Toward a Standardized Test of Fearful Temperament in Primates: A Sensitive Alternative to the Human Intruder Task for Laboratory-Housed Rhesus Macaques (Macaca mulatta)

Abstract

Standardized and sensitive tests to assess differences in temperament among primates housed in captivity are essential for monitoring welfare and improving science outcomes through reduced noise in data. Fearful temperament in primates has traditionally been assessed using the Human Intruder Test (HIT) in which duration of bodily freeze in response to approach by an unknown human is measured. The HIT is susceptible to variation between facilities in execution, interpretation of data and could be stressful for animals with more fearful temperaments. We tested the applicability of a touch-screen task with putatively negative stimuli as a more standardizable and sensitive tool for measuring fearful temperament in laboratory primates. Seventeen adult male rhesus macaques were assessed for fearfulness using the HIT. They were then tested on a touch-screen task designed to measure two behavioral indices of fearfulness: behavioral inhibition and response-slowing. We predicted monkeys assessed as having more fearful temperament in the HIT, would show the greatest degree of behavioral inhibition and response-slowing to negative pictures in the touch-screen task. In Study 1, monkeys were rewarded with juice for touching gray squares on the screen (control trials). On test trials a picture of an unknown male conspecific face with direct-gaze (signaling threat) was shown. Monkeys were less likely to touch direct-gaze faces than control trials, indicating behavioral inhibition to threat. Behavioral inhibition was greatest amongst monkeys scored with most fearful temperament in the HIT. This primary result indicates the touch-screen task may be sensitive to a more subtle form of the bodily freeze behavior measured using the HIT. In Study 2, we tested whether these findings generalized to other classes of putatively negative stimuli; monkeys were shown pictures of the human intruder and objects associated with veterinary and husbandry procedures, interspersed with control trials (gray squares). There was no evidence of behavioral inhibition in Study 2. There was some evidence for response-slowing, which was greater for pictures of objects than pictures of the human intruder, and occurred independently of fearfulness in the HIT. We propose touch-screen tasks provide a more standardized and sensitive approach for assessing fearful temperament in laboratory primates.

In or out: Response slowing across housing conditions as a measure of affect in three Western lowland gorillas (Gorilla gorilla gorilla)

“…The pattern of data observed here is also consistent with findings from Bethell et al (2019) in which macaques showed behavioral inhibition (failure to respond at all to some stimuli) but not response slowing, which might cause one to call the procedure into question. However, it is possible that the lack of effect was due not to a failure of the procedure itself, but of the stimuli we selected.…”

“…This study provided a proof of concept indicating that response times can be used to indicate negative affect in apes. However, Bethell et al (2019) showed that macaques responded more slowly to pictures of objects than human intruders. This unexpected result, coupled with the fact that the response slowing procedure has not yet been shown to be effective with apes, suggests that the response slowing paradigm requires further validation for use with apes.…”

“…We were interested in the affect of three gorillas in a bachelor group as a function of habitat available to them throughout the day and night. Given the challenges of other paradigms used to assess affective state, we adopted a response slowing procedure ( Bethell et al, 2016 , 2019 ) both to assess its validity for assessing affect in apes, and for potentially evaluating the effects of housing conditions on the affect of these three gorillas.…”

“…Macaques that had been subjected to recent veterinary exams, which are considered stressful, displayed a slower latency to touch threatening stimuli compared to baseline. The test was later validated by showing that animals that showed the strongest response to the human intruder task (HIT)—a more invasive assessment of behavioral freezing in response to an unfamiliar human—also showed the greatest behavioral inhibition to the touchscreen task, in that they were most likely to not touch the threatening stimuli ( Bethell et al, 2019 ). However, responses in the HIT did not predict response slowing to the aversive stimuli in the computer task.…”

“…Although Bethell et al (2019) did not obtain strong validation for response slowing as a measure of affect, the task is worth investigating further given that it can be implemented quickly without the extended period of training that characterizes most of the cognitive bias assessments available to date. This procedure has also been used with gorillas, chimpanzees and Japanese macaques ( Cronin et al, 2018 ).…”