How Did Altruism and Reciprocity Evolve in Humans? Perspectives from Experiments on Chimpanzees (Pan Troglodytes)

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How did altruism and reciprocity evolve in humans? Perspectives from experiments on chimpanzees (Pan troglodytes)

Shinya Yamamoto and Masayuki Tanaka Primate Research Institute, Kyoto University, Japan / Wildlife Research Center, Kyoto University, Japan

The evolution of altruism and reciprocity has been explained mainly from ultimate perspectives. However, in order to understand from a proximate perspective how humans evolved to be such cooperative animals, comparative studies with our evolutionary relatives are essential. Here we review several recent experimental studies on chimpanzees’ altruism and reciprocity. These studies have generated some conflicting results. By examining the differences in the results and experimental paradigms, two characteristics of prosociality in chimpanzees emerged: (1) chimpanzees are more likely to behave altruistically and/or recip- rocally upon a recipient’s request, than without request, and (2) chimpanzees also show a tendency to regard others and help in contexts not involving food. Supposing that these two characteristics of altruism, recipient-initiated altruism and non-food altruism, were present in the common ancestor of chimpanzees and humans, it is possible that increased social cognitive abilities, capacity for language, necessity for food sharing, and enriched material culture favored in humans the unique evolution of cooperation, characterized by voluntary altruism and frequent food donation.

Keywords: chimpanzees, prosocial behavior, reciprocity, recipient-initiated altruism, non-food altruism, human evolution

Introduction

Why did cooperation evolve? This is because cooperation sometimes provides a payoff. First of all, we should definitely distinguish two types of cooperation in order to avoid useless debate regarding the terminology (Bshary & Bergmüller,

Interaction Studies 10:2 (2009), 150–182. doi 10.1075/is.10.2.04yam issn 1572–0373 / e-issn 1572–0381 © John Benjamins Publishing Company Altruism and reciprocity in chimpanzees 151

2008; Noë, 2006; West, Griffin, & Gardner, 2007). When cooperators themselves can gain immediate benefits from cooperating, this kind of cooperation has a selfish motivation, which is a by-product of mutualism (mutual cooperation). For example, in cooperative group-hunting in chimpanzees (Boesch, 2003; Boesch & Boesch, 1989), participants in the hunt may be pursuing only their own gain (Gilby, 2006) without shared intentionality (Tomasello, Carpenter, Call, Behne, & Moll, 2005). This kind of cooperation may be affected by the timing of cooperating with other individuals (Hirata & Fuwa, 2007), coordination of actions according to the others’ behaviors (Boesch, 2003; Boesch & Boesch, 1989) and choice of individuals to cooperate with (Melis, Hare, & Tomasello, 2006a). Mutualism therefore imposes no evolutionary constraint, since the actor can increase his or her own fitness. In contrast, altruistic cooperation or altruism, which is beneficial only to the recipient but not to the actor, may negatively impact fitness. For example, during food sharing, the donor incurs a cost, since it relinquishes food to the recipient at a cost to itself. There have been two main explanations for the evolutionary origins of this behavior. Although altruistic cooperators may incur small costs in the short term, they may gain greater selfish benefits either by increasing their inclusive fitness (“kin selection”, Hamilton 1964) or by recouping their losses in future interactions (“reciprocal altruism”, Trivers 1971). In this article we focus on altruism in chimpanzees, one of our closest living evolutionary neighbors. Controversy abounds as to whether or not chimpanzees show altruism and/or reciprocal altruism (reciprocity), although they have been observed both in the wild and in captivity to exhibit apparently helping behaviors (Figure 1). We will briefly summarize the theoretical and empirical evidence for altruism and reciprocity. And then, we will review some recent experimental work on chimpanzees’ altruistic and reciprocal behavior, discuss some differences in the

Figure 1. Helping behavior in a wild chimpanzee. (Photo by Tetsuro Matsuzawa) 152 Shinya Yamamoto and Masayuki Tanaka

results obtained, and extract some significant factors which might be influencing chimpanzees’ behavior. We do not intend to summarize how chimpanzees are “similar” to humans with regards to reciprocity as previous studies have done (e.g., Brosnan & de Waal, 2002; de Waal & Brosnan, 2006). This paper aims rather to illuminate under which situations chimpanzees are more likely to cooperate with others. This comparative psychological approach might be more helpful for us to understand how humans evolved to be such cooperative animals.

Evolution of altruism

Theoretical work and empirical evidence in non-human animals Altruism toward kin individuals could evolve through kin selection. Animals that help their kin can increase their inclusive fitness (Hamilton, 1964). This kind of altruism requires no complex cognitive abilities, and has been reported in range of taxa, especially in social insects, e.g., ants and honey bees. In contrast, the evolution of altruism toward non-kin tends to require more conditions. Trivers (1971) proposed in his reciprocal altruism theory several prerequisites for the evolution of altruism toward non-kin: (1) the benefit to the recipient surpasses the cost to the actor; (2) the relationship between a certain pair is long-lasting and interactions occur many times; (3) the animals can recognize the partners and their behavior to avoid being exploited by non-cooperators. As for the third required condition, many theoretical studies have focused on what strategies would enable reciprocity to evolve and to become evolutionarily stable. In the computer tournaments run by Robert Axelrod, a “tit-for-tat” (TFT) strategy, in which a player cooperates when first meeting an opponent and sub- sequently copies whatever that opponent does, emerged as the winning strategy in iterated games of Prisoner’s Dilemma (PD) among 14 (Axelrod & Hamilton, 1981) and 62 recorded strategies (Axelrod, 1984). Nowak and Sigmund (1993) revealed that in their extended evolutionary simulations incorporating mutation and selection, TFT was outperformed by another outstanding strategy called the Pavlov strategy: win-stay, lose-shift, which has two advantages over TFT in that it can correct occasional mistakes and exploit unconditional cooperators. Connor (1992, 1995a, b) also proposed another explanation for reciprocity without using the framework of a PD game. In his “parceling” model, animals parcel into bouts the amount of altruistic behavior which their partner might require. Parceling can preclude the incentive to obtain a short-term benefit by defecting due to the small benefit parceled into bouts, and so can eliminate any opportunity of exploitation of the partner. Altruism and reciprocity in chimpanzees 153

Considering these very simple strategies aimed at maintaining cooperation, the evolution of reciprocity might not require animals to be equipped with complex and elaborated cognitive abilities. In fact, possible cases of reciprocity have been reported in various taxa, including fish, birds, and a range of mammals, including primates (Dugatkin, 1997; Kappeler & van Schaik, 2006). First, reciprocity in agonistic support (Packer, 1977) and exchange for support and grooming (Seyfarth & Cheney, 1984) were reported in non-human primates. Other than primates, Wilkinson (1984) suggested reciprocal food (blood) sharing in vampire bats (Desmodus rotundus). The system of their sharing behavior meets the important prerequisites proposed by Trivers (1971): (1) blood meal is critical for starving recipients, while the cost of sharing blood may not be so high; (2) the probability of future interaction is sufficiently high; and (3) vampires are able to recognize each other and are more likely to give blood to those that have donat- ed in the past (see also Wilkinson, 1986). Some experiments on sticklebacks’ (G. aculeatus) (Milinski, 1987) and guppies’ (P. reticulata) (Dugatkin, 1988) predator inspection behavior (Dugatkin & Godin, 1992) suggested that inspectors are using something akin to TFT when faced with a PD situation. And egg-exchange in simultaneous hermaphroditic sea basses (Hypoplectrus nigricans) (Fischer, 1980) and polychaete worms (Ophryotrocha gracilis) (Sella, Premoli, & Turri, 1997) and impalas’ (Aepyceros melampus) grooming behavior (Hart & Hart, 1992) might be good examples for the parceling model (Connor, 1992, 1995a, b). Recently, it has also been suggested that rats adopt a very simple strategy called generalized reciprocity, in which animals help unknown conspecifics in response to prior receipt of help, irrespective of the identity of the partner (Rutte & Taborsky, 2007). Simple forms of reciprocity might be widespread in the animal kingdom, although the mechanism underlying the behavioral exchange is still unclear and there has been a lot of criticism of the evidence for reciprocity (e.g., Hammerstein, 2003; Stevens & Hauser, 2004).

How humans cooperate and how such cooperation evolved? As described above, there have been a lot of suggestions concerning the evolution of altruism and reciprocity in animals. However, these are not completely satisfac- tory. First of all, the status of reciprocity itself is quite controversial (Stevens & Hauser, 2004). Previous empirical studies have faced criticism for ignoring alternative explanations, such as kin-selection (Hammerstein, 2003). Besides, if there is “evidence” for reciprocity, reports concern a wide range of taxa, suggesting evolutionary convergence. Each species might have acquired the behavior in accor- dance with their own circumstances and evolutionary pressures, and there might be little evolutionary continuity across species. This means that these theoretical 154 Shinya Yamamoto and Masayuki Tanaka

and empirical studies in themselves are not sufficient to understand how human altruism and reciprocity evolved. It is possible to consider that altruism and reciprocity in humans are somewhat different in quality from those reported in non- human animals, since the environment, social systems, and cognitive abilities are quite different (Fehr & Fischbacher, 2003). Unfortunately, the mechanisms underlying behavioral exchanges relevant to reciprocity have not been fully identified in non-human animals. To understand the evolution of human altruism and reciprocity, we need a better understanding of proximate factors. Theoretical frameworks normally deal with the ultimate reasons for the existence of reciprocal exchange as an explanation for the evolution of altruism. That is, it provides an explanation for why animals engage in such behavior, and which fitness benefits they derive from it. How- ever, it provides no explanation for how such cooperation is achieved (Brosnan & de Waal, 2002; de Waal & Brosnan, 2006). Not all forms of reciprocal altruism are cognitively complex. De Waal and his colleagues (Brosnan & de Waal, 2002; de Waal, 2000; de Waal & Luttrell, 1988) distinguished three types of reciprocity: (1) symmetry-based reciprocity, which is based on symmetries inherent in dyadic relationships (e.g., mutual association, kinship); (2) attitudinal reciprocity, which is based on the mirroring of social attitudes between partners; and (3) calculated reciprocity, which is based on mental scorekeeping. The most complex reciprocity, calculated reciprocity, is supposed to be rare in non-human animals (Hammer- stein, 2003; Stevens & Hauser, 2004), although some evidence was reported in chimpanzees (de Waal & Luttrell, 1988). Stevens and Hauser (2004) pointed out some cognitive constraints such as temporal discounting, numerical discrimina- tion and memory, which might make reciprocity difficult for animals. The cooperation system observed in humans might be unique in the animal kingdom (Fehr & Fischbacher, 2003). Humans might have acquired an ability for complex forms of reciprocity and have achieved societies based on cooperation with altruism after divergence from the common ancestor of humans and other living relatives. Now the question is how humans evolved to be such cooperative animals: in which situation did the evolution occur? What evolutionary basis for altruism and reciprocity did the common ancestor to humans and our evolutionary neighbors possess? To answer these questions, comparative studies on primates including humans are helpful (Matsuzawa, 2001). Studies of chimpanzees, or bonobos, are most revealing about the evolution of human behavior, since comparative studies on our living closest evolutionary neighbors are likely to illuminate the tendencies of our common ancestors. Although there exist many reports of altruism and contingency in patterns of altruism among both wild (Goodall, 1986; Hockings et al., 2007; Mitani, 2006; Mitani & Watts, 2001; Watts, 2002) and captive chimpanzees (de Waal, 1989, 1996, Altruism and reciprocity in chimpanzees 155

1997a; de Waal & Luttrell, 1988; Hemelrijk & Ek, 1991), few experimental studies have so far examined this behavior in detail in controlled laboratory settings. Experimental studies have the advantage of being able to manipulate and control possible influential factors, such as cost and benefit, contingency, and participants, which is practically impossible to do in observational studies. These days, however, this situation has changed gradually and fascinating experiments are being carried out, which have generated enthusiastic debate about chimpanzees’ altruism and reciprocity. Next, we would therefore like to review the recently conducted experiments with chimpanzees, and discuss the differing results that have emerged between these studies.

Experimental studies on chimpanzees

Altruism, prosociality and fairness in chimpanzees First of all, do chimpanzees show altruistic behavior toward conspecifics without any immediate benefit? Although there have been anecdotal reports of possible instances of helping (e.g., Goodall, 1986; de Waal, 1996), experimental evidence is scarce (but see Warneken & Tomasello, 2006; Warneken, Hare, Melis, Hanus, & Tomasello, 2007; see section on “Controversy over conflicting results”). Even though laboratory work on cooperation among chimpanzees goes back to Craw- ford (1937) and a considerable number of experiments have been conducted since then, most of them have been directed at examining mutually beneficial cooperation (Chalmeau, 1994; Chalmeau & Gallo, 1996a, b; Hare, Melis, Woods, Hastings, & Wrangham, 2007; Hirata & Fuwa, 2007; Melis, Hare, & Tomasello, 2006a, b, 2008; Povinelli & O’Neill, 2000). From these studies, various important aspects were revealed, such as the learning processes involved (Hirata & Fuwa, 2007), the influence of the relationship to the partner (Hare et al., 2007; Melis et al., 2006b), and the choice of the partner (Melis et al., 2006a, 2008). However, these studies have suggested that chimpanzees are selfishly motivated during mutually beneficial cooperation tasks, and it has therefore been suggested that chimpanzees do not possess shared intentionality with conspecifics (Tomasello, et al., 2005). In contrast to mutually beneficial cooperation, in altruistic behavior, the actor gains no additional benefit immediately by cooperating. It has been examined whether or not chimpanzees can give food to another conspecific without any material incentive in the act (Jensen, Hare, Call, & Tomasello, 2006; Silk et al., 2005; Vonk et al., 2008). Chimpanzees in these studies were offered a choice of two options with two different outcomes: the 1/0 option delivered a food reward only to themselves, and the 1/1 option delivered a reward not only to themselves but 156 Shinya Yamamoto and Masayuki Tanaka

also to their conspecific partner. The chimpanzees could get the same amount of food whether they chose the 1/0 or 1/1 option. In this situation, the chimpanzees could provide rewards to others by choosing 1/1 option at no cost to themselves (and so, strictly, we should use “prosociality” rather than “altruism” because of the absence of cost in the choice). The prediction was that if chimpanzees were other- regarding or were concerned about the welfare of others, they would prefer the 1/1 option in a test condition with a recipient present rather than in a control condition in which the partner was not in the recipient’s room but was in an irrelevant adjacent room. However, the chimpanzees showed no difference in the preference of their choice between the two conditions. Silk et al. (2005) and Jensen et al. (2006) concluded that chimpanzees lack other-regarding preferences and that such properties are unique to humans. We replicated these previous studies using button choice task (Figure 2), and obtained similar results as the previous study; that is, the chimpanzees showed no difference in the preference of the choice between the partner-present and partner-absent conditions (Yamamoto & Tanaka, submitted). The results were true not only between non-kin individuals but also between mothers and their offspring in both directions. This result for the mother–infant pairs contradicts kin-selection theory and empirical observations that have recorded biased altruism between mother-infant pairs (e.g., Goodall, 1986). In the meantime, however, some field studies such as at Ngogo in Uganda have revealed that kinship plays an ancillary role in chimpanzees’ affiliation and cooperation (Langergraber, Mitani, & Vigilant,

Figure 2. A chimpanzee in the room on the right is offered a choice of buttons between two options: 1/0 option (left orange button) which delivered a food reward only to themselves, and 1/1 option (right red button) delivered a reward not only to themselves but also to a conspecific recipient in the room on the left. (Yamamoto & Tanaka, submitted) Altruism and reciprocity in chimpanzees 157

2007; Mitani, Merriwether, & Zhang, 2000). Ueno and Matsuzawa (2004) also found that chimpanzee mothers seldom voluntarily gave food to their 1-year-old infants. Even mothers might not unconditionally behave altruistically toward their infant. These studies also aroused discussion on chimpanzees’ sense of fairness. Since Brosnan and her colleagues suggested that chimpanzees (Brosnan, Schiff, & de Waal, 2005) and capuchin monkeys (Brosnan & de Waal, 2003) demonstrate inequity aversion, there has been a lot of controversial discussion on the sense of fairness in non-human animals (Bräuer, Call, & Tomasello, 2006; Brosnan & de Waal, 2004, 2006; Jensen, Call, & Tomasello, 2007a; Roma, Silberberg, Ruggiero, & Suomi, 2006; Wynne, 2004). In the study described above, Jensen et al. (2006) also examined chimpanzees’ choice when the chimpanzees could choose between providing food solely to their partner (0/1 option) or no food at all including themselves (0/0 option). The results suggested that chimpanzees have no regard for the outcome to their partner. This is contradictory to Brosnan et al.’s (2005) finding of disadvantageous inequity aversion in chimpanzees. Taken together, there is still no consensus about the sense of fairness in chimpanzees.

Laboratory work in PRI on reciprocity in chimpanzees The previous experiments on altruism that we introduced above examined social preferences (e.g., empathy, inequity aversion) in chimpanzees. However, social preferences would not be the only one motivation for altruistic behavior. Animals might help others not only with other-regarding motivation but also with selfish strategies, since reciprocity has theoretically been shown to provide benefits to both players in a long-term perspective (Trivers, 1971). In order to understand the evolution of altruism, it is therefore also important to examine whether non-human animals show reciprocity, a strategic return-benefit system, with conspecifics. Unfortunately, there have been few well-controlled experimental studies, to our knowledge, on reciprocity among chimpanzees, except for our work conducted at the Primate Research Institute (PRI) of Kyoto University (Yamamoto & Tanaka, in press a, b, submitted). Melis et al. (2008) found that chimpanzees on the Ngamba Island Chimpanzee Sanctuary in Uganda increased their tendency to mutually cooperate with or help their partner if he or she had previously been helpful toward them. However, the effect was weak, and it was not the focus of the study to evaluate whether two chimpanzees establish and maintain reciprocal cooperation. In this section, therefore, we would like to review recent laboratory work at PRI on reciprocity in chimpanzees. We think two points are important in observing chimpanzees’ social behavior: (1) group-living chimpanzees as subjects, and (2) observation on chimpanzees’ interactions with conspecifics. At PRI, a group of 158 Shinya Yamamoto and Masayuki Tanaka

chimpanzees inhabits an enriched environment (Ochiai & Matsuzawa, 1998) and members spend their daily life with other conspecifics. Three infants born at PRI in 2000 were raised by their biological mothers. We tested not only non-kin pairs but also mother–infant pairs in order to examine the influence of kin relationship (cf. examination in the wild: Langergraber et al., 2007). PRI chimpanzees have taken part in various experiments, which have examined not only their perceptual and cognitive abilities by testing single subjects but also their social intelligence (Matsuzawa, 2001, 2003; Matsuzawa, Tomonaga, & Tanaka, 2006). First, using the same paradigm with 1/0 (selfish) and 1/1 (mutualistic) options described above, we developed a novel reciprocal paradigm context in the button choice task (Yamamoto & Tanaka, submitted). Previously, only one of two chimpanzees was the actor and chose one or two options, which always provided him/ her with a reward; whether the recipient received a reward or not depended on the choice made by the actor (unilateral condition). However, in this new reciprocal paradigm, the actor-recipient role was reversed alternately in every trial (bilateral condition): in the first trial, Chimpanzee A decided whether to give a reward to a recipient, Chimpanzee B, and in the second trial, Chimpanzee B made his/ her choice, and then Chimpanzee A again. We compared their “reward-giving” performance between the unilateral and bilateral conditions. The prediction was that if chimpanzees have a predisposition for reciprocity, they would choose the 1/1 option more often in the bilateral condition than in the unilateral condition, since they could gain more benefit by reciprocal reward-giving in the bilateral condition, although there was no difference in the amount of rewards to the actor in the unilateral condition whether they chose the 1/0 or 1/1 option. Contrary to our expectation, however, there was also no difference in the choice preference between the two conditions, which implies that this study failed to show reciprocity in chimpanzees. In this study (Yamamoto & Tanaka, submitted), each chimpanzee was put into a room separately, and could not interact physically with the partner. Chimpan- zees have been known to demonstrate some interactions, such as solicitation and recruitment of the partner when necessary, in order to achieve mutual cooperation (Crawford, 1937; Hirata & Fuwa, 2006; Melis, et al. 2006a). Then the question arose: how do chimpanzees behave when put together in reciprocal contexts? Hikami & Matsuzawa (1981) examined whether a pair of non-kin juvenile chimpanzees developed a reciprocal relationship in a “competitive/cooperative situation” (or “social problem situation” in Mowrer, 1940; Oldfield-Box, 1967). In their experiments, when a chimpanzee pressed a lever on a wall, food rewards were delivered on a food tray far away from the lever, so that the participant who actually pressed the lever had less of a chance in getting the rewards than a participant who waited beside the tray. In this situation, both of the two participants Altruism and reciprocity in chimpanzees 159 could have received a food reward if they had alternately adopted the actor’s and recipient’s role. However, they did not. Instead, the dominant monopolized both the lever and rewards, sometimes displaying at their partner. We tested chimpanzee mother–infant pairs in a similar situation using tokens and vending machines instead of the lever (Yamamoto & Tanaka, in press b). The results were the same except that the infant, although physically weaker than the mother, monopolized the food rewards. We also found that both the mother and infant chimpanzees developed some selfish tactics flexibly according to the partner’s behavior, but finally the mothers withdrew and the infants succeeded in monopolizing access to the food reward. The degree of tolerance exhibited in this case by the mother allowed the infant to monopolize the reward. The importance of tolerance has also been highlighted in mutual cooperation tasks (Hare et al. 2007; Melis et al. 2006b). In any case, with chimpanzee mother–infant pairs, we found no evidence of reciprocity in such a situation. Thereafter, we modified the experimental setup so that the chimpanzees could not monopolize the food rewards (Yamamoto & Tanaka, in press a, b). In these studies, two chimpanzees, mother–infant pairs or non-kin adult pairs, were put in two adjacent rooms separated by transparent panels. The chimpanzees could not move to the adjacent room, but could interact physically with the partner through a hole in a panel between the two rooms. Each room was equipped with a vending machine, and when one chimpanzee inserted a token into a vending machine, a food reward was delivered to the other chimpanzee in the adjacent booth. Two conditions were devised: (1) alternate turn-taking condition, in which the participants necessarily had to insert tokens alternately since a single token was sup- plied to one of two participants at a time, and (2) free turn-taking condition, in which they were free to take turns in inserting tokens since a token was given to each of the two subjects simultaneously. Between adult non-related pairs, token insertion persisted in the alternate turn-taking condition, but not in the free turn- taking condition (Yamamoto & Tanaka, in press a). Between chimpanzee mothers and their offspring, they stopped cooperating early on, even in the alternate turn- taking condition (Yamamoto & Tanaka, in press b). Apparent reciprocal cooperation was observed in a very limited way only in the non-kin adult pairs when the condition necessarily demanded that the participants insert tokens alternately. To summarize, the mothers and infants did not establish reciprocal cooperation at all; and the non-kin adults failed to take turns in exhibiting other-rewarding behavior by themselves in order to maintain reciprocal cooperation. The chimpanzees thus failed to spontaneously develop a sharing rule with their partner. 160 Shinya Yamamoto and Masayuki Tanaka

Controversy over conflicting results The results from these studies support the idea that chimpanzees do not spontaneously give food to others (Jensen et al., 2006; Silk et al., 2005; Vonk et al., 2008; Yamamoto & Tanaka, submitted) and fail to build reciprocal cooperative relationships by providing food rewards to each other (Yamamoto & Tanaka, in press a, b, submitted). However, conflicting results have also been emerging. Warneken and Toma- sello (2006) tested captive young chimpanzees, as well as 18-month-old human toddlers, and examined whether or not they helped others achieve their goals. The participants were presented with several situations in which an experimenter (highly familiar human caretaker for the chimpanzees and an unfamiliar male experimenter for the human infants) was having trouble achieving a goal. For example, the experimenter dropped a marker accidentally and reached with an outstretched arm toward the marker while alternating its gaze between the object and the participant and vocalizing his problem (and also calling the chimpanzee participant’s name to attract his or her attention). The chimpanzees in some situations, and the human infants in almost all cases, helped the experimenter: that is, in the case of the example, participants picked up the marker and handed it to the experimenter. Warneken and his colleagues also replicated this paradigm and confirmed that chimpanzees can demonstrate a tendency to help others without any benefit (Warneken, et al., 2007). In their study, they examined whether or not chimpanzees would help an unfamiliar human without any benefit in a similar situation as in the previous experiment, and whether they would continue to do so if help was costly. They also examined chimpanzees’ altruistic behavior between conspecifics. In their experiment, a chimpanzee could help a conspecific enter a booth and get food by releasing a chain which held shut the door between booths.

Figure 3. Solicitation by Pendesa (left) toward Mari (right). Pendesa reached out to Mari through the hole in the panel after inserting tokens. Prior to this reaching, Pendesa had inserted five tokens consecutively, which led five food rewards to Mari. Mari resumed token insertion after this scene. (Yamamoto & Tanaka, in press a) Altruism and reciprocity in chimpanzees 161

The results were all positive. Warneken et al. (2007) concluded that chimpanzees share crucial aspects of altruism with humans. In the cases of reciprocal contexts in our token experiments, although the adult chimpanzees did not spontaneously take turns in other-rewarding token insertion, we observed direct interactions which could be interpreted as solicitation (Yamamoto & Tanaka, in press a). A chimpanzee (Pendesa) poked out her arm towards her partner (Mari) through a hole in the panel separating the two booths, when Mari did not insert tokens while Pendesa did (Figure 3). After being reached by Pendesa, Mari sometimes took turns and inserted some tokens. How should we evaluate the previous positive and negative results on chimpanzees’ altruism and reciprocity? It is too early to conclude based on these few studies in an all-or-none principle whether or not chimpanzees show altruism and/or reciprocity. However, we think it is reasonable and constructive to pinpoint the differences in the experimental setups and procedures which might influence the results. This effort may help us understand where the contradictory results come from. We summarized the previous experimental studies in Table 1, and found some important and maybe relevant differences not only in their results but also in their experimental setup and procedures. Next, we examined the influence of these differences upon altruism and reciprocity in chimpanzees, dividing possible influential factors into the following three categories: (1) request from recipients, (2) punishment, and (3) characteristics of what was transferred during the interactions.

Table 1. Summary of previous experimental studies and their results on chimpanzees’ altruism and reciprocity. Studies Results Target behavior Recipients’ request Altruism Warneken & Tomasello, 2006 positive instrumental yes helping Warneken et al. 2007 positive instrumental yes helping Vonk et al. 2008 negative food delivery yes Silk et al. 2005 negative food delivery no Jensen et al. 2006 negative food delivery no Yamamoto & Tanaka, submitted negative food delivery no Reciprocity Hikami & Matsuzawa, 1991 negative food delivery no Yamamoto & Tanaka, submitted negative food delivery no Yamamoto & Tanaka, in press b negative food delivery no Yamamoto & Tanaka, in press a negative/ food delivery yes (infre- positive quently) 162 Shinya Yamamoto and Masayuki Tanaka

Factors influencing altruism and reciprocity in chimpanzees

Request from recipients Although many anecdotes and examples of altruistic behavior have been reported, most studies focused only on the end result of animals’ interaction. Thus few studies examined what was actually occurring during the interaction, especially with regards to the recipients’ behavior at the time (but see Vonk et al. 2008; Warneken et al. 2007). The function of the behavior might be different according to whether it is initiated by the giver or the recipient, and as Warneken et al. pointed out, it is highly possible that the recipients’ behavior has a lot of influence on the transfer of the service. It may therefore be helpful to review the results of the previous experimental studies with chimpanzees in the light of the recipients’ behavior. The studies which reported positive results for chimpanzees’ altruistic tendencies (Warneken & Tomasello, 2006; Warneken, et al., 2007) included recipients’ salient request in their experimental procedures. The chimpanzees helped a human who explicitly expressed his need for help by reaching with an outstretched arm towards an object while alternatively gazing back and forth between the object and the participant and vocalizing not only his problem but sometimes also iterating the chimpanzee’s name. Under these circumstances, these behaviors might have facilitated the captive chimpanzees’ understanding of the problem faced by the human. Warneken et al. (2007) also reported that the chimpanzees were less helpful when the human did not express his need explicitly. In one of the three experiments in their study, chimpanzees helped conspecifics. In this study, chimpanzee helpers unlocked a door by releasing a chain, and enabled the partner to enter a room containing food reward. In this case, the partner’s desire might have been explicitly expressed in his/her behavior by rattling the door and chain. Based on these results, Warneken and his colleagues suggested that chimpanzees might understand the partner’s goal when it is salient for the helpers. In contrast, in the experiments conducted by Silk et al. (2005), Jensen et al. (2006), and Yamamoto and Tanaka (submitted), which reported negative results concerning chimpanzees’ altruism or prosociality, a possible explicit request by the recipient was potentially prevented since the actor and the recipient were in separate rooms and it was difficult for them to interact with each other physically. In Vonk et al.’s (2008) study, the potential recipient demonstrated requesting behavior, but it did not affect the choice of the partner between 1/1 and 1/0. How- ever, again, the chimpanzees were restricted in direct interaction and might have had difficulty in understanding what the partner was requesting. It might also be possible that the chimpanzee actor was concentrating on the food in front of him Altruism and reciprocity in chimpanzees 163 or her, rather than paying attention to the partner’s behavior (we will discuss this matter in detail latter in the section “What to share”). The recipient’s request may be a necessary condition but not a sufficient condition for chimpanzees’ altruism. This viewpoint is also applicable to the results of the button choice experiments (Yamamoto & Tanaka, submitted) and the token experiments (Yamamoto & Tanaka, in press a) examining reciprocity in chimpanzees. In both studies, two chimpanzees were separated into two adjacent booths and their physical interactions were restricted, although in the latter study (Yamamoto & Tanaka, in press a) chimpanzees could contact each other physically through a hole in the panel. In these two experiments, chimpanzees did not build reciprocal cooperative relationship spontaneously. However, one chimpanzee (Mari) was observed to sometimes, but not always, respond to the other individual’s (Pendesa) requesting or soliciting behavior (Yamamoto & Tanaka, in press a). This might be a good example of the influence of the recipients’ behavior in the context of reciprocity. The idea that chimpanzees show altruistic behavior upon recipients’ request is also supported by the findings from previous observational studies. In food transfer among chimpanzees, there are few cases of active sharing without recipients’ request. Teleki (1973) reported that just 1.2% of meat transfer among chimpanzees were active sharing, in another words, donations. The majority of the sharing is passive and follows begging behavior performed by recipients (Boesch & Boesch, 1989; Goodall, 1986; Wrangham, 1975). Wrangham (1975) had proposed a sharing-under-pressure hypothesis, similar to the tolerated-theft hypothesis of Blurton-Jones (1989), to explain the phenomenon and evolution of food sharing: food owners share because it is in their own self-interest; that is, they avoid high costs associated with beggar harassment (see also Stevens & Stephens, 2002). This hypothesis was supported by an observational study (Gilby, 2006) and an experimental study (Stevens, 2004). De Waal (1989) refutes the sharing-under-pressure hypothesis by proposing the fact that the most generously sharing individuals were often dominant individuals, who had little to fear from anybody around them. However, harassment may not necessarily impose explicit physical threat to food possessors, but can cause psychological distress or discomfort. Ueno and Matsuzawa (2004) found that food transfers from captive chimpanzee mothers to their dependent infants less than two years old were also predominantly initiated by the infants’ request. They also found that the items actively given by the mothers to their infants were only unpalatable food parts, while palatable parts were rather transferred during infant-initiated-sharing. Tanaka and Yamamoto (in press) also reported that tokens exchangeable for food were transferred between chimpanzee mothers and their offspring only upon recipients’ request including poking hands, vocalizing and/or whimpering. The infants could not actually impose any physical harm to 164 Shinya Yamamoto and Masayuki Tanaka

the adults, but their begging was effective and successful in preventing the mothers from keeping food or tokens for themselves. It is highly possible that chimpanzees do not read the implicit mental state of other individuals, and do not really show voluntary, self-initiated, altruistic behavior. We should be cautious before concluding that the apparently altruistic helping behavior was really altruistic and other-regarding. It is difficult to distinguish between harassment and friendly requesting behavior. For example, how can we assign a cute baby’s crying as a favorable request, but not harassment? If recipients’ behavior can be interpreted as harassment, actors’ apparent altruistic behavior might be a byproduct of mutualism, selfishly pursuing their own immediate benefit or avoiding some physical cost or psychological disgust, as is predicted by the sharing-under-pressure or tolerated-theft hypothesis (Blurton-Jones, 1984; Stevens & Stephens, 2002; Wrangham, 1975). However, this point of view does not diminish the significance of the positive results for chimpanzees’ altruism and reciprocity. The positive results at least clearly show that chimpanzees have an ability to respond to the other individuals’ requests. In our token experiments (Yama- moto & Tanaka, in press a), the chimpanzee Mari sometimes responded to her partner’s (Pendesa’s) request by inserting her tokens so that Pendesa could receive a food reward. This suggests that Mari chose the altruistic option and responded to Pendesa’s request rather than ignoring it and not inserting tokens although Mari could avoid the request by staying away from Pendesa. In this section, we discussed the influence of recipients’ request on chimpanzees’ altruistic and reciprocal behavior. Request, in other words, begging, solicitation or sometimes maybe harassment, is the behavior which may directly encour- age the other to cooperate. Animals may also act against non-cooperators after the course of interaction, which may change the other’s behavior in the next interaction. Sanction against non-cooperators after their defection is called punishment (Clutton-Brock & Parker, 1995; Stevens, 2004). Next, we would like to discuss the existence and influence of punishment in chimpanzees.

Punishment Punishment is a behavior which imposes a cost on cheaters and defectors after the interaction and which discourages or prevents them from repeating the initial action (Clutton-Brock & Parker, 1995), while harassment, another form of sanction, imposes cost on non-cooperators during the interaction (Stevens, 2004). Punishment is considered to play a significant role in maintaining cooperation (Clutton-Brock & Parker, 1995; Gintis, Bowles, Boyd, & Fehr, 2003; Henrick & Boyd, 2001). Humans have unique social systems where the benefit of punishment can extend to others in the group (“altruistic punishment”: Fehr & Gächter, 2002). Altruism and reciprocity in chimpanzees 165

The combination of this “altruistic punishment” and reciprocity form a unique cooperative relationship known as “strong reciprocity” in humans (Fehr & Gächter, 2002; Gintis, et al., 2003). Chimpanzees may also punish non-cooperators. We reported some interesting, although anecdotal, behaviors in chimpanzees in the token experiment (Ya- mamoto & Tanaka, in press a). A chimpanzee (Pendesa) was observed to attack her partner (Mari) aggressively after sessions in which Mari inserted a smaller number of tokens than Pendesa. This aggression might have been derived from Pendesa’s punitive motivation, although this aggressive behavior did not have a positive influence on Mari’s token insertion in the next day’s session. De Waal and Luttrell (1988) observed agonistic interventions in chimpanzees and two species of macaques, and found significant reciprocal correlations with regard to harmful interventions only in chimpanzees. De Waal and Lutterell called this negative reciprocity “revenge system”; that is, if A often intervened against B, B did the same to A. Such aggression against defectors and revenge systems has also been reported in rhesus macaques (Hauser, 1992) and male bonnet macaques (Silk, 1992). Jens- en, Call, and Tomasello (2007b) experimentally examined whether chimpanzees react to the other’s harmful actions by retaliating, and whether they respond to disproportionate outcomes by behaving spitefully. The captive chimpanzees did not inflict costs on conspecifics by knocking food away if the outcome alone was personally disadvantageous, but did retaliate against conspecifics who actually stole the food from them. Jensen et al. (2007b) concluded that chimpanzees are vengeful but not spiteful. The previous observational and experimental studies suggest that chimpanzees are retaliatory and negatively reciprocal. Considering this together with the request described above, it is possible that chimpanzees have something like mea- sures against defectors. Recipients’ behavior might play an important role in chimpanzees’ altruism and reciprocity. So far, however, there has been no empirical evidence to show that retribution reinforces prosocial behavior through reciprocity. Jensen et al. (2007b) reported that revenge failed to cause a decline in harmful behavior (theft). Yamamoto and Tanaka (in press a) also found no increase of Mari’s other-rewarding token insertion after being attacked. If retaliation has no effect in changing recipients’ behavior, it does not contribute to the maintenance of reciprocal cooperation, although the failure of the previous studies to show a positive effect of retribution might be due in part to the experimental procedures. Future studies to investigate empirically how punishment influences the other’s behavior and cooperation in non-human animals would be most welcome. 166 Shinya Yamamoto and Masayuki Tanaka

What to share Warneken et al. (2007) discussed the influence of chimpanzees’ attitude toward food rewards over their prosocial tendency. In their experimental studies (Warnek- en et al, 2007; Warneken & Tomasello, 2005), positive results for chimpanzees’ altruism were gained from experiments with no food, while negative results arose from experiments using food (Jensen et al., 2006; Silk et al., 2005; Vonk et al., 2008; Yamamoto & Tanaka, submitted). What kind of items or service shared or transferred between participants also appears to strongly influence the chimpanzees’ behavior. In one of three experiments conducted by Warneken et al. (2007), the chimpanzees helped a conspecific partner gain access to food. However, the helping behavior itself involved unlocking a door, but no direct transfer of food. Since there was no possibility for the helper to gain any food in that situation, the helper’s attention might be given to the partner rather than the food. In two experiments in Jensen et al. (2006) which produced contradictory results (regarding other-regarding behavior), the situation was similar in that the actor never received food for themselves. In their experiments, however, the chimpanzees had previously had experience with obtaining food rewards from the same apparatus in the preceding test. The chimpanzees might therefore have lost their motivation to participate in the tests when they found no food on the tray for themselves. Indeed, the chimpanzees chose to do nothing in more than 50% of the trials in that condition. When food is presented to chimpanzees, it is highly possible that they are just concentrated on the food in front of them, and that their cognitive processing is overwhelmed by the incentive for food. Boysen and her colleagues found that a response disposition to high-incentive food stimuli introduced a power- ful interference effect on cognitive task performance in chimpanzees (Boysen & Berntson, 1995; Boysen, Berntson, Hannan, & Cacioppo, 1996). Although some previous studies demonstrated chimpanzees’ inhibition control in the presence of food, that is, chimpanzees could choose a large, delayed reward rather than small, immediate reward (Defour, Pelé, Sterck, & Thierry, 2007; Rosati, Stevens, Hare, & Hauser, 2007), this can also be interpreted as indicating that the larger amount of food reward in front of them was very compelling for the chimpanzees. Overall, it is possible that chimpanzees are attracted to and cannot release their attention from food just in front of them. This suggests that the strong incentive for food may hinder the altruistic and reciprocal tendency of chimpanzees, if any such tendency exists. Previous experimental studies have also suggested that chimpanzees are primarily competitive over food with conspecifics (Hare, 2001), even between mothers and infants (Yamamoto & Tanaka, in press b; for chimpanzees’ token competi- Altruism and reciprocity in chimpanzees 167 tion see also Tanaka & Yamamoto, in press). Hare and his colleagues succeeded in showing chimpanzees’ high social intelligence in competitive paradigms using food (Hare, Call, Agnetta, & Tomasello, 2000; Hare, Call, & Tomasello, 2001, 2006), and also found that a competitive paradigm rather than a cooperative paradigm is more applicable for testing chimpanzees’ behavior and cognition (Hare & Tomasello, 2004). Chimpanzees might become particularly self-regarding with food in front of them. Therefore, an experimental paradigm using food might not be ideal to examine altruism and reciprocity in chimpanzees. We might be able to obtain different results from experiments in which interaction among chimpanzees is mediated by non-food items or services. Boysen and her colleagues also found that when Arabic numerals were substituted for the real food, all the chimpanzees, free from the spell of a strong incentive for food, showed an immediate increase in performance in cognitive tasks (Boysen & Bern- tson, 1995; Boysen et al., 1996). More recently, Brosnan et al. (2007) found that chimpanzees exhibit an endowment effect in which chimpanzees favored items they had just received more than their preferred items that could be acquired through exchange, and that the effect was stronger for food than for less evolutionarily salient objects. The incentive for food might be overwhelmingly strong for chimpanzees. In contrast, non-food objects or services may be better “tools” for examining chimpanzees’ prosocial behavior. The chimpanzees’ failure to exhibit altruism and reciprocity in the previous experimental setups using food does not contradict field observations. In the wild, chimpanzees are omnivorous, but almost all populations studied (e.g. Goodall, 1986) depend primarily on fruits, which can normally be acquired without any kind of cooperation. It is basically unnecessary for chimpanzees to share their daily food with conspecifics. Nutritional intake from meat obtained through cooperation in the form of group hunting and subsequent meat sharing is trivial in quantity (Stanford, Wallis, Matata, & Goodall, 1994; Teleki, 1973), and is not so important or essential to the individual’s diet (Milton, 1999; 2003). Although plant food sharing has also been reported at several field sites (Bethell, Whiten, Muhumaza, & Kakura, 2000; Hockings et al., 2007; Nakamura & Itoh, 2001; Slo- combe & Newton-Fisher, 2005), it is quite infrequent. Although several studies have suggested that food is exchanged in a reciprocal manner for another service such as alliances and affiliative relationships (e.g. Mitani & Watts, 2001), the recent study conducted by Gilby (2006) found that sharing-under-pressure hypothesis (Wrangham, 1975) rather than reciprocity is more applicable to explain chimpanzees’ meat sharing at least in Gombe National Park in Tanzania (see also Stevens & Gilby, 2004 for review). Gilby and his colleagues also suggested from the long-term data in Gombe (Gilby, Eberly, Pintea, & Pusey, 2006) and Kibale National Park in Uganda (Gilby & Wrangham, 2007) that patterns of hunting can be explained by 168 Shinya Yamamoto and Masayuki Tanaka

simpler ecological factors rather than social, collaborative factors as previously suggested (Boesch, 2003; Boesch & Boesch, 1989).

Discussion and conclusion

Characteristics of chimpanzee’s altruism By reviewing the recent experimental studies on altruism and reciprocity in chimpanzees, we found that chimpanzees’ altruistic or reciprocal behavior is restricted by recipients’ behavior and depends on the characteristic of items or services transferred between individuals. The conditions in the studies conducted by Warneken and colleagues (Warneken & Tomasello, 2006; Warneken et al. 2007), which provide rare experimental evidence for chimpanzees’ altruism, met these requirements, i.e. the recipients’ request and absence of food. It might not be necessary to meet both of these requirements but neither alone may provide sufficient conditions for the expression of altruism and reciprocity. Chimpanzees did not show any prosocial choice with food even when the recipient demonstrated the request (Vonk et al. 2008). They also handed objects to a human experimenter less frequently when the human did not request (Warneken et al. 2008). It seems clearer that chimpanzees seldom show altruistic behavior when neither of the two requirements are met, that is, with food and without the recipients’ request. In this paper, we have mainly discussed chimpanzees’ altruism and reciprocity by reviewing previous experimental studies. Now we would like to expand our view to field studies more fully. Our findings fit with the patterns of evidence from the wild. Helping behavior in a context not involving food has been frequently reported (de Waal, 1996; Goodall, 1986; also see Figure 1). Agonistic support and allogrooming are such examples, and these behaviors may occur even in the absence of the recipient’s request. Hockings, Matsuzawa and Anderson (2006) reported cooperative road crossing among Bossou chimpanzees in Guinea, in which males’ leading or rearward positioning maximized group protection. This is also an example of cooperation outside of a food context, although it is difficult to say whether this cooperation is altruistic, mutualistic, or kin-biased, as it concerns the “group” rather than a specific individual. In contexts involving food, voluntary altruism in the form of active food sharing without the recipient’s request is very rare especially in meat sharing (Boesch & Boesch, 1989; Goodall, 1986; Teleki, 1973; Wrangham, 1975). Although there have been some reports of active plant-food donation (Bethell, Whiten, Muhumuza, & Kakura, 2000; Hockings et al., 2007; Humle, Hockings, Ohashi, & Matsuzawa, 2008, although Hockings et al. did not categorize types of sharing), these can also be considered as rare examples, Altruism and reciprocity in chimpanzees 169 and there are alternative explanations to the sharing behavior other than altruism in a strict sense. For example, it is possible that the sharing of fruits have occurred because the fruits (e.g., Treculia africana fruits and papaya fruits) were enough large for two or more individuals to share (Humle et al., 2008). Therefore, it might have been sharing of surplus parts, which may be conceptually comparable to active sharing of inedible food parts between a chimpanzee mother and infant (Ueno & Matsuzawa, 2004). To summarize, the evidence from the wild support our idea that chimpanzees are not altruistic when neither of the two requirements, i.e. the recipient’s request and absence of food in the interaction, are met. The importance of the recipient’s request might also propose a new implica- tion on the mechanism for reciprocity. Previous studies have mainly examined the donor’s behavior (e.g., de Waal & Berger, 2000; Hauser, Chen, Chen, & Chuang, 2003), focusing on the donor’s motivation, such as gratitude (Emmons & Mc- Cullough, 2004). However, the behavior of the recipient may be more important in initiating and maintaining a reciprocal cycle; that is, a previous donor dem- onstrates a request as a recipient, and in turn the previously recipient partner re- sponds to the request as a donor. Chimpanzees, as well as other animal species, might achieve reciprocal cooperation through a “recipient-initiated” cycle rather than through a “donor-initiated” cycle.

Possible scenario for the explosion of cooperation in humans On the basis of these findings, we would like to propose two hypotheses which might explain altruistic or reciprocal behavior in the common ancestor of humans and chimpanzees: (1) “recipient-initiated altruism” hypothesis, and (2) “non-food altruism” hypothesis. Although we already described in detail the two characteristics in chimpanzees, again we would like to explain the core of the two hypotheses, contrasting them with some characteristics which might be unique to human altruism. We will also briefly propose a scenario for the evolution of altruism in humans (Figure 4). Recipient-initiated altruism hypothesis predicts that altruistic behavior occurs upon the other’s request. Animals may respond to the other’s direct request when altruistically behaving or reciprocating. In this form of altruism, animals do not need to estimate or identify the other’s subtle mental state, and therefore any complex psychological mechanism which may play an important role in voluntary altruism in humans, such as theory-of-mind and/or perspective-taking, is not required. “Gratitude” (Emmons & McCullough, 2004) is also not considered as a necessary underlying mechanism for recipient-initiated altruism and reciprocity. If recipient-initiated altruism were the predominant component of prosocial behavior in the common ancestor of humans and chimpanzees, it may be possible 170 Shinya Yamamoto and Masayuki Tanaka

Uniquely human evolution – Elaborated social cognition – Language and social norm – Necessity of food sharing – Enriched material culture Humans Possible explosion of altruism (including voluntary altruism and frequent food donation)

Chimpanzees Shared characteristics – Recipient-initiated altruism – Non-food altruism

Figure 4. Schematic diagram of possible explanation for the evolution of altruism since the common ancestor between humans and chimpanzees.

to consider that altruism exploded in humans after divergence from the common ancestor. The recipient-initiated altruism hypothesis also predicts that the common ancestor seldom showed voluntary altruism and that voluntary altruism is practically absent in non-human animals. Although there is some evidence for theory of mind (Call & Tomasello, 2008) and/or empathy (de Waal, 2008) in chimpanzees, these social cognitive abilities might be obvious only when the others’ goals or psychological states are explicitly exposed, particularly in the form of request. And therefore, these are not sufficient abilities for voluntary altruism. Therefore a form of altruism unique to humans may be altruism without request. Humans might have developed this voluntary altruism alongside the acquisition of uniquely human social skills, such as sharing intentions (Tomasello et al., 2005), understanding others’ belief and desire (Call & Tomasello, 2008), triadic interactions (Tomonaga et al., 2004), and/or maybe others. Language might also have promoted the evolution of altruism in humans. Re- quest represented in the form of gesture is sometimes ambiguous. In our daily interactions with chimpanzees, we sometimes run into situations where we accidentally drop an object into the chimpanzees’ enclosure, but cannot reach it due to bars which act as a barrier between human and chimpanzee areas. In such cases, we call a chimpanzee over and ask him or her by gestures to retrieve the object for us. However, chimpanzees often give us stones, twigs or something we do not Altruism and reciprocity in chimpanzees 171 actually want. It seems easy for chimpanzees to understand that we are requiring “something”, but sometimes difficult for them to figure out exactly what we need. This is also suggested from the results in Vonk et al’s (2008) study, in which chimpanzees failed to comply with the partner’s request. In humans, on the other hand, language can convey exactly what we desire. In addition, maybe during later stages of human evolution, we came to be able to express an event in the past or in the future. This most certainly enabled important mechanisms for the maintenance of reciprocity, such as reputation (Milinski, Semmann, & Krambeck, 2002; Nowak & Sigmund, 1998, 2005) and social norms (Fehr & Fischbacher, 2004). Together with the development of social skills that enable voluntary altruism, the evolution of language in humans probably play an important role in the explosion of altruism and reciprocity in humans. The second hypothesis, the non-food altruism hypothesis, predicts that altruism and reciprocity occurs in the common ancestor more frequently with non-food items or services than with food. Three possible mechanisms should be considered. First, sharing food directly imposed more cost on a donor than sharing non-food items. Second, food was so compelling for the common ancestor, as suggested by the experiments with chimpanzees conducted by Boysen and her colleagues (Boy- sen & Berntson, 1995; Boysen, et al. 1996; Boysen, Mukobi, and Berntson, 1999). Third, there was practically no necessity for the common ancestor to share food, de- pending on food items which could be easily gained individually without sharing. This non-food altruism hypothesis, as well as the recipient-initiated altruism hypothesis, may together explain the evolution of altruism in humans. The non-food altruism hypothesis predicts that the common ancestor of chimpanzees and humans had a base for altruistic and/or reciprocal interactions with non-food items or service. Instead of food, tools might have played important roles in the development of non-food altruism. Although voluntary sharing of tools or objects among chimpanzees has been observed not only in captivity (Celli, Tomonaga, Udono, Teramoto, & Nagano, 2006; Yamamoto, Humle, & Tanaka, unpublished data) but also in the wild (Humle, Hockings, Ohashi, & Matsuzawa, 2008), it occurs infrequently. This might be due to chimpanzees’ comparatively lesser dependence on tools in their daily life. Instead, humans are much more dependent on tools and live in a rich material culture. Due to the increased dependence on tools, humans might have come not only to use various tools but also to share and/or exchange some good tools. Social interactions mediated by tools or objects might have become more common, acting as an important selective factor for altruism and reciprocity in our human societies. Enriched material culture might have en- hanced development of social systems based on altruism and reciprocity. Dependence on animal foods in humans might also have played a role as a selection favoring altruism and reciprocity. Chimpanzees, as well as other apes, 172 Shinya Yamamoto and Masayuki Tanaka

take most of their daily diet from plant sources, although they take important trace nutrients from small quantities of animal foods including not only vertebrate prey but also invertebrates such as ants (Milton, 2003). In contrast, it is suggested that humans have to take high quality, volumetrically concentrated amounts of food for the growth and maintenance of a large brain, and therefore insectivory and meat- eating probably became particularly important in human evolution (Milton, 1999, 2003). Although important, however, meat and insects are more difficult to obtain than plant foods. In order to obtain meat regularly, humans might have achieved more customary cooperation in hunting and food sharing compared to chimpanzees. In fact, food sharing is prevalent and plays an important role among humans (Gurven, 2004). Humans might have uniquely expanded and developed altruism in the form of food sharing according to the increase of our dependence on meat.

Future prospects So far, there are still not enough experimental studies investigating altruism and reciprocity in chimpanzees, and also in other apes. Particularly studies in bonobos are lacking. The bonobo is also one of our closest living relatives, and therefore humans should share some common traits with bonobos as well as with chimpanzees, or maybe even more so than with chimpanzees (e.g., a shared microsatellite element between humans and bonobos, but not chimpanzees: Hammock & Young, 2005). Interestingly, although the chimpanzee and the bonobo are evolutionarily very close, there are significant differences between the two species in their social behavior (de Waal, 1988; Boesch, Hohmann, & Marchant, 2002). For example, bonobos establish peaceful relationships with conspecifics through sexu- al interactions (Kano, 1980; Kuroda, 1980), while chimpanzees’ societies are rather competitive (Hare, 2001). Hare et al. (2007) revealed that bonobos outperform chimpanzees on a mutually cooperative task due to greater social tolerance among bonobos than among chimpanzees. This suggests similarity in cooperative behavior between humans and bonobos rather than chimpanzees. If social tolerance is a determining factor in the evolution of altruism and reciprocity, bonobos should show similarity with humans in altruism and reciprocity. However, if the other factors we pointed out above such as language and enriched material culture are more important for the evolution of human prosociality, bonobos’ performance would be similar to that of chimpanzees rather than that of humans. Unfortunately, to date, there have been practically no experiments, to our knowledge, on altruism and reciprocity in bonobos. Comparative studies with bonobos are essential for a better understanding of the evolution of altruism and reciprocity in humans. Comparative studies with other non-human primates and non-primate animals are also important in order to investigate the phylogenetic origin of human Altruism and reciprocity in chimpanzees 173 altruism and reciprocity as well as to understand what factors, ecological and/or social, have influenced its evolution. More and more experimental evidence for and against altruism and reciprocity in other animals is now available. Particu- larly, regarding altruism or prosociality, experiments adopting the paradigm of 1/1 (mutual) vs. 1/0 (selfish) or 0/1 (altruistic) vs. 0./0 (weak spiteful) choices have come to suggest species differences. In contrast to chimpanzees, who have never shown any prosocial tendency in this paradigm with food (Jensen et al., 2006; Silk et al., 2005; Vonk et al., 2008; Yamamoto & Tanaka, submitted) as mentioned above, some New World monkeys have performed other-rewarding choice (common marmosets: Burkart, Fehr, Efferson, & van Schaik, 2007; tufted capuchin monkeys: de Waal, Leimgruber, & Greenberg, 2008; Lakshminarayanan & San- tos, 2008), although cottontop tamarins did not show such a tendency (Cronin, Snowdon, & Silk, 2008). In macaques, there has been much less evidence, and the results are mixed, that is, all types (altruistic, selfish, and no regarding tendencies) were observed (Macaca mulatta and M. speciosa: Colman, Liebold, & Boren, 1969). As for reciprocity, there have also been some experimental results support- ing the capacity of reciprocity in cottontop tamarins (Hauser et al., 2003; Cronin & Snowdon, 2008) and tufted capuchin monkeys (de Waal & Berger, 2000; Hattori, Kuroshima, & Fujita, 2005), although no experiments have investigated the role of turn-taking, an important component in reciprocity as suggested by our previous experiment with chimpanzees (Yamamoto & Tanaka, in press a). It may therefore be still too early to give some conclusions about the phylogenetic evolution of altruism and reciprocity. Experiments have advantages in controlling contingency, manipulating the amount of cost and benefit, and examining behavioral sequences in controlled conditions, which enables direct comparative studies with various species under similar conditions. We propose the importance of detailed analysis of the animals’ behavior. To understand the mechanism of sharing behavior, for example, it may be more helpful to analyze how the item is transferred between individuals by cod- ing both the actors’ and recipients’ behavior, rather than recording based on an all- or-none principle — whether or not transfers occurred. Proximate factors might be different between active and passive sharing, even though ultimate factors may be the same. In addition, empirical studies investigating the role of punishment are needed. It may also be interesting to compare experiments involving food and those that do not, in establishing the influence of the presence of food on altruistic or reciprocal behavior in animals. Suppose that we give a chimpanzee tool A and food B which can be obtained only by using tool B, while supplying the other individual with tool B and food A which requires tool A, will the chimpanzees “exchange” the tools? Savage-Rumbaugh, Rumbaugh, and Boysen (1978) reported tool trans- 174 Shinya Yamamoto and Masayuki Tanaka

fer between human-raised juvenile chimpanzees in a similar situation; however, although the results were interesting, particularly in that the tool exchange was mediated by symbolic communication, the giving behavior could be interpreted as a behavior artificially shaped by human praise and reward. It might be worthwhile to replicate this kind of test without training from the viewpoint of altruism and reciprocity, and also from the comparative point of view between food and tool. If tools rather than food solicit altruism and/or reciprocity in chimpanzees, then it may suggest an interaction between material intelligence and social intelligence. Some studies have previously suggested the correlation between the two. For example, Visalberghi and Tomasello (1998) discussed primates’ understanding of “causality” which is related to both the physical and psychological world. Here we propose the possibility that apparently two independent or non-related factors, using tools and cooperating with others, can also stimulate each other. Enriched material culture would solicit social exchange. And this would allow the existence of division of labor and the emergence of “specialists” who only make specific tools. This, in turn, would lead to sophistication in material culture. This idea of a co-evolution between material intelligence and social intelligence might explain in part the reason why material technology, symbol use, and complex social system in humans have evolved quickly in a comparatively evolutionarily short period of time (Tomasello, 1999). To understand further the evolution of altruism and reciprocity, collaborative work among various fields would also be welcome. In humans, neuroscience has achieved a remarkable breakthrough, and has revealed aspects of the human “social brain”, for example, the perception of fairness (Singer, et al., 2006). On the other hand, neurophysiological studies exploring endogenous neural activities have rarely been reported in non-human hominid species, due to the practical difficulties in conducting non-invasive measurements on awake individuals. Re- cently, however, Ueno et al. (2008) succeeded in measuring auditory event-related potentials (ERPs) in a fully awake chimpanzee. Using this kind of methodology, it may be possible to study and compare social cognition and neural processing between chimpanzees and humans. Some recent studies also succeeded in incorporating methodologies using physiological indicators, such as heart rate (Parr, 2001), and brain and skin temperature (Parr & Hopkins, 2000). Developmental studies are also essential to understand how young achieve the complex social interactions with others during different ontogenetic stages. Studies on human infants will especially provide useful insights into the influence of language, social norms or reputation upon the development of altruism and reciprocity. We expect that an interdisciplinary approach will generate fruitful advances in our understanding of the evolution of prosociality. Altruism and reciprocity in chimpanzees 175

Acknowledgements

This work was financially supported by grants (#16002001 and #20002001 to Tetsuro Matsu- zawa) from the Ministry of Education, Culture, Sports and Technology (MEXT), Japan, by the Global COE Program A06 and D07 of MEXT to Kyoto University, and by grants from the Japan Society for the Promotion of Science for Young Scientists (#18–3451 to Shinya Yamamoto). We would like to thank Tetsuro Matsuzawa, Masaki Tomonaga, Tatyana Humle and many other colleagues at the Section of Language and Intelligence, the Primate Research Institute (PRI), Kyoto University for their support and comments on this study. Three anonymous review- ers also kindly gave helpful comments on our manuscript. Thanks are also due to Juri Suzuki, Takako Miyabe, Akino Watanabe, Kiyonori Kumazaki, Norihiko Maeda, Shohei Watanabe, Rui Hirokawa, and other staff members for veterinary and daily care of the chimpanzees at the PRI, Kyoto University.

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Author’s addresses Shinya Yamamoto Masayuki Tanaka Great Ape Research Institute, Wildlife Research Center, Kyoto University Hayashibara Biochemical Laboratories, Inc. 2-24 Tanaka-Sekiden-cho, Sakyo, Kyoto, 952–2 Nu, Tamano, Okayama, 6068203, Japan 7060316, Japan [email protected] [email protected]

About the authors Shinya Yamamoto is a postdoctoral fellow at the Japan Society for the Promotion of Science for Young Scientists, University of Tokyo, and Great Ape Research Institute, Hayashibara Biochemi- cal Laboratories, Inc (GARI). He received a Ph. D. in Science from Kyoto University in 2009. His current research focuses on chimpanzees’ social intelligence, especially altruism, reciprocity, and understanding of others. He conducted experiments for these five years at the Primate Research Institute, Kyoto University, and is now continuing his chimpanzee study at GARI. Masayuki Tanaka is Associate Professor at the Wildlife Research Center, Kyoto University. He worked as Assistant Professor at the Primate Research Institute, Kyoto University and participat- ed in research on chimpanzee cognitive development. He also collaborated with S. Yamamoto on studies of chimpanzees’ social intelligence. He holds a Ph.D. from Kyoto University.