Inequity aversion in animals

Inequity aversion in animals is the willingness to sacrifice material pay-offs for the sake of greater equality, something humans tend to do from early age. It manifests itself through negative responses when rewards are not distributed equally between animals. In controlled experiments it has been observed, in varying degrees, in capuchin monkeys, chimpanzees, macaques, marmosets, dogs, wolves, rats, crows and ravens. No evidence of the effect was found in tests with orangutans, owl monkeys, squirrel monkeys, tamarins, kea, and cleaner fish. Due to inconclusive evidence it is assumed that some bonobos, baboons, gibbons, and gorillas may be inequity averse. Disadvantageous inequity aversion is most common, that is, the animal protests when it gets a lesser reward than another animal. But advantageous inequity aversion has been observed as well, in chimpanzees, baboons and capuchins: the animal protests when it gets a better reward. Scientists believe that sensitivity to inequity co-evolved with the ability to cooperate, as it helps to sustain benefitting from cooperation.

The first researchers to discover inequity aversion in animals were Sarah Brosnan and Frans de Waal, in an experiment with five capuchins, described in a 2003 article in Nature. The monkeys tended to refuse to participate in a food-for-token exchange task once they saw another monkey get rewarded more desirable food for equal effort. On some occasions they threw the food back at the human experimenter.

Dozens of studies have been undertaken since. A few experimental paradigms have been used to test inequity aversion. The exchange is most common. Here animals need to hand over a token to the human experimenter in exchange for a food reward. The results and findings are mixed. In terms of refusal rates being higher in inequity conditions than equity, there is substantial variation across species, across studies, and even across individuals within the same studies. Some researchers have argued that small differences in experimental setup can make the effect disappear. For instance, if the animals are not side by side and do not have good visibility of their partner and their actions, or if there is no task and the animals are simply given food. In some species the females do not refuse inferior rewards but the males do; in some other species it was the other way around. Due to low sample sizes, not all studies controlled for sex and rank.

Background

The ability of humans to cooperate is well documented, but its origin is an open question.[1] One key aspect of cooperation is a sense of fairness: the reward an individual gets from cooperating should be fair compared to others or else future cooperation may break down.[2] Humans show a consistent preference for equal over unequal outcomes.[3] A full-blown concept of fairness is typically present in children aged 6, although 3-year-olds already prefer a giver who distributes rewards from cooperation fairly over one who does so unfairly.[4][5] When given the choice to accept an unfair reward, children rejected it if it was less valuable than the reward of their peer (disadvantageous inequity aversion, or also, first-order inequity aversion),[6] researchers Blake et al. found in a study across seven countries. Even if it was more valuable than the reward of their peer, older children in three countries still on average rejected it (advantageous inequity aversion, or also, second-order inequity aversion).[upper-alpha 1][8][6] Disadvantageous inequity aversion is considered a universal feature of human behavior, whereas advantageous inequity aversion may be strongly influenced by cultural norms.[9][10][11]

Humans are not the only cooperative animals.[12] Many species of animals cooperate in the wild.[13] Collaborative hunting has been observed in the air (e.g., among Aplomado falcons),[14] on land (e.g., among chimpanzees),[15] in the water (e.g., among killer whales),[16] and under the ground (e.g., among driver ants).[17] Further examples of cooperation include parents and others working together to raise young[13] (e.g., among African elephants),[18] and groups defending their territory, which has been studied in primates and other social species such as bottlenose dolphins, spotted hyenas, and common ravens.[19] By researching aspects of cooperation in other species, evolutionary psychologists aim to pinpoint when and under which conditions cooperation emerges.[2] With cooperation not being uniquely human, inequity aversion may not be uniquely human either.[20] Fairness in cooperative animals in the wild has also been observed, in particular in primates. Chimpanzees are known to divide the carcass obtained during collective hunting partially based on each individual's contribution to the hunt.[21] Through controlled experiments with animals, researchers look for this behavior and hope to be able to answer the questions of how and why inequity aversion, and cooperative behavior as a whole, evolved.[2]

First research

The first researcher to test inequity aversion in animals was Sarah Brosnan. As a PhD student at Emory University in Atlanta, Georgia, the idea for an experiment came to her during a feeding session with capuchin monkeys. As she was handing out peanuts to the lower-ranked monkeys, an alpha male named Ozzie offered her an orange, a higher-value food, to also get a peanut.[upper-alpha 2] Under guidance of her professor, Frans de Waal, Brosnan set up an experiment to ascertain if capuchins' behavior is influenced by rewards given to others. In a preliminary test with two conditions, capuchins were tested side by side and were either both given a cucumber as a reward, or one was given a cucumber and the other a grape (known to be perceived as a higher-value food). The results indicated that female capuchins might be sensitive to unequal distribution of rewards. Male capuchins did not show any different behavior between the two conditions.[23]

Brosnan subsequently tested five female capuchins in different conditions. As before, the rewards were either equal or inferior to what the other monkey received. Brosnan also tested if it mattered if the other monkey received food as reward for effort or for not doing anything at all. The task the capuchins had to perform was a common exchange task: the experimenter handed the monkey a stone which simply had to be handed back. If done so, the experimenter would give the food reward. In the side-by-side setting the capuchins could see each other's actions and, crucially, each other's rewards. A further control condition was to ascertain if the behavior was caused merely by the presence of the higher-value reward, since primates have long been known to show a contrast effect.[upper-alpha 3] In this condition there was only one capuchin and the experimenter first placed a grape in front of the empty place where the other monkey would have been, before starting the exchange task with the test subject and a piece of cucumber.[23]

The results showed a clear effect of others' rewards influencing capuchins' acceptance of rewards. Whereas in the equity condition cucumbers were happily accepted as reward for handing back the rock, in the inequity condition cucumbers were rejected one in three times. Rejection sometimes took the shape of throwing the piece of cucumber back at the experimenter, and sometimes as violently pulling the dividing screen. One in six times the capuchins did not even return the stone in the inequity condition. The failure rate to exchange was even higher in the effort control, where the other capuchin got a grape for not doing anything at all: three out of four times there was no successful exchange. In the food control, where grapes were visible but without any other monkey present, the monkeys were also more likely to refuse than in the equity condition.[23]

Each run of tests consisted of 25 trails in the same condition. The researchers compared the results of the first 15 against the last 10. They found that in the inequity condition and in the effort control, the failure rate in the last 10 was higher than in the first 15, suggesting that it may have taken a few trials before the monkeys noticed what reward the other had received. In the food control however, the failure rate in the last 10 was lower than in the first 15, suggesting that expectations are based on seeing a partner receive high-value rewards rather than the mere presence of such rewards.[26] The researchers concluded that female capuchin monkeys are inequity averse.[27]

Brosnan and de Waal published the results of their study in 2003 in the science journal Nature.[28] The study has since been cited over a thousand times.[29]

Subsequent studies

The original Brosnan and de Waal study has been replicated many times, with various variations of the experimental design and involving a diverse set of species as subjects.[30]

Subjects

Researchers have selected various species as subjects of their inequity aversion experiments.[30] Within the group of species closely related to humans, researchers have chosen both social primates (chimpanzees, bonobos, owl monkeys, marmosets,[31] baboons,[32] gorillas,[33] and tamarins),[34] and ones living solitary or just with their offspring (orangutans, gibbons,[35] and squirrel monkeys).[36] Researchers have also tested non-primates that display any capability of cooperation: corvids (crows, ravens, kea), canines (dogs, wolves),[37][38][39] cleaner fish[40] and rats.[41] Brosnan and de Waal have called for experiments with elephants, dolphins, and domestic cats to further the understanding of the evolution of fairness.[42]

Within their experiments researchers have controlled for various characteristics of subjects, just like Brosnan and de Waal did by using only female capuchins. A common factor is relationship: whether or not the two animals in the experiment have a genetic relationship or not. Dominance rank in social animals has also been known to play a role in cooperation experiments and is thus often controlled for.[6] The number of subjects is often limited, making robust statistical conclusions challenging.[43]

Conditions

To control for factors that may or may not influence inequity aversion researchers have used various conditions in their experiments. A food-contrast control is common. Is reward refusal due to the social aspect of the experiment or due to the animal expecting a higher-value reward? Contrast studies date back to the 1920s[25] and involve a series of higher-value rewards, followed by a low-value reward. Subjects can be tested alone[44] or side-by-side.[45] Some researchers have questioned Brosnan and De Waal's use of the last 10 trials in their food control to arrive at the inequity aversion conclusion. These researchers have designed various ways to control for food expectation, for example hiding it after having shown it, or putting it in another cage.[46]

Another common control is effort control. Does it matter if the food is handed out as a reward for effort or simply as a gift? Most commonly used for effort is Brosnan and De Waal's token-exchange task. Sometimes subjects must hold on to a token for a specified period of time (a task referred to as "target"). For no effort there are two cases: neither animal has to do anything, or the partner gets a free gift but the subject has to complete a task.[30]

Ultimatum Game

A few studies have deviated from the token-exchange paradigm and followed a paradigm used in inequity experiments with humans, the Ultimatum Game.[47][48] In this game, one individual, the proposer, has to choose between two tokens, one representing a fair division of rewards, the other an unfair division. The other individual, the responder, then needs to decide to either accept the chosen token, in which case rewards are given as per token value, or reject the token, in which case both proposer and responder do not get any reward.[6] [upper-alpha 4]

Choice

Some studies give the subject a choice between two options with different rewards, typically one in which both animals get rewarded and one in which only the chooser gets rewarded. This could be a direct choice between food plates on sliding platforms,[40] or indirect, typically a choice between two different tokens,[49] but also for example between two pathways that lead to different rewards.[41]

Cooperative pulling

Within the cooperative pulling paradigm (an experimental design in which two or more animals pull rewards towards themselves via an apparatus that they cannot successfully operate alone) researchers have varied the rewards for participants. They compare the likelihood of animals cooperating again after both received the same reward for jointly pulling to that of one receiving more than the other, or even one receiving all and the other none. This division can be done by the experimenter (one bowl each) or by the animals (one bowl).[37]

Findings

Overview

The results and conclusions are mixed. In terms of refusal rates being higher in inequity conditions than equity, there is substantial variation across species, within species, and even across individuals within the same studies. The conclusions researchers have drawn from these results are therefore also mixed.[50] In studies that did find a relatively higher refusal rate in the inequity condition than in the control conditions, there were always some individuals that did not refuse at all.[51] Researchers have found evidence of disadvantageous inequity in capuchin monkeys, chimpanzees, long-tail macaques, rhesus macaques, marmosets, baboons, gibbons, gorillas, dogs, wolves, rats, crows and ravens.[37][52][2][32] Bonobos may be inequity averse, as researchers have interpreted findings differently.[53][30]

Orangutans,[35] squirrel monkeys,[36] owl monkeys,[31] tamarins,[34] parrots,[39][54][55] and cleaner fish[40] were not found to be sensitive to inequity in any study.[37] Pet dogs behave differently from pack dogs and wolves. Pet dogs only object to the other receiving a reward while they themselves do not get anything, but when the difference is in quality, they do not seem to mind.[56]

The first follow-up studies that failed to replicate the original Brosnan and de Waal findings subsequently were shown to have a crucial difference in experimental setup. They involved animals getting food for no effort. Later studies have shown that the effect disappears in this context.[57] Talbot, Parrish, Watzek, Essler, Leverett, Paukner, and Brosnan argue that it is likely that the results are mixed because of small procedural differences.[58] They acknowledge that controlling for this is hard, especially across species as procedures often have to be tailored to the species in question, for instance in terms of their size and natural behaviour.[51] Other factors that may affect outcome but have not always been controlled for are gender and rank. Some researchers have suggested inequity may exist in one population but not another.[59] Many studies mention their small sample size puts limits on their conclusions.[60][59][61][62]

Studies that controlled for contrast effects ruled out that the higher refusal rates were due to mere visibility of better rewards. This is in line with the finding that animals reliably perform tasks for lesser rewards even when better ones are immediately in front of them.[44] Only Engelmann et al. did not explain reward refusal as inequity aversion. But they did not attribute the refusals to the contrast effect either. Instead, from their experiments with chimpanzees they concluded that refusal is due to disappointment in the behavior of the human experimenter.[63] Sheskin et al., however, found no evidence that capuchins differentiated between experimenters who either distribute equal rewards or unequal ones.[64] A few species (e.g., squirrel monkeys) respond more strongly to contrast effects than inequity; some respond to both (rhesus macaques), some seem indifferent to either condition (orangutans),[44] and some respond more strongly to inequity.[65]

In cooperative pulling tasks, individuals who are the victim of reward-monopolizing individuals punish this behavior by refusing to cooperate subsequently.[37] In a bar-pulling apparatus with unequal rewards capuchins still achieved success. Pairs that tended to alternate which monkey received the higher-value food were more than twice as successful in obtaining rewards than pairs in which one monkey dominated the higher-value food.[66] In an experiment with chimpanzees, on almost half the trials the pair negotiated to work for the equal division.[67]

Physical proximity is an essential ingredient for inequity aversion to appear in effortful tasks. Across species the effect virtually disappears if the animals are not side by side with full visibility of the action.[44] Dominance rank, sex, the quality of the relationship, and reward characteristics all also influence the presence or strength of the reaction.[6] For example, within an established group of chimpanzees inequity aversion was less pronounced than in a newly-formed group.[68] And the difference in value between the higher and lower reward matters for capuchins, as does the quality of the reward but not the quantity.[58] Having a barrier between the capuchins or not did not make any difference.[69]

Only three studies have found evidence for advantageous inequity aversion, two with chimpanzees and one with capuchins.[37] Although in previous studies with chimpanzees it had never been observed, in a 2010 study with 16 captive adult chimpanzees, males and females, it was found chimpanzees that received a higher-value grape refused to participate more often when the other chimpanzee received an inferior carrot than they did when the other chimpanzee also received a grape.[70] On the other hand, there have been a few reports of advantaged primates showing no empathy for their disadvantaged partner but instead eating their rejected lower-value food as well.[71]

In a modified version of the Ultimatum Game, researchers gave chimpanzees and very young humans a choice between a token representing five bananas for them and one for their partner, and a token representing an equal split of three bananas each. They had to pass this token to their partner who could either accept it and have it exchanged into the appropriate reward distribution, or reject it, resulting in nothing for both. Two of the four chimpanzees chose the equity token significantly more often than chance. When comparing their choices to those in a control condition, in which their partner had no option to reject the token, all four chimpanzees chose the equity token significantly more often.[72] Respondents never rejected an offer, but they did sometimes protest, for instance by spitting water at the selfish proposer.[42]

Some researchers have questioned the ecological validity of the results of inequity aversion experiments, including their own. For many species cooperation typically occurs outside of the food domain. But all experiments testing for inequity aversion are with food.[40]

Mixed results are not uncommon in research in moral behavior of animals. The results of prosocial experiments, which also aim to explore fairness in animals, are mixed as well.[73]

List of research by species
Method Evidence
Species Task Side-by-side Disadvantageous Advantageous Researchers
BaboonTargetYesMaybeMaybeFeller (2016)[32]
BonoboNoneNoNo–Bräuer et al. (2006)[74]
BonoboExchangeNoMaybe–Bräuer et al. (2009)[75][30]
BonoboUltimatum GameNoNoNoKaiser et al. (2012)[76]
CapuchinExchangeYesYes–Brosnan & de Waal (2003)[28]
CapuchinNoneYesNo–Roma et al. (2006)[77]
CapuchinChoiceYesNo–Dubreuil et al. (2006)[78]
CapuchinExchangeYesYes–van Wolkenten et al. (2007)[79]
CapuchinExchangeNoNo–Fontenot et al. (2007)[80]
CapuchinNoneYesNo–Dindo & de Waal (2007)[81]
CapuchinPullingYesYes–Fletcher (2008)[82]
CapuchinExchangeYesNo–Silberberg et al. (2009)[83]
CapuchinPullingNoYesYesTakimoto et al. (2010)[84]
CapuchinChoiceYesNo–Sheskin et al. (2014)[64]
CapuchinChoiceYesNoNoMcAuliffe et al. (2015)[85]
CapuchinExchangeYesYes–Talbot et al. (2018)[86]
ChimpanzeeExchangeYesYes–Brosnan et al. (2005)[68]
ChimpanzeeNoneNoNo–Bräuer et al. (2006)[74]
ChimpanzeeUltimatum GameNo–NoJensen et al. (2007)[87]
ChimpanzeeExchangeNoNo–Bräuer et al. (2009)[75]
ChimpanzeeExchangeYesYesYesBrosnan et al. (2010)[88]
ChimpanzeeUltimatum GameNoNoNoKaiser et al. (2012)[76]
ChimpanzeeUltimatum GameYes–YesProctor et al. (2013)[47]
ChimpanzeeExchangeYesYes–Hopper et al. (2014)[89]
ChimpanzeePullingNoNoNoUlber et al. (2017)[90]
ChimpanzeeChoiceYesYes–Engelmann et al. (2017)[63]
ChimpanzeeNoneYesYes–Kim et al. (2018)[91]
ChimpanzeeUltimatum GameNoNoNoBueno-Guerra et al. (2019)[92]
Cleaner fishChoiceYesNo–Raihani et al. (2012)[40]
CrowExchangeYesYes–Wascher & Bugnyar (2013)[52]
CrowExchangeYesNo–Jelbert et al. (2015)[2]
DogActionYesYes–Range et al. (2009)[93]
DogActionYesYes–Range et al. (2012)[94]
DogChoice[95]YesNoNoHorowitz (2012)[95]
DogActionYesYes–Brucks et al. (2016)[96]
DogActionYesNo–Brucks et al. (2017)[97]
DogActionYesYes–McGetrick et al. (2019)[98]
Dog (pack)ActionYesNo–Essler et al. (2017)[38]
GibbonTargetYesMaybeNoFeller (2016)[32]
GorillaNoneNoNo–Bräuer et al. (2006)[74]
GorillaExchangeYesMaybeNoFeller (2016)[32]
MacaquePullingYesYesNoMassen et al. (2012)[99]
MacaqueTargetYesYes–Hopper et al. (2013)[61]
MarmosetTargetYesNoNoFreeman et al. (2013)[31]
MarmosetPullingYesYes–Mustoe et al. (2016)[100]
MarmosetTargetYesYes–Yasue et al. (2018)[101]
OrangutanNoneNoNo–Bräuer et al. (2006)[74]
OrangutanExchangeNoNo–Bräuer et al. (2009)[75]
OrangutanExchangeYesNoNoBrosnan et al. (2011)[35]
OrangutanExchangeYesNoNoFeller (2016)[32]
OrangutanNoneYesNo–Kim et al. (2018)[91]
Owl monkeyTarget[31]YesNoNoFreeman et al. (2013)[31]
ParrotExchangeNoNo–Heaney et al. (2017)[39]
ParrotExchangeYesNo–Krasheninnikova et al. (2019)[55]
ParrotExchangeYesNo–Laumer et al. (2019)[54]
RatChoiceYesYes–Hernandez-Lallement et al. (2015)[41]
RatChoiceYesYes–Oberliessen et al. (2016)[102]
RavenExchangeYesYes–Wascher & Bugnyar (2013)[52]
Squirrel monkeyExchangeYesNoNoTalbot et al. (2011)[36]
Squirrel monkeyTargetYesNoNoFreeman et al. (2013)[31]
TamarinExchangeYesNoNoNeiworth et al. (2009)[34]
TamarinPullingYesNoNoMcAuliffe et al. (2014)[103]
WolfActionYesYesNoEssler et al. (2017)[38]

Baboons

Baboons live in complex societies of up to 150 individuals.[104] They are tolerant and cooperative.[105] Feller tested 12 olive baboons (Papio anubis) in pairs who had not been exposed to each other before. Both apes had to pick up and hold a target for 1 second to be rewarded.[106] Rewards were either identical, inferior or superior in either quality or quantity.[107] On average the baboons' refusal rate in the inequity conditions (both quality and quantity) differed significantly from the equity control conditions, but it did not differ significantly from the contrast control conditions, making it not possible to rule out a non-social reason for their behavior. However, there were striking individual differences. Five baboons had dramatically higher refusal rates in the quality inequity condition than in the quality contrast conditions.[108] For quantity inequity this number was four.[109] Demographic variables such as sex, rank, and rearing history could not explain why some individuals were inequity averse and others not.[110] As for advantageous inequity aversion, three baboons showed the effect for quality and one for quantity.[111]

Bonobos

Bonobos (Pan paniscus) are social animals that live in hierarchical structures, though not as hierarchical as chimpanzees.[112] Researchers Bräuer, Call, and Tomasello tested bonobos, together with other great apes, twice and twice failed to find evidence of inequity aversion.[74][75] In the first study the apes were simply given food.[33] Three years later they made a few procedural changes, critically now using the token-exchange paradigm.[53] They argued that because in their method apes in the equity condition were shown the higher-value reward prior to receiving the lower-value reward, only their method allowed for proper comparison between inequity and equity conditions.[113] Although all five bonobos refused lower-value food more often after having seen a partner getting a better reward, the researchers concluded that there was no sufficient evidence to say bonobos are inequity averse.[114] Brosnan and de Waal drew different conclusions from the Bräuer, Call, and Tomasello study and wrote that bonobos may be inequity averse.[30] Kaiser, Jensen, Call, and Tomasello designed a variant of the Ultimatum Game that involved inequity being created by the proposer stealing a portion of the responder's share. They did not find any bonobo refusing any food, and proposers consistently stole food from responders, seemingly oblivious to the effect theft would have on others. They concluded bonobos are insensitive to unfairness.[115]

Capuchins

After the original Brosnan and de Waal paper almost a dozen studies with capuchins have been published. The results of these studies are mixed, with some confirming the original finding that capuchins are inequity averse and some concluding they are not.[51] McAuliffe, Chang, Leimgruber, Spaulding, Blake, and Santos, for example, found no evidence of either disadvantageous or advantageous inequity aversion in a choice experiment often used with humans.[85] Talbot, Parrish, Watzek, Essler, Leverett, Paukner, and Brosnan argued that the results had been mixed because the experimental setups differ and even small details might influence the capuchins' behavior.[51] To test this they investigated two factors that differ across the capuchin studies. They gave 13 capuchins the token-exchange task and varied the quality of food. They introduced a medium-preferred food reward and found that the effect is far stronger when the difference in food preference is large (i.e. high and low) than medium (e.g., high and medium), and that it disappears if the low-value food is not much liked at all. This outcome may explain some of the mixed results of previous experiments.[116] They also tested the impact of having a physical barrier between the two monkeys or not, another factor that had varied in the experiments so far. They found it did not matter if there was one or not.[69] They suggested future studies should control for each detail of the experimental setup, as it helps to understand the effect better, rather than seeing mixed results as a negative.[58]

Chimpanzees

Chimpanzees (Pan troglodytes) are smart, social animals.[1] In the wild they cooperate to hunt, dominate rival groups, and defend their territory.[117] They share food, but possibly do this to avoid challenges.[118] Results of inequity aversion studies have yielded mixed results.[119] Bräuer, Call, and Tomasello, for instance, provided six chimpanzees with a token-exchange task, controlling for social and food comparison factors. They concluded that any difference in behavior in the inequity condition compared to the equity condition was due to the apes comparing the food on offer, not due to unfairness.[120] On the other hand, Brosnan, Talbot, Ahlgren, Lambeth, and Schapiro administered a similar test to 16 chimpanzees and found that males were inequity averse but females were not. The higher refusal rate in the inequity condition was due to social comparison.[121] The researchers also found the first evidence of advantageous inequity aversion in animals. Multiple times chimpanzees refused a grape after having observed their partner only receive a carrot.[122] Studies using the Ultimatum Game instead of token exchange also produced mixed results.[87][47] Five studies involved an experimental setup in which the chimpanzees were not side by side. None of them found any evidence of inequity aversion.[74][87][75][76][90] Brosnan, Talbot, Ahlgren, Lambeth, and Schapiro attributed overall variability in results to differences in procedures and small sample sizes making it hard to reliably control for factors such as rank and sex.[119]

Gibbons

Gibbons (Nomascus leucogenys) live in small groups, two parents with their offspring, and do not cooperate with non-kin.[123] Feller tested two white-cheeked gibbons in a target-holding experimental paradigm. She predicted that they would not respond negatively to receiving inferior rewards than their partner.[124] Indeed, there was no significant difference with the control conditions, although one of the two gibbons did refuse more than in the equity conditions, both in the case where rewards differed in quality and in the case where they differed in quantity.[125] Feller did not find any contrast effect for gibbons.[126]

Gorillas

In an experiment including three other great ape species as well, Bräuer, Call and Tomasello put six gorillas (Gorilla spp.) to the inequity test.[33] In the wild gorillas live in family groups of on average nine individuals.[127] Apes were given food without having to perform a task.[33] The researchers did not report results specifically for gorillas, but overall for all four species the apes did not refuse food more often when a partner got better food.[128] From their controlled experiments they concluded that any food refusal is not due to inequity aversion but, most likely, to not meeting their expectation. This food expectation hypothesis says that subjects have an expectation to receive the preferred food in some conditions but not others. Seeing the experimenter give favored food to a partner, not just being placed into an empty cage, may have created the expectation that they will get some of the favored food as well.[128] In speculating why their findings are different from Brosnan and de Waal's, Bräuer, Call and Tomasello point to procedural differences, especially giving food versus token exchange.[129] In a token-exchange test with two male gorillas, siblings, Feller did find some evidence of inequity aversion.[130] One of the apes refused food far more often when his partner had received a better value reward for exchanging a token than in the control condition.[130] But since both brothers also reacted to the contrast effect, Feller did neither rule out nor confirm that gorillas are inequity averse.[131]

Macaques

Macaques (Macaca spp.) are small monkeys that live in hierarchical groups. They do not habitually use tools, hunt cooperatively or share food.[132] Two out of two studies with macaques found evidence for inequity aversion.[99][61] Massen, Van Den Berg, Spruijt, and Sterck tested 12 long-tailed macaques in a tray-pulling experiment with strangers and "friends". The researchers hypothesized that friends pay less attention to equity than strangers and thus they predicted no or only a small effect in the friends condition. Contrary to their predictions, the macaques responded to inequity in largely the same way with a friend as with a stranger. The monkeys only refused food significantly more in the inequity condition when their effort was moderate. No effort or a lot of effort (the tray the subjects had to pull towards themselves was counterweighted extra) did not result in higher refusal rates.[133] The researchers ruled out that refusal rates were higher due to a contrast effect because each individual monkey only ever received one type of reward. No evidence for advantageous inequity aversion was found.[134]

Hopper, Lambeth, Schapiro, Bernacky, and Brosnan were the first researchers to study the development of inequity aversion in animals. They first tested 20 young rhesus macaques (on average 17 months old) and found no difference in refusal rate between inequity and equity conditions. A year later they tested eight of them again and now found them refusing rewards more often in the inequity condition. They ruled out refusals being due to the animals being frustrated seeing but not getting the higher-value food.[61]

Marmosets

Marmosets (Callithrix spp.) are small monkeys that form long-term parental pair bonds.[135] In two of three experiments with marmosets evidence was found of inequity aversion.[31][101][100] Freeman, Sullivan, Hopper, Talbot, Holmes, Schultz-Darken, Williams, and Brosnan found that none of the ten marmosets they tested differed significantly in their rate of refusals among the three task conditions.[136] In contrast, Yasue, Nakagami, Nakagaki, Ichinohe, and Kawai did find a difference in their test of six marmosets required to hold a spoon for two seconds to receive a reward. The monkeys almost always successfully performed the task when they had observed a partner receiving the same reward, but only in 70% of trials when they witnessed the partner receiving a more attractive reward.[137] This high refusal rate was not present in another condition where five other marmosets had been exposed to valproic acid, leading the researchers to conclude that inequity aversion stems from weak social motivation.[138]

Mustoe, Harnisch, Hochfelder, Cavanaugh, and French tested eight marmosets in a tray-pulling experiment, where subjects pulled a tray with food towards themselves and partners. They found evidence for inequity aversion in the four male marmosets. The males did not avert inequity when paired with strangers. The neurohypophysial hormone oxytocin, which has been found to modulate social behavior in primates, did not influence inequity aversion.[139]

Orangutans

Five inequity aversion studies involving orangutans (Pongo pygmaeus), a great ape with a semi-solitary lifestyle and not known to be great co-operators,[140] have been published. No study found evidence of inequity aversion. Brosnan, Flemming, Talbot, Mayo, and Stoinski used the same experimental set-up and method as the group had previously used with chimpanzees.[141][88] Five orangutans were put in eight different conditions, seven of which involved a token exchange. The highest refusal rate, 10%, was in the inequity condition but it did not differ significantly from the refusal rate in the equity conditions, neither the one in which both apes received a low value reward nor the one with a high-value reward. The orangutans also did not refuse often in individual contrast conditions.[142] As with many other species, in the no-effort condition the refusal rate was very low.[143] Feller tested two orangutans with various conditions including a quantity inequity condition.[144] Neither ape refused any food in any condition.[145]

Owl monkeys

Owl monkeys (Aotus) live in small groups of up to five individuals, usually a male and female and their offspring. Both parents look after the children.[146] Freeman, Sullivan, Hopper, Talbot, Holmes, Schultz-Darken, Williams, and Brosnan tested three different monkey species, including owl monkeys, in a variation of Brosnan and de Waal's original experiment. Instead of exchanging tokens with experimenters the monkeys had to reach out of their cage, pick a token and hold on to it. Apart from the non-social condition with high-value food visible but not given, there also was a no-effort control condition. The researchers found that owl monkeys did not differ in their rate of refusals among any of the four conditions.[136] They hypothesized that for species that provide bi-parental care the cost of having conflict with their reproductive partner may be too high to warrant a refusal reaction over a small amount of inequity.[147]

Squirrel monkeys

In the wild, squirrel monkeys (Saimiri sciureus) do not regularly cooperate.[147] Talbot, Freeman, Williams, and Brosnan tested squirrel monkeys in a token-for-food exchange experiment, with a free food and contrast conditions as controls. The monkeys did not refuse food more often in the inequity condition than in the equity condition. They refused food far less often in the free food condition than in the token-exchange conditions. The male squirrel monkeys refused food the most in the contrast condition, when given inferior food after initially having been shown better food. The females refused food less often in all conditions, the least in the free-food condition. The researchers concluded that squirrel monkeys are not averse to inequity.[148] Freeman, Sullivan, Hopper, Talbot, Holmes, Schultz-Darken, Williams, and Brosnan found no evidence of inequity aversion in their test with squirrel monkeys either. They too observed a strong contrast effect: when there was no partner but a better reward present than given the monkeys refused food the most by far.[136]

Tamarins

Cotton-top tamarins (Saguinus oedipus) are New World monkeys that breed cooperatively, cooperative on tasks and tolerate food sharing.[149] Neiworth, Johnson, Whillock, and Greenberg tested 11 tamarins in six conditions. In one of the conditions, the effort+food inequity condition, the subjects were given the less preferred food as reward for a token exchange, whereas the partners were just handed the more preferred food for no effort. The highest rejection rates were in the food-control condition, with low-value food given while preferred food was present. The researchers did find some evidence of inequity aversion, but only by comparing results from the first set of trials to the last in the food inequity condition of the token-exchange task, similar to Brosnan and de Waal's original analysis. In the non-social conditions this significant rise in rejections was not found. The researchers attributed the rise to an increasing aversion to the perceived inequity. Curiously, in the effort+food inequity condition the rejection rates did not increase significantly. The researchers theorised that the animals judged the situation differently as the partner did not have to act, not triggering the equity comparison scheme.[150]

McAuliffe, Shelton, and Stone tested the reaction of 12 cotton-top tamarins to inequity in a personalised handle-pulling task. The researchers suspected that the amount of effort involved is a key factor in inequity aversion and therefore designed a tray-pulling task with weights, after having calibrated how much weight each subject was willing to pull for food. In the inequity conditions the subjects had to exert a lot of effort for little food while their partners received more food for no effort. The researchers found weak support for the influence of effort on inequity aversion, largely driven by one female.[103]

Dogs

Dogs (Canis familiares) are known to cooperate in hunting, breeding and defending territories. McGetrick and Range reviewed seven studies into inequity aversion in dogs.[151] Range, Horn, Virányi, and Huber found a negative reaction to an all-or-nothing distribution of rewards, in an experimental setup similar to Brosnan and de Waal's original work, with the task of giving a paw. However, there was no effect when the distribution was uneven in quality. The researchers concluded that dogs possess a primitive form of disadvantageous inequity aversion.[152][93] Brucks, Essler, Marshall-Pescini, and Range replicated this study with 32 pet dogs and came to the same conclusion.[152][96]

Three other studies came to the opposite conclusion. McGetrick and Range challenged the validity of one of them, a study by Horowitz involving dogs choosing between a fair and an unfair human, on the grounds of it was not asking the same question of the dogs: for instance, the task was not prosocial.[95][153] Nonetheless, the Horowitz study did study both advantageous and disadvantageous inequity, unlike the original Range, Horn, Virányi, and Huber design, so it was more able to speak about inequity aversion in both contexts. The findings of two other studies are also seemingly at odds with the notion that dogs are inequity averse. Brucks, Marshall-Pescini, Essler, McGetrick, Huber, and Range tested the willingness of 44 dogs to press a buzzer with their paw to get a food reward inferior to their partner's. Their experimental setup did include one set of conditions without any human being present. While the dogs did show signs of stress, they did not refuse to perform the task relatively more. They stopped pressing the buzzer once they saw that their partner was being rewarded and they did not, but this behaviour was not significantly different from the condition without a partner.[154][155] Essler, Marshall-Pescini, and Range obtained similar results with ten pack-living dogs.[38][154] McGetrick and Range concluded that with the current evidence it is likely that dogs possess a primitive form of disadvantageous inequity aversion.[154] McGetrick, Ausserwöger, Leidinger, Attar, and Range1 tested the hypothesis that a shared food source is necessary to elicit inequity aversion in dogs, but found that not to be the case. Even when rewards came from different sources they observed some inequity aversion.[98]

Rats

Rats (Rattus norvegicus) often develop in social groups, cooperate naturally, have been found to reciprocate, and generally display behavior that benefits others.[41] Hernandez-Lallement, van Wingerden, Marx, Srejic, and Kalenscher tested 68 male rats in a series of maze experiments where the animals could choose between a path that lead to rewards just for them or for a partner as well.[41] Most rats chose the option that rewarded both significantly more, albeit with a small margin (55% versus 45%).[156] In a control condition the researchers replaced the partner rat with a toy lookalike. In this condition, the rats chose the option to just reward themselves more. The researchers concluded that rats derive value from another rat's access to food.[156] They attributed the relatively small size of the effect to individual differences. About 60% of rats showed this pro-social behavior.[157] In a similar experiment with 23 rats, Oberliessen, Hernandez-Lallement, Schable, van Wingerden, Seinstra, and Kalenscher found supporting evidence of inequity aversion.[102]

Wolves

Wolves (Canis lupus) are highly social animals that cooperate in hunting, breeding and defending their territories. Essler, Marshall-Pescini, and Range set up an experiment with nine wolves and ten pack-living dogs to investigate if domestication was the reason dogs show a primitive form of inequity aversion. The animals had to press a buzzer to receive a reward, which was either equal or inferior to the reward of a partner performing the same action in an adjacent enclosure. The wolves stopped pressing the buzzer once they observed their partner got a better reward for the same action. In the conditions without receiving a reward, wolves completed fewer tasks when there was a partner who did get rewarded than when there was no partner at all. Taking the social hierarchy into account, dominant wolves reacted strongly to a subordinate being rewarded when they were not. Given that the results for pack-living dogs were very similar, the researchers concluded that the common ancestor of wolves and dogs likely already was inequity averse, and that domestication is not a factor for this behavior in dogs.[38]

Crows

Carrion crows (Corvus corone corone) are smart, social birds from the corvids family. Wascher and Bugnyar tested six crows in a setup similar to the original Brosnan and de Waal study (they also tested ravens at the same time).[158] They made sure that the birds always saw the reward before the task, in order to control for a frustration effect.[159] The exchange rate was significantly higher in the equity condition than in the inequity condition, as the researchers had expected.[160] The biggest drop in task completion rate was when the partner received a reward for no effort but the crow had to work for it.[161] Wascher and Bugnyar concluded that crows reject unfair offers.[162] Because of their small sample size they were cautious to attribute this to disadvantageous inequity aversion, but strongly suspected so.[163] Brosnan and de Waal concluded from Wascher and Bugnyar's research that crows are inequity averse.[30]

Parrots

Parrots generally live in complex social structures and perform well on cognitive tasks. [55] Kea (Nestor notabilis) are parrots that live in groups. Although in lab settings they have displayed cooperative behaviour, in the wild they do not appear to cooperate.[164][165] Researchers Heaney, Gray, and Taylor presented four male kea with a series of token-exchange conditions, with the birds side by side, so they could see their partner's behaviour. They found that the success rate did not differ significantly between the four conditions involving rewards (inequity condition, equity condition, free gift condition, and food control condition, in which both kea were shown a high-value food but upon token exchange only received a low-value reward). A significant drop in success rate was observed in the condition where the subject received nothing while the partner did. The researchers concluded that this is not due to any social factor, as the drop in rate was similar to the one observed in the no partner + no reward condition. Based on these results the researchers concluded that kea are not sensitive to inequity.[39] Krasheninnikova, Brucks, Buffenoir, Blanco, Soulet, and von Bayern subjected 28 parrots, of four different species, great green macaws, blue-throated macaws, blue-headed macaws and African grey parrots, to token exchange experiments. All of these species form long-term monogamous relationships with a partner, while living in larger family groups. As the researchers expected, they found no evidence of inequity aversion. The great green macaws did stop exchange tokens, but this was deemed to be due to the mere presence of high-quality rewards rather than to the partner receiving it. All four parrots species seemed to be sensitive to differences in reward quality, strongly suggesting that they were paying attention to what their partners were getting.[55] Researchers Laumer, Massen, Wakonig, Lorck‐Tympner, Carminito, and Auersperg found tentative evidence for inequity aversion to unequal work‐effort but not to unequal reward distribution in cockatoos.[54]

Ravens

Ravens (Corvus corax) are large-brained corvids that in the wild form coalitions and cooperate.[158] Researchers Wascher and Bugnyar tested four ravens on their behavioral response to inequity in a token-exchange task (they also tested crows at the same time).[158] Two ravens never refused food in any condition. Overall, the ravens refused to accept the low-quality reward more often in the inequity condition than in the equity condition.[161] Most striking were the results in the condition were the partner simply was given food but the subject had to work for it. Here the ravens successfully completed the task the least.[159] The researchers made the caveat that their sample size was low and were thus reluctant to come to firm conclusions, but it seemed that ravens reject unfair offers even at a cost to themselves.[60] Brosnan and de Waal concluded from Wascher and Bugnyar's research that ravens are inequity averse.[30]

Cleaner fish

Bluestreak cleaner wrasses (labroides dimidiatus) are cleaner fish, found in coral reefs, that engage in mutualism with other aquatic animals, so-called clients, by feeding on their surface ectoparasites, mucus and dead skin. Clients prefer having their ectoparasites being removed; they do not like cleaners cheating by biting off surface mucus or dead skin. Sometimes a male and female cleaner wrasse jointly clean a client. Males punish females for cheating because it often results in the end of the feeding session. This suggests cleaner fish may be aware of the payoffs accrued by an interaction partner.[40] Researchers Raihani, McAuliffe, Brosnan, and Bshary tested two sets of cleaner fish (12 and 10 individuals) on their sensitivity to unequal outcomes. The fish had to perform a task to provide food rewards for themselves and a partner. They were equally likely to work when their partner received higher-value rewards or same-value rewards. There was no significant difference whether their partner was unfamiliar and of the opposite sex or familiar and of the same sex. The researchers provided two possible explanations for these results. It may be that the fish did not see or pay attention to the food distribution prior to performing their task. Alternatively, cleaner wrasses may not be inequity averse.[40]

Evolution

Almost all researchers explain the findings of animals refusing less-preferred food while others receive more-preferred food in terms of inequity aversion and a sense of fairness. The cost of foregoing a low-value food when the partner gets a high-value reward is low. It's worth to reject, protest and possibly get something better. The cost of foregoing a high-value food when the partner gets an even higher-value reward is high, not worth protesting about and risk being left empty-handed.[166] Comparing one's gains to those of others makes evolutionary sense. If individuals were satisfied with any absolute benefit, they might still face negative fitness consequences if they were doing less well than competing others.[71] But this applies only in the context of extensive cooperation outside of kinship relationships.[30]

One explanation of the findings so far is that inequity aversion evolves in order to foster long-term cooperation between unrelated individuals. In particular, Brosnan suggests that responding to inequity facilitates partner choice. This increases an individual's fitness by enabling them to reject partnerships which repeatedly lead to unequal outcomes. In support of this, inequity aversion is found in highly-cooperative capuchins, but not in the closely related, less cooperative squirrel monkey; and in cooperative chimpanzees, but not in typically less cooperative orangutans.[167] (McAuliffe and Santos however warn that there may be a sampling bias, since far more cooperative species have been tested than less-cooperative ones.[168]) A further refinement is that inequity aversion is only adaptive in species which cooperate with multiple partners and can switch cooperative partners without bigger costs, thus ruling out the long-term monogamous parrots.[55] But it fails to explain why no inequity aversion was found in the cooperative cleaner fish.[168]) This theory predicts that domestic cats are far less sensitive to inequity than dogs.[42]

Brosnan ruled out the possibility that cognitive differences are driving inequity aversion, as orangutans are equally skilful in cognitive and exchange tasks as other great apes but never display the effect.[169] Brosnan and de Waal summarized the findings as inequity aversion being most pronounced in animals that cooperate outside of the bonds of mating and kinship.[44] Chimpanzees, bonobos, capuchins, macaques, dogs and corvids are all highly cooperative in nature and show inequity aversion; orangutans, owl and squirrel monkeys are not cooperative outside kin and do not show inequity aversion.[170]

The main explanation for disadvantageous inequity aversion is anticipatory conflict resolution. The animal anticipates their partner reacting negatively to disadvantageous inequity and thus rejects the better reward, or in the case of the Ultimatum Game, favours the equity token over the favorable one. Researchers have speculated that the reason why it is limited to chimpanzees and capuchins is that it requires the cognitive capability of planning, anticipating their partner's disadvantageous inequity aversion. Few species have this capacity. Chimpanzees have shown their ability to plan ahead in other contexts, for instance in tool use. Advantageous inequity aversion may also directly benefit an individual by enhancing its reputation, which may increase that individual's long-term access to beneficial relationships.[42]

Including evidence from canines, Essler, Marshall-Pescini, and Range conclude that it is possible that sensitivity to inequity was already present in an earlier common ancestor with primates. Alternatively, convergent evolution may be at play: under similar conditions the same behavior has emerged multiple times in evolution.[171] For example, bluebirds, bats and butterflies all have wings but do not share an ancestor that could fly, and the way their wings are constructed are entirely different.[172] Basing their argument partly on the facts that female chimpanzees often range solitarily and avert inequity less than males, Brosnan, Flemming, Talbot, Mayo, and Stoinski state the most likely hypothesis is that natural selection favours those who care how their outcomes compare to others. The level and intensity of cooperation may be less relevant for female chimps than for males, which may reduce the need for the building of social expectations among females.[173] Kim, Choe, Jeong, and Kim state it is an open question whether orangutans have lost or chimpanzees have acquired a sense of fairness in the hominid lineage.[91]

McAuliffe and Santos conclude that there is weak evidence for the social hypothesis for how inequity aversion came about and indirect evidence for the non-social hypothesis. They suspect inequity aversion has non-social roots but has been coopted for social interaction.[174]

While the controlled experiments have advanced the understanding of inequity aversion, their context cannot include all possible outcomes that exist in natural social interactions. In the standard inequity task, refusals only hurt the actor, whereas in a natural social context, protest against inequity may lead to the actor either receiving a larger share or seeking out a better partner to work with.[6]

Debove, Baumard, and André ran computer simulations of individuals of different rank cooperating with equal and unequal reward distributions and concluded that when partner choice is a characteristic of the setup, fairness emerges.[175]

Footnotes
  1. Advantageous inequity aversion was found in the US, Canada, and Uganda, but not in Senegal, Peru, Mexico, and India.[7]
  2. Brosnan's proposed experiment to better understand this socio-economic behavior nearly was rejected by her PhD committee, because she had already planned six other experiments. But because the committee could not agree on the expected outcome of her proposed experiment, her advisor, professor Frans de Waal, told her she obviously had to do it.[22]
  3. Research into the contrast effect in animals dates back to 1928 when Tinklepaugh tested the effect of expectation in macaques. He let the monkeys see he put treats under a bucket. The next day he would lift the bucket and hand out the treats. But when he secretly switched the treats for a lettuce leaf, the monkeys reacted poorly in the morning, refusing those rewards.[24][25]
  4. The Impunity Game is a variant of the Ultimatum Game: if the responder rejects the proposal, the proposer gets to keep the reward and the responder gets nothing.[6] This game has not been tested with animals. The challenge is to ensure the animals understand that the proposer had a choice.[45]

References
  1. Rekers, Haun & Tomasello 2011, p. 1756.
  2. Jelbert et al. 2015, p. 1.
  3. Fehr & Schmidt 1999.
  4. Tomasello & Vaish 2013, p. 244.
  5. McAuliffe et al. 2017.
  6. Brosnan & de Waal 2014, p. 1251776-2.
  7. Blake et al. 2015, p. 259.
  8. Blake et al. 2015, p. 258.
  9. Heinrich et al. 2001.
  10. McAuliffe & Santos 2018, p. 394.
  11. Blake et al. 2015, p. 260.
  12. Dugatkin 1997.
  13. Péron et al. 2011, p. 545.
  14. Hector 1986, p. 247.
  15. Boesch & Boesch 1989.
  16. Pitman & Durban 2012, p. 16.
  17. Brian 2012, p. 18.
  18. Lee 1987, p. 278.
  19. Massen, Ritter & Bugnyar 2015, p. 1.
  20. Brosnan & de Waal 2003, p. 297.
  21. Watts & Mitani 2002, p. 13.
  22. Brosnan, Sarah (2014). That's Not Fair! What Cucumber-Throwing Capuchins Tell Us About the Evolution of Fairness. The Social Mind: A Festschrift Symposium Honoring the Career of Frans de Waal, September 19, 2014.
  23. Brosnan & de Waal 2003, p. 297-298.
  24. Brosnan et al. 2011, p. 57.
  25. Tinklepaugh 1928.
  26. Brosnan & de Waal 2003, p. 298-299.
  27. Brosnan & de Waal 2003, p. 299.
  28. Brosnan & de Waal 2003.
  29. "Google Scholar results". Retrieved 24 May 2018.
  30. Brosnan & de Waal 2014, p. 1251776-3.
  31. Freeman et al. 2013.
  32. Feller 2016.
  33. Bräuer, Call & Tomasello 2006, p. 3124.
  34. Neiworth et al. 2009.
  35. Brosnan et al. 2011.
  36. Talbot et al. 2011.
  37. Brosnan & de Waal 2014, p. 1251776-4.
  38. Essler, Marshall-Pescini & Range 2017.
  39. Heaney, Gray & Taylor 2017.
  40. Raihani et al. 2012.
  41. Hernandez-Lallement et al. 2015, p. 1.
  42. Brosnan & de Waal 2014, p. 1251776-5.
  43. Talbot et al. 2018, p. 79.
  44. Brosnan & de Waal 2014, p. 1251776-1.
  45. Brosnan 2013, p. 10418.
  46. Neiworth et al. 2009, p. 10-11.
  47. Proctor et al. 2013.
  48. Yamagishi et al. 2009.
  49. Amici, Visalberghi & Call 2014, p. 1.
  50. Talbot, Price & Brosnan 2016.
  51. Talbot et al. 2018, p. 76.
  52. Wascher & Bugnyar 2013.
  53. Bräuer, Call & Tomasello 2009, p. 176.
  54. Laumer et al. 2019.
  55. Krasheninnikova et al. 2019.
  56. Essler, Marshall-Pescini & Range 2017, p. 1861.
  57. Massen et al. 2012, p. 146.
  58. Talbot et al. 2018, p. 85.
  59. Bräuer, Call & Tomasello 2009, p. 180.
  60. Wascher & Bugnyar 2013, p. 7-8.
  61. Hopper et al. 2013.
  62. Feller 2016, p. 77.
  63. Engelmann et al. 2017, p. 1.
  64. Sheskin et al. 2014.
  65. Talbot et al. 2018, p. 80.
  66. Brosnan, Freeman & de Waal 2006, p. 713.
  67. Melis, Hare & Tomasello 2009.
  68. Brosnan, Schiff & de Waal 2005.
  69. Talbot et al. 2018, p. 84.
  70. Brosnan et al. 2010, p. 1235.
  71. Brosnan 2006.
  72. Proctor et al. 2013, p. 2071.
  73. Debove 2015, p. 133.
  74. Bräuer, Call & Tomasello 2006.
  75. Bräuer, Call & Tomasello 2009.
  76. Kaiser et al. 2012.
  77. Roma et al. 2006.
  78. Dubreuil, Gentile & Visalberghi 2006.
  79. van Wolkenten, Brosnan & de Waal 2007.
  80. Fontenot et al. 2007.
  81. Dindo & de Waal 2007.
  82. Fletcher 2008.
  83. Silberberg et al. 2009.
  84. Takimoto, Kuroshima & Fujita 2010.
  85. McAuliffe et al. 2015.
  86. Talbot et al. 2018.
  87. Jensen, Call & Tomasello 2007.
  88. Brosnan et al. 2010.
  89. Hopper et al. 2014.
  90. Ulber, Hamann & Tomasello 2017.
  91. Kim et al. 2018.
  92. Bueno-Guerra et al. 2019.
  93. Range et al. 2009.
  94. Range, Leitner & Virányi 2012.
  95. Horowitz 2012.
  96. Brucks et al. 2016.
  97. Brucks et al. 2017.
  98. McGetrick et al. 2019.
  99. Massen et al. 2012.
  100. Mustoe et al. 2016.
  101. Yasue et al. 2018.
  102. Oberliessen et al. 2016.
  103. McAuliffe, Shelton & Stone 2014.
  104. Feller 2016, p. 78.
  105. Dumas et al. 2017, p. 20170248-5.
  106. Feller 2016, p. 36.
  107. Feller 2016, p. 41.
  108. Feller 2016, p. 86.
  109. Feller 2016, p. 87.
  110. Feller 2016, p. 66.
  111. Feller 2016, p. 71.
  112. Hare et al. 2007, p. 619.
  113. Bräuer, Call & Tomasello 2009, p. 179.
  114. Bräuer, Call & Tomasello 2009, p. 178-179.
  115. Kaiser et al. 2012, p. 943.
  116. Talbot et al. 2018, p. 82.
  117. Melis, Hare & Tomasello 2006, p. 275.
  118. Ulber, Hamann & Tomasello 2017, p. 49.
  119. Brosnan et al. 2010, p. 14.
  120. Bräuer, Call & Tomasello 2009, p. 175.
  121. Brosnan et al. 2010, p. 9.
  122. Brosnan et al. 2010, p. 13-14.
  123. Feller 2016, p. 15,63.
  124. Feller 2016, p. 22.
  125. Feller 2016, p. 48-49.
  126. Feller 2016, p. 54.
  127. Feller 2016, p. 21.
  128. Bräuer, Call & Tomasello 2006, p. 3126.
  129. Bräuer, Call & Tomasello 2006, p. 3127.
  130. Feller 2016, p. 73.
  131. Feller 2016, p. 46,49.
  132. Massen et al. 2012, p. 154-155.
  133. Massen et al. 2012, p. 145;149.
  134. Massen et al. 2012, p. 151.
  135. Mustoe et al. 2016, p. 70.
  136. Freeman et al. 2013, p. 4.
  137. Yasue et al. 2018, p. 38.
  138. Yasue et al. 2018, p. 36.
  139. Mustoe et al. 2016, p. 69.
  140. Brosnan et al. 2011, p. 58.
  141. Brosnan et al. 2011, p. 60.
  142. Brosnan et al. 2011, p. 64-65.
  143. Brosnan et al. 2011, p. 65.
  144. Feller 2016, p. 1.
  145. Feller 2016, p. 82.
  146. Freeman et al. 2013, p. 2.
  147. Freeman et al. 2013, p. 6.
  148. Talbot et al. 2011, p. 681.
  149. Neiworth et al. 2009, p. 11.
  150. Neiworth et al. 2009, p. 15-16.
  151. McGetrick & Range 2018, p. 1.
  152. McGetrick & Range 2018, p. 4.
  153. McGetrick & Range 2018, p. 5.
  154. McGetrick & Range 2018, p. 6.
  155. Brucks et al. 2017, p. 6.
  156. Hernandez-Lallement et al. 2015, p. 5.
  157. Hernandez-Lallement et al. 2015, p. 6.
  158. Wascher & Bugnyar 2013, p. 1.
  159. Wascher & Bugnyar 2013, p. 6.
  160. Wascher & Bugnyar 2013, p. 4.
  161. Wascher & Bugnyar 2013, p. 5.
  162. Wascher & Bugnyar 2013, p. 7.
  163. Wascher & Bugnyar 2013, p. 8.
  164. Heaney, Gray & Taylor 2017, p. 1.
  165. Heaney, Gray & Taylor 2017b, p. 1.
  166. Talbot et al. 2018, p. 83.
  167. Jelbert et al. 2015, p. 2.
  168. McAuliffe & Santos 2018, p. 396.
  169. Brosnan et al. 2011, p. 66.
  170. Brosnan & de Waal 2014, p. 1251776-4,5.
  171. Essler, Marshall-Pescini & Range 2017, p. 1864.
  172. Brosnan 2019.
  173. Brosnan et al. 2011, p. 67.
  174. McAuliffe & Santos 2018, p. 397.
  175. Debove, Baumard & André 2015.

Bibliography
This article is issued from Wikipedia. The text is licensed under Creative Commons - Attribution - Sharealike. Additional terms may apply for the media files.