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.

The effect of long-term ovariectomy on midbrain stress systems in free ranging macaques

“…However, the trend toward Intact animals having higher CRF fibers in the dorsal raphe than the Ovx group is the opposite of earlier data. Although the ranks of the individuals did not change, the Intact individuals participated in sexual behavior to a significantly greater extent than the Ovx individuals (Coleman et al, 2011). There is an increase in fighting in the troop during mating season that would have involved the Intact animals to a much larger extent than the Ovx animals.…”

“…There were subtle differences between the regulation of serotonin-related genes by hormone replacement in the short-term Ovx monkeys compared to the differences in expression observed in the Intact versus long-term Ovx monkeys, again possibly related to the loss of serotonin neurons in the latter. We also reported that the same Ovx monkeys exhibited a decrease in positive social behavior in the troop and exhibited an increase in certain anxiety-related behaviors in temperament tests (Coleman et al, 2011). …”

“…After 3 years, the animals were collected for temperament tests, pharmacological challenges and euthanasia. The results of the behavioral observations and pharmacological challenge are published (Bethea et al, 2012; Coleman et al, 2011). …”

Managing the Cayo Santiago rhesus macaque population: The role of density

“…However, unwanted side-effects of hormone-mediated contraceptives such as diabetes mellitus, Cushing’s diseases, osteoporosis, weight gain, increased aggression, as well as suppression of oestrus and proceptive behavior might develop among individuals [Glatston, 1998]. Permanent sterilization has also been associated with negative effects on social behavior and anxiety in macaques [Colemana et al, 2011]. The use of contraceptive vaccines developed for wildlife in monkeys is also controversial as the adjuvants currently used caused skin lesions and infections and the duration of contraception is variable [Dascanio et al, 2014].…”

Effects of cocaine on aggression and associated central ERα and oxytocin expression in ovariectomized and intact mandarin voles

“…A previous study found that ovariectomized Japanese macaques (Macaca fuscata Blyth, 1875) exhibited a significant decrease in positive social behavior (Coleman et al 2011). In contrast, systemic estradiol-priming significantly increased time spent in social interaction with a conspecific in rats (Frye et al 2008).…”