Long-term ovariectomy alters social and anxious behaviors in semi-free ranging Japanese macaques

Abstract

Symptoms of anxiety and depression often occur in young women after complete hysterectomy and in older women during menopause. There are many variables that are hard to control in human population studies, but that are absent to a large extent in stable nonhuman primate troops. However, macaques exhibit depressive and anxious behaviors in response to similar situations as humans such as isolation, stress, instability or aggression. Therefore, we hypothesized that examination of behavior in ovariectomized individuals in a stable macaque troop organized along matriarchal lineages and in which individuals have social support from extended family, would reveal effects that were due to the withdrawal of ovarian steroids without many of the confounds of human society. We also tested the hypothesis that ovariectomy would elicit and increase anxious behavior in a stressful situation such as brief exposure to single caging. Japanese macaques (Macaca fuscata) were ovariectomized (Ovx) or tubal-ligated (intact controls) at 3 years of age and allowed to mature for 3 years in a stable troop of approximately 300 individuals. Behaviors were recorded in the outdoor corral in the third year followed by individual temperament tests in single cages. There was no obvious difference in anxiety-related behaviors such as scratching between Ovx and tubal-ligated animals in the corral. Nonetheless, compared to tubal-ligated animals, Ovx animals exhibited a significant decrease in (1) positive social behavior, (2) initiating dominance behavior, (3) time receiving grooming, (4) locomoting, (5) mounting behavior, and in (6) consort behavior. However, Ovx females exhibited a significant increase in (1) consummatory behavior and (2) object play compared to tubal-ligated controls. In the individual temperament tests, Ovx individuals exhibited an increase in anxiety-related behaviors. There was no difference in adrenal weight/body weight suggesting that neither group was under chronic stress. These data indicate that ovarian hormones enable females to successfully navigate their social situation and may reduce anxiety in novel situations.