To Each According to his Need? Variability in the Responses to Inequity in Non-Human Primates

Abstract

While it is well established that humans respond to inequity, it remains unclear the extent to which this behavior occurs in our non-human primate relatives. By comparing a variety of species, spanning from New World and Old World monkeys to great apes, scientists can begin to answer questions about how the response to inequity evolved, what the function of this response is, and why and how different contexts shape it. In particular, research across non-human primate species suggests that the response is quite variable across species, contexts, and individuals. In this paper, we aim to review these differences in an attempt to identify and better understand the patterns that emerge from the existing data with the goal of developing directions for future research. To begin, we address the importance of considering socio-ecological factors in non-human primates in order to better understand and predict expected patterns of cooperation and aversion to inequity in different species, following which we provide a detailed analysis of the patterns uncovered by these comparisons. Ultimately, we use this synthesis to propose new ideas for research to better understand this response and, hence, the evolution of our own responses to inequity.

Appendix

Chimpanzees

Chimpanzees (Pan troglodytes) are great apes, and one of our two closest living relatives (along with bonobos, Pan paniscus). Chimpanzees are highly social, living in large fission–fusion groups with complex social relationships and strong dominance hierarchies (de Waal, 1989; Harcourt & Waal, 1992). Males are philopatric and remain in their natal social communities, forming strong social bonds, while females emigrate when they reach adolescence. Chimpanzees also cooperate, for instance in territorial patrols (Boesch & Boesch-Achermann, 2000) or when hunting in groups (Boesch, 1994; Mitani & Watts, 2001). Although food sharing is in general rare outside of mothers and offspring (Goodall, 1986; Silk, 1978; although see Pruetz & Lindshield, 2011), meat sharing occurs (Goodall, 1986; Nishida, Hasegawa, Hayaki, Takahata, & Uehara, 1992), often in return for agonistic support (Mitani & Watts, 2001) or mating opportunities (Gomes & Boesch, 2009). Males may also share hard-to-get cultivated fruits with females (Hockings et al., 2007). The wide range of tolerant, cooperative behavior in the wild suggests that chimpanzees are aware of each other’s behaviors and the distribution of payoffs received through these interactions.

Chimpanzees also show a number of behaviors indicative that they pay attention to the equity of distributions. For instance, in laboratory cooperation studies, in which individuals must work together to acquire rewards, chimpanzees who were working for a single reward that must be shared were far more likely to succeed with a partner with whom they otherwise tolerantly share food (Melis et al., 2006b), and actively recruited the more tolerant partner (Melis et al., 2006a). Chimpanzees also were able to coordinate their responses in a Stag Hunt game such that both individuals achieved the highest reward, although this ability seemed to interact with experience, with chimpanzees with a more extensive history of testing outperforming those with less such experience (Brosnan, Parrish, et al., 2011).

Chimpanzees also respond to inequity in experimental studies (following the exchange procedure described in the main body of the text), although responses vary widely, based on factors that are not yet well understood. For instance, chimpanzees’ responses have varied between facilities, even when an identical protocol was used (Brosnan et al., 2005; Brosnan, Talbot, et al., 2010). Within the same facility, responses have varied based on the quality of individuals’ relationships (Brosnan et al., 2005), sex, and rank (Brosnan, Talbot, et al., 2010), with male and dominant chimpanzees responding more negatively to inequity than females and subordinates (when tested in same-sex pairs). These results seem to fit chimpanzee socio-ecology; males form much closer bonds, through coalitions and alliances often associated with hunting and patrolling, and therefore may be more sensitive to differing outcomes, while females spend most of their time foraging alone or with offspring, and so may be more focused on individual expectations. In addition, high-ranking individuals may be more accustomed to receiving a better share of a distribution or a better quality food resource. However, what is important to remember is that this is not always consistent across sites and protocols; sometimes sex and rank differences are seen, but other times they are not (Bräuer et al., 2006, 2009; Brosnan, Talbot, et al., 2010; Brosnan et al., 2005). In addition, even the orientation of the subjects to each other in the experimental set-up appears to make a difference in their responses (Brosnan, Talbot, et al., 2010). Thus, future study is needed to understand how this variation affects responses, and what this tells us about the evolution of inequity responses.

Bonobos

Bonobos (Pan paniscus) differ from chimpanzees in their social structure. Bonobo society is more female-centered, female-dominant, and egalitarian (de Waal, 1995). Males are philopatric and remain in their natal group, while females migrate around adolescence (Idani, 1991; Kano, 1982). Female bonobos have much stronger bonds compared to males, and bonobo females can cooperatively dominate males (Kano, 1992; Parish, 1994, 1996). Bonobos have been observed in the wild and captivity sharing both plants and meat (de Waal, 1992; Hohmann & Fruth, 1993; White, 1994), and may exchange food for mating access (Kuroda, 1984), although recent evidence indicates that chimpanzees may actually be more tolerant sharers (Jaeggi, Stevens, & Van Schaik, 2010). Bonobos have also cooperated in captive experiments, and in such studies were more successful than chimpanzees when food sources were monopolizable (Hare, Melis, Woods, Hastings, & Wrangham, 2007). Only one study has tested the inequity response in bonobos, and although individuals refused rewards twice as often when their partner got a better reward than when they got the same, lower-value reward, the result was not statistically significant, possibly due to the small sample size (Bräuer et al., 2009).

Gorillas

Gorillas (genus Gorilla) live in harems comprised of one adult male (silverback), multiple adult females with their offspring, and sometimes other males (Harcourt, 1978; Robbins, 1995). The silverback has strong bonds with his females (Harcourt, 1979a) but bonds between females vary, ranging from friendly to aggressive interactions (Harcourt, 1979b). In the wild, female gorillas have been observed cooperating and forming alliances in competition over food resources and to protect relatives from harm (Harcourt & Stewart, 2007; Watts, 1997). Although food sharing is rarely reported in the wild, gorillas have demonstrated food sharing in captivity (Maestripieri, Ross, & Megna, 2002; Schaller, 1963). Unfortunately, there is as yet very little captive research on social cognition in gorillas, although one recent study investigating responses to inequities during play fighting (Van Leeuwen et al., 2011) found that individuals worked to maintain inequities in their favor (e.g., running away after hitting, apparently so that the competitive advantage could be maintained). Future study on gorillas is needed to complete our understanding of the great apes.

Orangutans

Orangutans (Genus Pongo) are great apes that, in the wild, have a more solitary lifestyle compared to the other great apes. Although home ranges overlap (Galdikas, 1988), orangutans other than mother–offspring dyads spend most of their time alone (MacKinnon, 1974). Nonetheless, groups of orangutans may travel together, or feed together when fruit is abundant, and in captivity, orangutans show increased social behavior (Edwards & Snowdon, 1980). Based on research in the wild, food sharing among orangutans is rare (Bard, 1992; Jaeggi, van Noordwijk, & van Schaik, 2008; van Noordwijk & van Schaik, 2009). Also, unlike other apes in the wild, orangutans form coalitions and alliances to a lesser degree (van Schaik, 2004). However, the lack of cooperative behavior may again be due to limited opportunities, not limited abilities. In captivity, orangutans have both solved cooperative tasks to achieve food (Chalmeau, Lardeux, Brandibas, & Gallo, 1997) and traded tokens reciprocally to receive mutual benefits (Dufour, Pelé, Neumann, Thierry, & Call, 2009). Despite this, however, orangutans did not show negative responses to inequity (Bräuer et al., 2009; Brosnan, Flemming, et al., 2011).

Macaques

Macaques (genus Macaca) are Old World monkeys, and include two species that have received attention in inequity studies, rhesus macaques (Macaca mulatta) and long-tailed macaques (Macaca fascicularis). Macaques are social, living in large, multi-male, multi-female groups, but tend to be despotic, with low social tolerance, and frequently use aggression to establish and reinforce social position in the asymmetrical dominance hierarchy (Smuts, Cheney, Seyfarth, Wrangham, & Struhsaker, 1987; Thierry, 2000). Although macaques are not known to cooperatively share food, or to successfully cooperate in experimental studies (Petit, Desportes, & Thierry, 1992), they demonstrate other forms of cooperative behavior in the wild. Long-tailed macaques form alliances in aggressive contexts (de Waal, 1977; van Noordwijk & van Schaik, 1985), reciprocate grooming to decrease aggression (Gumert & Ho, 2008), and exchange grooming for access to sexually active females, infant handling, and support (Gumert, 2007a, 2007b; Massen, 2010). Female rhesus macaques show cooperative behavior (grooming and agonistic aid) toward kin (Widdig, Nürnberg, Krawczak, Streich, & Bercovitch, 2001). Possibly connected to this, long-tailed macaques have shown prosocial behavior in the laboratory, choosing options that bring food to their partners (Massen, Van Den Berg, Spruijt, & Sterck, 2010). However, in most cases prosocial behavior was limited to female kin pairs or the dominant member of the pair, the latter of which may have been an attempt to curry favor with the subordinate. In fact, rank predicted prosocial sharing better than did relationship quality (Massen, Luyten, Spruijt, & Sterck, 2011). Related to this, dominant long-tailed macaques showed responses to inequity when the level of effort required was small (Massen, van den Berg, et al., 2011). As with long-tailed macaques, rhesus monkeys coordinated in a Stag Hunt game (Brosnan, Wilson, & Beran, 2012), and also have responded negatively to inequity, although only once they have reached ~2 years of age (Hopper et al., in review).

Capuchin Monkeys

Brown capuchins (genus Cebus) are New World monkeys that live in small groups comprised of related females with offspring and several males. Capuchin society is rather tolerant (Fragaszy et al., 2004); capuchins both share food (Perry & Rose, 1994) and cooperate, including cooperative hunting (Rose, 1997), defense against predators (Boinski, 1988; Rose, 1994), and coalitions against neighboring groups (Gros-Louis, Perry, & Manson, 2003). These coalitions are especially interesting because, unlike chimpanzee males, who form strong bonds and who often form coalitions for aggressive purposes, capuchin males are not philopatric and do not form close affiliative bonds (Perry, 1998).

Capuchins have been widely used in cooperative studies, which have confirmed that they are aware of the contingencies of cooperation, including the role of a partner, the effort required, and the distribution of outcomes (see Brosnan, 2010 for review). Capuchins have also shared food (de Waal, 1997), and after successful cooperative trials, the amount of food shared increased (de Waal & Berger, 2000). On the other hand, in the Stag Hunt game, capuchins showed the least structured coordination behavior compared to humans, rhesus, and chimpanzees, and apparently require cues to be able to coordinate (Brosnan, Parrish, et al., 2011; Brosnan et al., 2012). Capuchins have also demonstrated prosocial preferences, which seem to be affected by dominance rank or social closeness with the partner, whether or not they can see the partner, and reward distribution (de Waal, Leimgruber, & Greenberg, 2008; Takimoto et al., 2010). They have even brought their partner more food than they received (Brosnan, Houser, et al., 2010; Lakshminarayanan & Santos, 2008).

Several studies have confirmed a negative response by an individual when unequal distributions resulted in a partner receiving a better reward (Brosnan & de Waal, 2003; Brosnan, Houser, et al., 2010; Fletcher, 2008; Takimoto et al., 2010; Van Wolkenten et al., 2007).They have also been sensitive to the effort required to perform the task, at least in some contexts (Hattori et al., 2005, but see Fontenot et al., 2007; van Wolkenten et al., 2007). Finally, individuals who were working together for rewards were more sensitive to their partners’ behavior than to their outcomes, continuing to cooperate as long as both the partners received the superior reward sometimes (Brosnan et al., 2006). This latter study demonstrated that they could extrapolate rewards across multiple trials, presumably an essential ability given that cooperative encounters do not result in equal outcomes on every trial.

Squirrel Monkeys

Squirrel monkeys (genus Saimiri) share both a phylogenetic Family and a similar ecology with capuchins, but differ in their social structure and behavior (Boinski, 1999). Most importantly for this discussion, they demonstrate only limited cooperative behavior in the wild. Adult females with neonates will cooperate in anti-predator vigilance and defense (Boinski, 1987), and males form coalitions to immigrate into a new group (Boinski, 1999; Mitchell, 1994). Squirrel monkeys have not been tested experimentally for cooperative behavior, but did show reduced food sharing behavior, except when harassed by a partner (Stevens, 2004). Squirrel monkeys also did not respond negatively to inequity (Talbot et al., 2011).

Tamarins

Tamarins (genus Saguinus) are cooperatively breeding New World monkeys that live in groups in which, typically, only a single female is reproductively active (Sussman & Garber, 1987). Cooperation is vital in tamarin societies; data from the field and captivity have demonstrated that infant survival is directly related to number of caretakers present (Garber, Moya, & Malaga, 1984; Savage, Snowdon, Giraldo, & Soto, 1996; Snowdon, 1996). Food sharing is also common. Field studies show that food sharing is used to help the young locate and obtain prey that may be hard to acquire, and this food sharing decreases as the young become more competent (Rapaport, 2006; Rapaport & Ruiz-Miranda, 2002). Studies in captivity reinforce tamarins’ tendencies to share food (Cronin & Snowdon, 2008; Cronin, Kurian, & Snowdon, 2005; Feistner & Price, 1999, 2000; Price & Feistner, 2001; Rapaport, 1999). Data conflict on whether tamarins are prosocial (Cronin, Schroeder, Rothwell, Silk, & Snowdon, 2009; Cronin, Schroeder, & Snowdon, 2010; Stevens, 2010). Tamarins showed little evidence of an inequity response, although they were more likely to respond negatively to a lower-value reward when any effort was involved (Neiworth et al., 2009).

Marmosets

Marmosets (genus Callithrix) are also New World monkeys that are in many ways similar to tamarins (they share a phylogenetic family and are also cooperative breeders; Koenig, 1995; Sussman & Garber, 1987). Marmosets tend to share food in the wild (Brown, Almond, & Bergen, 2004; Goldizen, 1987) and in captivity (Brown, Almond, Bates, 2005). Group territorial defense is also common (Lazaro-Perea, 2001). In experimental studies, marmosets demonstrated cooperative behavior that depended on the distribution of roles in a cooperative task as well as the tolerance of high-ranking individuals (Werdenich & Huber, 2002) and prosocial behavior (Burkart, Fehr, Efferson, & Van Schaik, 2007). However, marmosets were not sensitive to situations in which a partner received a better reward (Freeman et al., in review).

Owl Monkeys

Owl monkeys (genus Aotus) are also New World monkeys that, while not considered cooperative breeders, are monogamous and rely on dual-parental care for the survival of offspring (Fernandez-Duque et al., 2001; Wright, 1994). Food sharing has been observed in the wild (Wolovich, Perea-Rodriguez, & Fernandez-Duque, 2008) and in captivity (Wolovich, Feged, Evans, & Green, 2006; Wolovich, Evans, & French, 2008). They also exhibit biparental care, a form of cooperation in which males help to transport and groom infants (Rotundo, Fernandez-Duque, & Gimenez, 2002; Rotundo, Fernandez-Duque, & Dixson, 2005; Wright, 1984). However, as with the cooperative breeders, owl monkeys did not respond negatively to inequity in an experimental context (Freeman et al., in review).