Evaluation of environmental and intrinsic factors that contribute to stereotypic behavior in captive rhesus macaques (Macaca mulatta)

Abstract

Full body repetitive behaviors, known as motor stereotypic behaviors (MSBs), are one of the most commonly seen abnormal behaviors in captive non-human primates, and are frequently used as a behavioral measure of well-being. The main goal of this paper was to examine the role of environmental factors (i.e., foraging enrichment and socialization) and intrinsic factors (i.e., temperament and origin) in the development of MSB in rhesus macaques living in cages. MSB was assessed during short annual observations in which a trained observer recorded a monkey's behavior for 5 min, followed by a 3-min novel object test. Data were collected over 11 years, totaling 9805 observations. We compared MSB for animals with and without foraging enrichment, and across three socialization conditions: full contact pairing, protected contact socialization (partners physically separated by widely spaced bars), and single housing. In addition, we evaluated whether individual differences in response to a novel object and ancestral origin (i.e., China vs. India), predicted MSB expression during the annual observations. Data were analyzed using generalized mixed effects modeling, with the best fitting models chosen using Akaike Information Criterion. Subjects were at lowest risk for MSB when a foraging device was present (p < 0.05), and when in full contact social housing (p < 0.001). There was no statistically significant difference in MSB between subjects that were single housed and subjects housed in protected contact pairs. In addition, subjects that never touched the novel object were significantly less likely to exhibit MSB than those that touched the object immediately (p < 0.001) or within 3 min (p < 0.001). Finally, monkeys with some degree of Chinese ancestry were significantly more likely to display MSB than Indian-origin monkeys (p < 0.05). These results add to the growing body of literature on factors that can contribute to the development of MSB.

Keywords: abnormal behavior; enrichment; foraging; protected-contact; stereotypy; temperament; welfare.

Fig. 1

Two rhesus macaques utilizing a type of foraging enrichment.

Fig. 2

Percent of observations in which subjects displayed motor stereotypic behavior in housing conditions (single housed, protected contact housed, and full contact pair housed). *** indicates significant differences at P < 0.001. Note: Plot represents raw data, however statistical analyses and effect sizes were calculated while controlling for all other variables.

Fig. 3

Percent of observations in which subjects displayed motor stereotypic behavior categorized by subject’s response to novel object: inspected the object within 5 sec (Bold), inspected the object in more than 5 sec (Moderate), or did not inspect object (Inhibited). *** indicates significant differences at P < 0.001. Note: Plot represents raw data, however statistical analyses and effect sizes were calculated while controlling for all other variables.

Fig. 4

Percent of observations in which subjects from various rearing conditions displayed motor stereotypic behavior. Rearing conditions that have the same shading have overlapping 95% confidence intervals and are not considered significantly different. Note: Plot represents raw data, however statistical analyses, and effect sizes, and 95% confidence intervals were calculated while controlling for all other variables.