Early social experience affects behavioral and physiological responsiveness to stressful conditions in infant rhesus macaques (Macaca mulatta)

Abstract

Studies on early development have demonstrated the profound effects of early social experience on the behavioral development and physiology of young rhesus macaques. Given these relationships, we hypothesized that rhesus macaques exposed to different nursery-rearing conditions may develop unique biobehavioral profiles. If this is true, the assessment of temperament may allow us to pinpoint successful rearing environments, thus improving the overall health of nonhuman primates that are raised in captive environments. We conducted biobehavioral assessments in order to examine differences in the development of infants raised under four different peer-rearing conditions (continuous pairing (CP), intermittent pairing, CP with partner rotation, and intermittent rotational pairing) and compared these animals with data from a mother-reared control group. Overall, continuous rotationally paired animals were most similar to mother-reared controls on most behavioral and temperament measures, suggesting that more socially complex rearing environments (greater number of social partners) favor a more active behavioral style. Cortisol profiles of mother-reared controls were similar to both CP groups, and these three groups had higher cortisol concentrations than the intermittent rotational-pairing group. In addition, intermittently paired infants displayed a significantly higher frequency of self-stroke behavior during a human intruder challenge, an abnormal behavior also known as floating limb which has been shown to be a precursor of self-biting. Overall, the data are consistent with the idea that social complexity in the nursery, as operationalized in our continuous rotational pairing, leads to a biobehavioral profile that is most similar to that of infants raised by their mothers in large, socially complex, cages.

Figure 1

Effects of rearing condition on plasma cortisol concentrations at the 4 different sampling times. Significant main effect of rearing condition (CON, CP, CRP > IRP, p<0.05). Significant rearing x sample interaction (Sample 1: CON > IP, p<0.05; Sample 3: CON, CP, CRP > IRP, all p<0.01; Sample 4: CP, CRP > IRP, both p<0.05).

Figure 2

Effects of rearing condition on the proportion of time active (A), rate of self-stroke (B), and rate of cooing (C) during the Human Intruder test. Significant main effect of rearing condition (Activity: CRP > IP (p<0.05), IRP (p=0.054); Self-stroke: IP>CON (p=0.055), CRP (p=0.055); Coo: IRP > CON (p<0.01), CP (p<0.05)).

Figure 2

Effects of rearing condition on the proportion of time active (A), rate of self-stroke (B), and rate of cooing (C) during the Human Intruder test. Significant main effect of rearing condition (Activity: CRP > IP (p<0.05), IRP (p=0.054); Self-stroke: IP>CON (p=0.055), CRP (p=0.055); Coo: IRP > CON (p<0.01), CP (p<0.05)).

Figure 3

Effect of rearing condition on the Confident temperament factor. Significant main effect of rearing condition (CON > IRP (p<0.001), CP (p<0.05); CRP > IRP, p<0.001).