Low-status monkeys "play dumb" when learning in mixed social groups

Abstract

Many primates, including humans, live in complex hierarchical societies where social context and status affect daily life. Nevertheless, primate learning studies typically test single animals in limited laboratory settings where the important effects of social interactions and relationships cannot be studied. To investigate the impact of sociality on associative learning, we compared the individual performances of group-tested rhesus monkeys (Macaca mulatta) across various social contexts. We used a traditional discrimination paradigm that measures an animal's ability to form associations between cues and the obtaining of food in choice situations; but we adapted the task for group testing. After training a 55-member colony to separate on command into two subgroups, composed of either high- or low-status families, we exposed animals to two color discrimination problems, one with all monkeys present (combined condition), the other in their "dominant" and "subordinate" cohorts (split condition). Next, we manipulated learning history by testing animals on the same problems, but with the social contexts reversed. Monkeys from dominant families excelled in all conditions, but subordinates performed well in the split condition only, regardless of learning history. Subordinate animals had learned the associations, but expressed their knowledge only when segregated from higher-ranking animals. Because aggressive behavior was rare, performance deficits probably reflected voluntary inhibition. This experimental evidence of rank-related, social modulation of performance calls for greater consideration of social factors when assessing learning and may also have relevance for the evaluation of human scholastic achievement.

Figure 1

Housing and color discrimination problem for a captive monkey colony. Two indoor quarters (A), each with access to the outdoor enclosure (1450 m²) and apparatus (top right corner) (B). Two sets of boxes, containing peanuts hidden in a sand-rock matrix, were attached to the outside of the fenced enclosure, 1 m off the ground, in two experimental zones (semicircles separated by metal barrier). (Inset) Monkey’s view of the apparatus under discrimination conditions in which sets were colored differently to signal food availability (baited ▩ vs. nonbaited □). Animals had to select between sets (visual discrimination), enter the appropriate zone, i.e., baited zone (BZ) or nonbaited zone (NZ), and search box contents (manual discrimination). Behavior was recorded and filmed from an observation tower (OT) that provided an unobstructed view of both zones. B is reproduced with permission from ref. (copyright 1995, The Psychonomic Society).

Figure 2

Experimental design. (A) Combined acquisition (the context in which each monkey was among all colony members) presented one discrimination problem, involving a choice between baited blue (■) vs. nonbaited red (▨) boxes. (B) Split acquisition (the context in which each monkey was among only the members of the same social class) presented the other discrimination problem, involving a choice between baited yellow (□) vs. nonbaited green () boxes. In split testing (C) and combined testing (D), the discrimination problems remained the same, but the social contexts were reversed. Arrows 1–4 show the specific comparisons made to test the predictions regarding performance by subordinates.

Figure 3

Mean ± SEM time spent in zones by subgroups across acquisition trials 23–28 and test trials 1–6: (A) combined acquisition; (B) split acquisition; (C) split testing; (D) combined testing. Both subgroups preferred the baited zone in split contexts, but only the dominant subgroup showed this preference in combined contexts (*, P < 0.05; **, P < 0.01; ***, P < 0.001).

Figure 4

Total frequency of peanut retrievals by dominant (circles) and subordinate (triangles) subgroups per acquisition trials 23–28 and test trials 1–6: (A) combined acquisition; (B) split acquisition; (C) split testing; (D) combined testing. Dominant animals were more successful than subordinates in every combined trial (*, P < 0.05).

Figure 5

Mean ± SEM frequency of peanut retrievals by individual matrilines during split acquisition: (A) dominant subgroup; (B) subordinate subgroup. The alpha matriline was more successful than the beta and gamma matrilines (*, P < 0.05; **, P < 0.01). The same rank-related trend was evident for the subordinate subgroup, but was not statistically reliable.

Figure 6

Mean ± SEM frequency of threats received per trial for each subgroup: (A) combined conditions; (B) split conditions. Values are corrected for the number of potential partners in each social context (n − 1).