Supplemental Data: Capuchin Monkeys Are Sensitive to Others Welfare. Venkat R. Lakshminarayanan and Laurie R. Santos
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1 Supplemental Data: Capuchin Monkeys Are Sensitive to Others Welfare Venkat R. Lakshminarayanan and Laurie R. Santos
2 Supplemental Experimental Procedures Subjects Seven adult capuchin monkeys were tested. All of the monkeys in the study were housed in a single social enclosure in the Yale University Comparative Cognition Laboratory. Six of the monkeys tested (HG, MD, JM, FL, NN, JB) played against one monkey as receiver (AG). To minimize the likelihood that the social rank of the receiver induced proposers to provide rewards, we chose a low-ranking, reproductively inactive adult male (AG) to serve in the role of the receiver. To exclude the possibility that any observed effects were due to reciprocity, we only tested dyads in one direction no proposer that we tested had previously played the game as a receiver similarly to other one-shot experiments with New World monkeys. In order to test the greatest number of subjects in the role of the proposer, the monkey in the role of the receiver (AG) throughout the experiment first played as a proposer against a different monkey (HR) in the role of the receiver. HR was not involved in any further experimental trials, and no other monkeys besides AG and HR ever played the receiver s role. Because of the dynamics of our social group, this resulted in two pairs in which the proposer and receiver were related (HG was AG s younger sister, and HR was AG s niece), and five pairs (MD, JM, FL, NN, JB vs. AG) in which monkeys were not related. For testing, monkeys voluntarily entered a set of testing chambers positioned so that they were adjacent to the home cage, but could be closed off with a sliding door to allow testing without interference from the colony.
3 Apparatus Subjects were tested in two side-by-side testing cage mesh chambers (1 m x 1.6 m x 2.4 m), one housing the proposer and one housing the receiver. Subjects could easily see and hear each other through the mesh wall dividing the two chambers. Subjects were trained to make choices using an apparatus that would deliver food to the side-by-side chambers. As illustrated in Figure 1, the apparatus consisted of two wooden shelves (each 45.5 cm x 23.5 cm). The shelves were separated vertically by a distance of 25 cm, and were attached to the outside of the testing enclosures. Each shelf supported a wooden plank that could be baited with food. The part of each plank on the proposer s side of the apparatus was baited with food that could only be accessed from the proposer s chamber, whereas the part of each plank on the receiver s side of the apparatus was baited with food that could only be accessed from the receiver s chamber. During testing, the two planks provided the same reward to the proposer, but differed in the rewards provided to the receiver. The planks were initially positioned so that the food rewards were out of both monkeys reach, but the proposer could choose to move one of the two planks into both monkeys reach by pulling a rope handle. Only the monkey in the proposer s enclosure had access to these ropes. In addition, the testing chambers could be modified so that the partition between the two test chambers was open, in which case the proposer would have access to the rewards pulled towards the receiver s testing chamber. Finally, we used a clear Plexiglas blocker to prevent subjects from accessing the planks while the experimenter was baiting the planks with the food payoffs. As rewards, we used marshmallows and celery pieces; previous choice testing (Santos, unpublished data) has demonstrated that capuchins consistently prefer marshmallows to celery pieces.
4 Training All subjects completed two stages of training in order to ensure that they could discriminate between a large reward (marshmallow) and a small reward (celery) before beginning any experimental trials. In the first stage of training, subjects were required to distinguish between the large and small reward on the side of the apparatus that could be obtained by the proposer. The first sessions of training consisted of 10 trials in which the large reward, the marshmallow, was placed on either the top or bottom plank in the location that could be reached by the proposer. Specifically, subjects had to choose between one plank with a marshmallow payoff on the proposer s side and a lower reward (either celery or nothing) on the receiver s side and another plank with a lower reward (either celery or nothing) on the proposer s side and a marshmallow on the receiver s side. Each subject completed this phase of training with no receiver present and with the solid partition separating the proposer s and receiver s chambers in place, such that the proposer could not access rewards on the receiver s side of the plank. Subjects were tested on these training sessions until they were able to select the plank with the marshmallow on the proposer side 80% of the time across two consecutive sessions (for a total of at least 16 of 20 trials). Subjects received two consecutive sessions on each training day, and while some subjects reached the criterion in a single day (FL), the remaining subjects required greater exposure before reaching criterion, (n = 4 for AG, n = 7 for HG, n = 6 for JB, n = 3 for JM, n = 4 for MD, n = 3 for NN). After completing this first stage of training, subjects advanced to a second stage of training. The goal of this second training stage was to have subjects distinguish between a large and small reward on either the proposer s or receiver s side. In these
5 training sessions, no receiver was present and the partition between the two testing chambers was left open so that the subject could access rewards pulled to the receiver s side. In each session, one side of the apparatus always had the same payoffs (either both marshmallows or both celery) while the other had a choice between a large marshmallow reward and a lower reward (either celery or nothing). In this way, we required subjects to attend both to the proposer s side payoff and the receiver s side payoff in order to obtain the better reward. Subjects were presented with these training sessions until they were able to select the marshmallow over lower reward 80% of the time across two consecutive sessions (for a total of at least 16 of 20 trials). Again, subjects received two consecutive sessions on each training day, and varied in the speed with which they achieved criterion (n = 6 for AG, n = 2 for FL, n = 4 for HG, n = 11 for JB, n = 2 for JM, n = 5 for MD, n = 7 for NN). Testing After completing both of these training phases, subjects began their experimental sessions. Subjects completed two sets of three different types of sessions: two control sessions in which no monkey was present to play the role of the receiver, and a test session in which a receiver monkey was present. In the first control, the empty control, the partition between the testing chambers was closed and no receiver monkey was present. With this setup, any rewards provided to the receiver s chamber were inaccessible to the subject. The second control, the selfish control, was identical to the empty control except that the partition between the testing chambers was open, and thus the proposer could reach through and claim any rewards that were delivered to the receiver s chamber. Finally, in the test session, the partition between the chambers was
6 closed, and a receiver monkey was present (as illustrated in Figure 1). In this condition, the proposer and receiver could only access the rewards delivered to their own separate sides of the enclosure. To minimize effects of order, each subject received a randomly determined sequence of the three types of sessions (empty control, selfish control, and test condition). Subjects received two 20-trial sessions (40 trials) of each type of session. Before each session, monkeys received four familiarization trials so that they could learn whether the opening between the two chambers was open and thus understand which rewards were accessible to them. During these familiarization trials, only a single marshmallow was present in one of the four possible locations (top plank, proposer side, top plank receiver side, bottom plank proposer side, bottom plank receiver side). The goal of these familiarization trials was to allow the subject to easily realize whether the partition between the two chambers was open or closed, and (in the case of the test condition) that the receiver was present to eat the food if delivered. Once subjects pulled on all of these familiarization trials, the actual testing began. Each session then consisted of twenty trials with two possible pay-off structures to the proposer s side: celery payoff trials (10 per session) and marshmallow payoff trials (10 per session). In celery payoff trials, the subject could choose to deliver either marshmallow or celery to the receiver side, but always received a piece of celery on the proposer side. In the marshmallow payoff trials, monkeys could choose to deliver either marshmallow or celery to the receiver side, but always received a marshmallow on the proposer side. In both conditions, the location of the marshmallow and celery on the receiver s side was counterbalanced so that the top plank was baited with marshmallow
7 for half the trials, and the bottom plank was baited with marshmallow for the remaining half. Supplemental Results We explored whether subjects delivered the marshmallow more than would be expected by chance in each of these three conditions. These three one sample t-tests were evaluated against a Bonferroni-corrected alpha level of p = Additionally, all reported proportions were transformed for normalization using an arcsine transformation. Subjects delivered the marshmallow more than chance on the selfish control condition (t(6) = 5.55, p < 0.001) and the test condition (t(6) =3.47, p < 0.01), but not on the empty control condition (t(6) = 1.73, p = 0.13). In support of this pattern of data (Figure S1), we performed a repeated-measures ANOVA with session type (selfish control, empty control, and test condition) and proposer payoff (marshmallow and celery) as factors. The dependent variable was the proportion of trials in which the proposer delivered a marshmallow instead of celery to the receiver s chamber. We observed a main effect of proposer payoff (F(1,6) = 6.54, p < 0.04). Collapsing across condition, proposers were more likely to deliver marshmallow to the receiver s test chamber on a celery condition than on a marshmallow condition. This effect is likely due to the fact that subjects paid more attention to the location of the marshmallow when they received only celery than when they received marshmallow. We also observed a significant omnibus effect of condition (F(2,12)= 5.76, p < 0.02). Subjects were more likely to deliver the marshmallow during the selfish control condition than during the test condition, but were also more likely to deliver the marshmallow during the test condition than they were during the empty control condition (see Figure
8 2). To examine this effect further, we performed planned one-tailed t-tests comparing the differences in the rates that proposers delivered marshmallow in each of the three conditions. Subjects were significantly more likely to deliver the marshmallow to the recipient s testing chamber on the selfish control than on the empty control (Mean Difference: 20.6% marshmallow pulls, t(6) = 4.99, p = 0.001). Additionally, subjects were more willing to deliver the marshmallow during the test condition than the empty control condition (Mean Difference: 8.1%, t(6) = 1.91, p = 0.05), and slightly but not significantly more willing to deliver the marshmallow in the selfish control condition than in the test condition (Mean Difference: 12.6%, t(6) = 1.77, p = 0.06). In support of the claim that proposer monkeys significantly donated the higher reward to their partner even when they themselves received a lower reward, we also observed no interaction between condition and proposer payoff (F(2,12) = 1.56, p = 0.25). Monkeys performance in this task is consistent with the view that capuchins exhibit prosocial tendencies even in cases in which the receiver s payoff is larger than the one the proposer is allowed to keep for himself. One alternative to this interpretation, however, is that monkeys prosocial tendencies may have emerged merely as a result of the training procedure we used in this experiment. As described above, monkeys were trained in the second training condition to consistently attend to the location with the marshmallow, a training procedure that may have inadvertently lead to an increased number of times that the proposer chose the marshmallow option in the test conditions as well. However, this alternative cannot explain the full pattern of performance we observe across test conditions. More specifically, we only observe a tendency to choose the marshmallow reward in the test condition and selfish control; monkeys chose at random
9 between the marshmallow and celery options in the empty control condition. For this reason, the training procedure alone cannot account for the pattern of results we obtain across the different conditions. Another possible alternative for the pattern of results we observe is that some monkeys may have acted prosocially because they were genetically related to receivers. Indeed, some of the monkeys (n = 2) we tested as proposers were related to their receiver. To examine whether subjects were more generous to related individuals, we investigated whether monkeys who were relatives of the receiver (HR, his niece, and HG, his sister) exhibited a different pattern of giving than unrelated individuals. We found that family members were no more likely to deliver the marshmallow to the recipient than unrelated subjects in the test condition (related subjects: Mean = 67.5% marshmallow pulls, unrelated subjects: 69.6% pulls). A third alternative explanation for the pattern of results we observe is that subjects willingness to provide partners with generous rewards in the test condition may have been due to the fact that proposers were simply more aroused, and reacted more quickly, when another monkey was present. If subjects were more aroused when another monkey was present, then they may have attended more to the pulling task and thus to the location of the better reward. Under this alternative, then, monkeys may have been more likely to select a marshmallow in the test condition simply because another monkey s presence made them more attentive. To further investigate this possibility, we measured how quickly monkeys reacted to different rewards and session types by coding how long it took the monkeys to complete the action of pulling the apparatus on each trial. Specifically, we recorded the time difference between the beginning of each trial (i.e.,
10 when the proposer s rope first became available after the Plexiglas blocker was lifted) and the end of the trial (i.e., when the proposer has finished pulling the rope). A repeated measures ANOVA with session type (selfish control, empty control, vs. test condition) and proposer payoff (marshmallow vs. celery) as factors revealed no overall omnibus effect of session type on time to pull (F(2,12) = 0.56, p = 0.59). Collapsing across proposer payoff, monkeys pulled just as quickly on the test and two control conditions, suggesting that they did not react faster when another monkey was present. We did, however, observe a significant effect of proposer payoff (F(1,6) = 9.65, p = 0.02). Irrespective of session type, monkeys pulled more quickly when a marshmallow was delivered to the proposer s side than when a celery piece was delivered to the proposer s side. Finally, we observed an interaction between session type and proposer payoff (F(2,12) = 10.32, p = 0.003). Planned t-tests (with Bonferroni-corrected alpha level of p = 0.02) revealed that proposer monkeys pulled more quickly when a marshmallow was on the proposer s side in the empty control condition (t(6) = 3.28, p < 0.02), but not in the selfish control condition (t(6) = 1.02, p = 0.35) or the test condition (t(6) = 2.34, p = 0.06). This analysis revealed two important features about the proposer monkeys reaction times in our task. First, the monkeys do react more quickly on trials in which they receive a marshmallow versus a celery piece on the proposer s side. The fact that subjects reacted more quickly when offered marshmallow rather then celery as their proposer-side reward makes sense because monkeys are known to prefer marshmallow over celery (Santos, unpublished data). Second, and more importantly, monkeys reacted equally quickly on the test and control conditions, suggesting that they were not more
11 aroused when another monkey was present. The pattern of reaction times we observe thus cannot explain the effects of prosociality demonstrated in this task. Put differently, although obtaining a marshmallow on the proposer s side did seem to cause the monkeys to act more quickly, this increased arousal was, crucially, not related to the specific situations in which proposer monkey s were more likely to deliver the prosocial reward to the receiver s side. The differences in reaction time did not map onto whether another test monkey was present or absent, and so these differences in reaction time do not relate to the proposer s decision to deliver the marshmallow to the receiver s side. As such, arousal or attention patterns from the presence of another monkey cannot account for the pattern of prosociality observed in this study. A final alternative explanation is that monkeys provided better rewards in the test condition because the receiver monkey signaled which reward he wanted by selectively positioning himself. To address this alternative, we coded videos of all reported test trials to determine whether the receiver monkey s position relative to the available rewards had any impact on the proposer s choice. During the test trials, the receiver was free to move around his enclosure, and typically chose to position himself on a shelf equidistant from both planks. In support of this observation, and ruling out the possibility that the proximity to either the top or bottom plank could account for the proposer s choice, we found that the recipient monkey positioned himself near the chosen plank on fewer than 10% of trials (only 27 out of 280 trials).
12
13 Supplemental Figure Legends Figure S1. Proportion of large reward (marshmallow) deliveries across experimental condition, proposer s reward, and subject. The proportion of trials in which proposers chose to provide a receiver with marshmallow rather than celery is plotted on the y-axis, and subject, condition type (test, selfish control, empty control), and proposer payoff (celery or marshmallow) is plotted on the x-axis. Asterisks indicate that subjects were genetic relatives of the receivers with whom they were tested.
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