageous inequity situation, prosocial behavior and advantageous inequity aversion work todiminish the inequity. Bottom when there is disadvantageous inequity situation, prosocial behaviorincreases the inequity. Disadvantageous inequity aversion may restrict this unnecessarily excessiveprosocial behavior

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Miller, 2007). Therefore, how animals perceive imbalance and whether or not the

animals really do the two-by-two comparison with respect to effort remains to be

resolved in future studies.

Nevertheless, some have suggested that capuchin monkeys, although not, so far,

chimpanzees (Melis, Schneider, & Tomasello, 2011), are sensitive to the amount of

others’ labor at least in cooperation tasks. De Waal and Berger (2000) found that

capuchin monkeys shared more food reward with the partner when the reward was

obtained by cooperation with the partner than when they obtained the reward by

themselves. Moreover, Takimoto and Fujita (2011) showed that capuchin monkeys

did not discriminate between prosocial and selfish choices when the partner did not

need to help, but actively tried to benefit their partner when the partner did help.

Food sharing in de Waal and Berger (2000) could have been a by-product of

increased proximity between the monkeys rather than an intention of the operator.

However, this account fails to apply to Takimoto and Fujita (2011) as the operator

monkeys had to make a dichotomous choice, and there was no increased proximity

between the operator and the recipient. These results suggest that non-human

animals are equipped with sensitivity to the amount of others’ efforts as well as

sensitivity to the reward distribution.

Considering competition between a sense of fairness and prosociality, inequity

aversion may not actively ‘‘promote’’ prosociality during the first stage, but may

‘‘stabilize’’ cooperation, by keeping the balance between giving and receiving

prosocial behavior. There can be two mechanisms to stabilize cooperation: one with

a negative response directly aimed at free-riders, such as punishment that leads free-

riders to amend their behavior, and the other is one that involves an evaluation of

the partner, enabling animals to avoid free-riders and choose appropriate partners

for cooperative interactions. In non-human animal studies, there has been limited

evidence supporting the idea that punishment maintains cooperation by changing

free-riders into valuable cooperators. Even in humans it has been reported that

punishment leads to lower payoffs in repeated public goods games (Rand, Dreber,

Ellingsen, Fudenberg, & Nowak, 2009). Thus, we can question whether costly

punishment is an ideal force for promoting cooperation, at least in all situations. It is

almost certain that non-human animals, especially chimpanzees, have a revenge

system, i.e., negative reciprocity (de Waal & Luttrell, 1988; Jensen et al., 2007b).

However, such a negative response to inequity often results in the corruption of

reciprocal cooperation (Yamamoto & Tanaka, 2009b, c), rather than promoting

cooperation (although see Raihani, Grutter, & Bshary, 2010; Raihani & McAuliffe,

2012, previous issue).

It may be more plausible to assume that instead, a sense of fairness stabilizes

cooperation through the mechanism of the evaluation of the partner (Fehr &

Schmidt, 1999; Brosnan, 2006, 2011). The ability to recognize situations in which

one is receiving a lesser outcome than a partner in a cooperative interaction may

encourage individuals to switch to a new partner. If the new partner is more

equitable, this ultimately functions to increase the individuals’ payoffs and ensures

proper benefits for both. The negative response to inequity can also function as a

commitment device (Frank, 1988; Yamagishi et al., 2009). It can be an indicator of

an individual’s fairness, whereby a good reputation as a good cooperative partner is

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obtained (Frank, 1988). Similarly, refusing absolute gains which are relatively

unequal may send a signal to potential partners that they cannot get away with such

behavior with you, perhaps increasing future gains (Yamagishi et al., 2009). This

theory can possibly be applied to non-human animals. Melis, Hare, and Tomasello

(2006) reported that chimpanzees facing a collaboration task recruited the more

collaborative and effective of two potential partners on the basis of their experience

with each of them on a previous day. This suggests that non-human animals, or at

least chimpanzees, can evaluate others’ cooperative tendencies and appropriately

choose the cooperative partner, which leads to reciprocal interaction (Melis, Hare,

& Tomasello, 2008). Although reciprocal cooperation did not last long when the

pairs of chimpanzees were fixed in experimental settings (Yamamoto & Tanaka,

2009b, c), it has been suggested that reciprocal interaction is balanced between

individuals in the wild (Gomez, Mundry, & Boesch, 2008; Mitani, 2006; Mitani &

Watts, 2001). This may be achieved due to their fission–fusion society that allows

individuals to flexibly change their partner in social interactions.

As stated above, fairness and cooperation seem to be closely linked phyloge-

netically, and possibly coevolved (Brosnan, 2011). However, the mechanism

remains a theoretical concept supported by inadequate collateral evidence and

should be empirically examined in the future studies. If a sense of fairness is

actually a useful device for detecting free-riders and choosing partners, this

mechanism ensures a deterrent for defection; nevertheless, it cannot actively

promote prosocial behavior. In concluding this section, a sense of fairness may

stabilize cooperation, but it is unlikely to play a promoter role. To start cooperative

relationships by initiating prosocial behavior, there has to be a mechanism to

overcome inequity aversion during the first stage. How do animals realize this, and

what actively promotes the commencement of prosocial behavior?

Prosociality and Empathy

It is quite plausible that a sense of fairness is closely related to prosocial behavior.

Moreover, it may play a role as a stabilizer of prosocial behavior, albeit not a

promoter. Therefore, there is a need to identify another psychological mechanism

that acts as a promoter of prosocial behavior. Empathy seems to be the best

candidate for this role (de Waal, 2008).

Empathy is the capacity to (1) be affected by and share the emotional state of

another (e.g., emotional contagion), (2) assess the reasons for the other’s state, and/

or (3) identify with the other, adopting his or her perspective (de Waal, 2008; de

Waal & Suchak, 2010). This definition of empathy does not necessarily require

developed cognitive abilities. Psychologists sometimes speak of empathy only when

it involves perspective-taking and are skeptical about the existence of empathy in

non-human animals (Hauser, 2000; Povinelli, 1998). However, de Waal (2008)

emphasized that at its most basic, empathy can be defined as emotional sensitivity to

others or emotional contagion (Hatfield et al., 1994). According to de Waal (2008),

perception of the emotional state of another automatically activates shared

representations, causing a matching emotional state in the observer. He also

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proposed a model in which empathy is cognitively multilayered: from state-

matching (e.g., emotional contagion) to sympathetic concern (e.g., consolation) and

perspective-taking (e.g., targeted helping) with increasing cognitive capacities (de

Waal, 2008, 2012).

How does empathy promote prosocial behavior? Previously, de Waal et al. (de

Waal, 2008; de Waal & Suchak, 2010) pointed out that sympathetic concern occurs

when emotional contagion is combined with the appraisal of the other’s situation,

leading to attempts to understand the cause of the other’s emotions. This other-

oriented emotional activation might be seen in consoling and assisting others against

aggression in the wild. When the ability to understand others (i.e., perspective-

taking) is added, it enables animals to perform targeted helping, i.e., help and care

based on a cognitive appreciation of the other’s specific need, or situation. This

explains the mechanism by which empathy may cause prosocial behavior. In

addition, empathy may also work as a feedback system based on the consequences

of prosocial behavior. If animals can be affected by the positive emotion of another

that they have helped, this emotional contagion will work as a positive feedback to

promote future prosocial behavior. People sometimes worry about whether their

helping is actually helpful to others and also get upset when their offer of help is

refused. Thus, in humans, expression of gratitude is important, even if this is not an

actual return benefit. Although this has not been fully examined in non-human

animals (but see Bonnie & de Waal, 2004), chimpanzee helpers in the targeted

helping test sometimes closely watched the partner getting a reward with a tool that

they donated (Yamamoto et al., unpublished data; cf. see supplemental videos in

Yamamoto et al., 2009, 2012). They did not seem to be interested in the reward

itself in the partner’s hand, as they often demonstrated no request for it. Thus, even

though they received no return benefit (e.g., there was no sharing the juice reward),

they continued to help the partner.

Therefore, according to this explanation, prosocial behavior may be solicited by

empathy in situations in which animals are able to recognize another’s desire easily.

Returning to the laboratory findings, we see that in the prosocial choice test, the

partner’s need was obvious in the simplest setup: for the prosocial option, food was

set in front of the partner, and their own and the partner’s desire for food was the

same. Takimoto and Fujita (2011) reported that capuchin monkeys participating as a

‘‘partner’’ often made a request to the subject, or expressed a desire for the food by

reaching out for it. Therefore, if we can assume the animals are equipped with

sensitivity to another’s emotion, prosocial behavior in this choice test could

naturally occur in the animals.

Now the question is why chimpanzees did not proactively help others even when

they understood exactly the partner’s need (e.g., Yamamoto et al., 2012). In the

targeted help tests, chimpanzees understood what the partner needed and

appropriately selected and donated a tool to the partner so that they could get a

reward using it. This study also suggested that the chimpanzees could only

understand the partner’s goal by visual assessment, but not by direct vocal and

gestural communication between them. In spite of this, they did not help the partner

proactively, but only after being requested. Why did prosociality not occur

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automatically following the chimpanzees’ understanding of the needs of their

partners?

Here, we may have to separately consider empathy and the understanding of

others’ goal. de Waal stated (2008 p. 285) that ‘‘Perspective-taking by itself is, of

course, hardly empathy: It is so only in combination with emotional engagement’’.

Continuing this line of discussion, cognitively developed species do not necessarily

show high levels of empathy or prosociality.

We would like to advance this discussion by hypothesizing that cognitively

developed animals have to be equipped with some modulatory mechanism to deal

with empathy-based prosociality. If animals automatically responded to every desire

of others with prosocial behaviors, they would be exhausted from helping. Such

individuals could also be easily exploited by free-riders, which would result in the

extinction of prosociality. Therefore, animals that have the capacity to put

themselves in the other’s ‘‘shoes’’ and can easily recognize the other’s desire

paradoxically have to limit their helping to some extent. As a result, in animals that

are skilled at perspective-taking, their inhibitory mechanism should also be strong,

and therefore some additional triggers should be required for eliciting prosocial

behavior. This hypothesis fits the results for chimpanzees. Chimpanzees may

recognize others’ goals and needs, but may not take them into account unless

directly requested for help.

How do animals limit their prosociality? One strategy is to refrain from

proactively helping, as the chimpanzees do in the tests described above. Social

relationships may also have a considerable influence on this process. The closest

relationship is the mother–infant relationship, which can be considered as the core

unit of a social group (Hirata, 2009; Matsuzawa, Tomonaga, & Tanaka, 2006).

Prosocial behavior occurs most often between the mother and infant (Hirata, 2009),

although request is still important even in this closest bond in chimpanzees (Ueno &

Matsuzawa, 2004; Yamamoto et al., 2009; Yamamoto & Tanaka, 2009c, 2010);

other kin, friends, old acquaintances, and in-group members follow this in

frequency. In capuchin monkeys, it was reported that prosocial tendencies increased

with social closeness, being lowest toward strangers and highest toward kin (de

Waal et al., 2008). In long-tailed macaques, Massen et al. found a strong effect of

kin-ship on prosocial behavior (Massen et al., 2010), although they did not find an

effect of relationship quality among non-kin (Massen et al., 2010, 2011).

Competition may also serve as an inhibitor of prosociality. It is suggested that

chimpanzees demonstrate cognitively sophisticated abilities in experiments using

competition paradigms, as compared to cooperation paradigms (Hare, 2001; Hare &

Tomasello, 2004). Therefore, chimpanzees seem to be fine-tuned to competition, in

which naturally the automatic arousal of prosociality should be minimal.

Another way that animals limit prosociality is through fairness. Disadvantageous

inequity aversion serves to stop the unnecessarily excessive expression of

prosociality. When others are getting an equal or greater benefit, there is no need

to help them. A sense of fairness plays a role in this evaluation. A sense of fairness

also helps animals choose an appropriate partner to whom they should direct their

prosociality. In humans, research on neural activity suggests that empathic brain

responses to another person’s pain are modulated by perceived fairness of the other

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person (Singer et al., 2006). In Singer et al.’s (2006) experiments, empathy-related

activation was observed when a fair, likeable player was in pain. However, men, but

not women, showed an absence of such empathic brain response when seeing an

unfair player in pain. The link between fairness and empathy will be discussed again

in the section ‘‘Fairness and empathy.’’

In conclusion for this section, empathy can serve as a promoter of prosocial

behavior, but does not possess in itself mechanisms for stabilizing cooperation (i.e.,

free-rider avoidance). Therefore, animals equipped with empathy need a braking

system to avoid being exploited by free-riders. We suggest that empathy and

fairness may work interactively with each other to maintain the balance of

prosociality. We will discuss this in detail in the next section.

Fairness and Empathy

Here is a brief review of our points. Empathy promotes but does not stabilize

prosocial behavior, whereas a sense of fairness stabilizes but does not promote.

These two psychological mechanisms can be likened to a car’s accelerator and

brake. To drive a car (prosociality and cooperation), both an accelerator (empathy)

and a brake (a sense of fairness) are necessary, and balance between the two is

important. A brake of course, cannot start a car, and an accelerator cannot stop a car

from crashing.

Emerging data support the hypothesis that a sense of fairness and empathy

coevolved in conjunction with prosociality. Comparative studies indicate that

species that respond to inequitable outcomes also demonstrate empathic prosocial

behavior (Table 1). Although we are limited to data from only a few species, studies

on chimpanzees and capuchin monkeys have shown disadvantageous inequity

aversion in these species (chimpanzees: Brosnan et al., 2005; Brosnan, Talbot, et al.,

2010, capuchin monkeys: Brosnan & de Waal, 2003; Fletcher, 2008; van Wolkenten

et al., 2007). They are also known to be other-regarding in some ways

(chimpanzees: Horner et al., 2011; Melis et al., 2010; Warneken & Tomasello,

2006; Warneken et al., 2007; Yamamoto et al., 2009; 2012, capuchin monkeys: de

Waal et al., 2008; Lakshminarayanan & Santos, 2008; Takimoto & Fujita, 2011;

Takimoto et al., 2010). Bonobos have been considered to be prosocial and more

cooperative than chimpanzees (Hare & Kwetuenda, 2010; Hare, Melis, Woods,

Hastings, & Wrangham, 2007; but see also Jaeggi, Stevens, & van Schaik, 2010),

and in a study of direct comparison with chimpanzees and orangutans, they have

demonstrated the highest difference in the rejection rate between the inequity

(approximately 20 % rejection) and equity conditions (approximately 10 %

rejection), although this difference was not significant (possibly due to the small

sample size; see the discussion in Brosnan, 2011 referring to Brauer et al., 2009; see

also Brauer & Hanus, 2012, this issue). Recently, long-tailed macaques (who are a

despotic species) have demonstrated both empathic prosociality (Massen et al.,

2010) and inequity aversion (Massen et al., 2012). We cannot directly examine

empathy itself from behavioral data; however, in experimental paradigms (prosocial

choice tests and targeted helping tests) animals could not expect any return benefit,

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and therefore the psychological motivation could be interpreted as being driven by

empathy (de Waal, 2008).

The hypothesis that a sense of fairness and empathy coevolved is also supported

by data on the absence of prosocial behavior. Among the New World monkeys,

squirrel monkeys, which cooperate in only limited situations (Boinski, 1987), did

not respond negatively to inequity (Talbot, Freeman, Williams, & Brosnan, 2011).

Data on cottontop tamarins are not fully consistent. In some studies, cottontop

tamarins demonstrated sympathetic concerns (Cronin et al., 2010); however, in

others they did not show other-regarding behavior in the prosocial choice tests

(Cronin et al., 2009; Stevens, 2010). Their tendency of inequity aversion is also still

debated (cf. Neiworth et al., 2009; see also Price & Brosnan, 2012, previous issue).

Considering that cottontop tamarins are cooperative breeders and have demon-

strated intense levels of cooperation (Cronin et al., 2005; Cronin & Snowdon, 2008),

we can expect that they are equipped with these two psychological traits; however,

at this moment, we just point out the necessity of further investigation with this

species. Common marmosets, another cooperative-breeding New World monkey,

have shown prosociality, choosing the prosocial option more often when the partner

was present than absent (Burkart et al., 2007). Unfortunately, at this moment, data

on inequity aversion in this species are not available. Again further studies are

needed.

Both a sense of fairness and empathy might have evolved on the basis of

preference for similarity with others. Humans, from a very early age, are known to

show preference to individuals who are similar to themselves. Sanefuji, Ohgami,

and Hashiya (2006) presented 6- and 9-month-old babies with movies and pictures

of 6-, 9-, and 12-month olds. The results revealed that 9-month olds showed peer

preference when they saw movies of infants and that 6- and 9-month olds preferred

static images of same-age infants. This study suggests that humans inherently have a

sensitivity to similarities and differences between others and themselves, and that

they feel familiarity with those who have similar traits. Such sensitivity can be

considered as a basis for fairness and empathy. Similarity between individuals

seems to be important in affiliative interactions among non-human primates, too.

Capuchin monkeys affiliate preferably with human experimenters who imitated

their behavior (Pankner, Suomi, Visalberghi, & Ferrari, 2009). Primates sometimes

intentionally adjust their power balance between individuals. For example, analysis

of play behavior in primates indicates that physically stronger, or socially dominant

participants tend to inhibit their power and control playful interactions with weaker

or subordinate individuals (self-handicapping: Fagan, 1981; Shimada, 2006). As a

result, actual differences in relative ranks, or power among participants, do not seem

to exist during social play, which leads to maintaining this affiliative interaction (but

see also van Leeuwen, Zimmermann, & Davila Ross, 2010: gorillas seem to try to

maintain their competitive advantage during play fights).

Peer preference in non-human animals can also be easily seen in their in-group

biases in friendly social interactions. They restrict cooperative behavior to familiar

group members. In the experiments that have examined responses to inequity, it has

been suggested that chimpanzees, but not long-tailed macaques (Massen et al.,

2012), show higher tolerance to inequity between long-term associates, in

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comparison to recently introduced individuals (Brosnan et al., 2005). Thus, inequity

aversion is regulated by the social relationship between individuals. Social closeness

also affects empathy, although in the opposite direction, by enhancing empathy. In

prosocial choice tests, prosocial tendencies in capuchin monkeys increased with

social closeness, being lowest toward strangers and highest toward kin (de Waal

et al., 2008). In chimpanzees, mutual request behaviors were observed in mother–

infant pairs more frequently than in non-kin adult pairs, leading to more frequent

and mutual helping between mothers and infants (Yamamoto et al., 2009). As

mentioned in the section ‘‘Prosociality and empathy,’’ a sense of fairness and

empathy are closely related: when feeling inequity, men did not feel empathy for the

unfair person in pain. For the emergence of prosociality, the balance between a

sense of fairness and empathy is important, and this seems to be regulated by the

social relationship with others.

In short, we postulate that a sense of fairness and empathy emerged from the

same principle and work interactively and differently for soliciting and maintaining

prosocial behavior. Although empathy, or at least its perception–action mechanism

(Preston & de Waal, 2002), is an automatic response that does not require conscious

effort, a sense of fairness may require a higher level of cognition, such as comparing

the reward/effort balance with others (Fehr & Schmidt, 1999). Therefore, emotional

contagion, the first step of empathy, may be found in various mammals and birds (de

Waal, 2008), but the existence of a sense of fairness may be restricted to several

more cognitively-developed species (including non-primates; see Range, Leitner, &

Viranyi, 2012, previous issue; Horowitz, 2012, previous issue; Pierce & Bekoff,

2012, previous issue). We hypothesize that if both a sense of fairness and empathy

are important for promoting and stabilizing prosocial behavior, empathy (emotional

contagion) alone may not be related to the prevalence of prosociality, in the absence

of a sense of fairness, which may be considered to be the braking mechanism. For

example, mirror neurons seem to compose the core part of empathy, such as the

perception–action mechanism, but may not warrant sympathetic concern in animals

(Preston & de Waal, 2002). Thus, the existence of mirror neurons itself does not

directly lead the existence of prosociality in a species.

Conclusion and Future Direction

In this article, we have discussed prosocial behavior and cooperation in relation to their

possible underlying mechanisms, a sense of fairness and empathy. We then proposed a

hypothesis of the coevolution of a sense of fairness and empathy and suggest that they

function as a promoter and a stabilizer of prosocial behavior, respectively. Of course,

not all prosocial behavior requires empathy (de Waal, 2008), and the propensity to

engage in other-regarding behavior is not determined exclusively by whether an

animal is equipped with such empathic resonance mechanisms, but by many other

factors as well (Singer, 2009). Keeping this in mind, we simplified our discussion by

focusing on these two mechanisms and the triadic relationship.

Figure 3 exemplifies how prosocial behavior and cooperation are related to a

sense of fairness, empathy, and other relevant factors. We suggest that starting from

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the preference for similarity, perhaps through the avoidance of heterogeneity,

psychological mechanisms for inequity aversion, i.e., a sense of fairness, emerged.

This may have developed into social norms when animals acquired a reputation

system and its required cognitive abilities, such as language and an understanding of

triadic interactions (self, partner, and third-party), which can be found specifically in

humans (Tomonaga et al., 2004). Although social norms may promote prosocial

behavior directly, a sense of fairness, represented as disadvantageous inequity

aversion, functions to stabilize prosocial behavior through the evaluation of others’

fairness, and partner choice. The other line of mechanisms, i.e., empathy, also starts

from psychological traits that prefer similarity with others, going through simple

emotional contagion and leading to sympathetic concern. Although the ability

to understand others, such as perspective-taking, is not necessarily connected to

prosocial behavior, empathy, and especially sympathetic concern, function to

promote prosocial behavior directly.

We have reviewed a number of comparative studies conducted with non-human

primates that at least partially support our hypothesis. Unfortunately, however, there

are still not enough data to conclusively support, or reject, our hypothesis. First of

all, controversy still continues as to whether a sense of fairness exists in non-human

animals (Brauer et al., 2009; Henrich, 2004; Silberberg, Crescimbene, Addessi,

Anderson, & Visalberghi, 2009; see also Christen & Glock, 2012, this issue). To

counter this skepticism, we suggest that researchers have to focus more on the

balance between reward and effort (see also Skitka, 2012, this issue). Previously

Fig. 3 The relationship among prosocial behavior, a sense of fairness, empathy, and other relevantfactors. A sense of fairness and empathy interact with each other (we do not mean that each factor in thetwo lines is linked one by one). Similarity also influences these two mechanisms, and therefore ultimatelyhas an effect on prosocial behavior

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studies with non-human animals have focused mainly on reward inequity, almost

ignoring the effort imbalance. Furthermore, we also have to consider individual

differences. Who is concerned about fairness? It is possible that individual A may

feel inequity to a certain payoff that individual B may consider fair? Social status,

physical abilities, and many other factors might affect a sense of fairness. When

discussing a sense of fairness in this article, we focused on disadvantageous inequity

aversion because there has been little evidence for advantageous inequity aversion

in non-human animals (Brosnan, Talbot, et al., 2010). As mentioned above (see the

section ‘‘Prosociality and fairness’’), advantageous inequity aversion is directly

linked to prosocial behavior, and some researchers have pointed out the possibility

that human prosocial behavior, as observed in economic game paradigms, may well

be based on fairness motives rather than empathic motives (Singer, 2009). The

evolution of advantageous inequity aversion is still mysterious and worth further

investigation.

As for empathy, many issues also remain to be investigated. Preston and de Waal

(2002) proposed the perception–action model in which empathy is automatically

aroused upon observing others in some emotional states. However, considering the

observed empathy–fairness intervention in neural activities, which is found in men

who did not feel empathy for the unfair person in pain (Singer et al., 2006), it is

plausible that empathy is not always a mere automatic consequence of the passive

observation of emotional cues in others, but rather subject to an appraisal of the

situation and modulation (de Vignemont & Singer, 2006; Singer, 2009). The

interaction between fairness and empathy recently received attention in empirical

studies with non-human animals (e.g., de Waal et al., 2008), and further

developments are expected.

In human prosociality, we can detect the influence of a sense of fairness and

empathy, as well as their interaction, and it seems that human psychological

tendencies are more biased toward prosociality, which allows for our highly

cooperative society. From the viewpoint of cognitive mechanisms, this seems to be

linked to what appear to be human-unique traits, including advantageous inequity

aversion, social norms, and sophisticated abilities to understand others’ desires,

although perspective-taking itself should be carefully discussed apart from

sympathetic concern. In addition to searching for the evolutional basis for these

cognitive mechanisms, we would also like to understand individual, sex, cultural,

and/or developmental differences in human prosociality, fairness, and empathy. As

the literature on these topics has begun to develop only recently (e.g., Singer et al.,

2006; Svetlova, Nichols, & Brownell, 2010), there is not yet enough evidence to

draw firm conclusions. A better understanding of the nature, culture, and

development of the promoting and modulating factors of prosociality will help us

to understand the complex interplay of conditions determining prosocial behavior.

Acknowledgments We thank Dr. Sarah Brosnan, the editor of this pair of special issues, and the

anonymous reviewers for their thoughtful comments. This study was financially supported by the Japan

Society for the Promotion of Science Grants #22800034 (to S.Y.) and #20220004 (to A.T.), and by the

Ministry of Education, Culture, Sports, Science & Technology in Japan #24000001 (to Tetsuro

Matsuzawa).

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Conflict of interest The authors declare that they have no conflict of interest.

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