The effects of predictability in daily husbandry routines on captive rhesus macaques (Macaca mulatta)

Abstract

Rhesus macaques (Macaca mulatta) housed indoors experience many routine husbandry activities on a daily basis. The anticipation of these events can lead to stress, regardless of whether the events themselves are positive or aversive in nature. The specific goal of this study was to identify whether increasing the predictability of husbandry events could decrease stress and anxiety in captive rhesus macaques. This study was conducted on 39 single-housed subjects in four indoor rooms at the Oregon National Primate Research Center. Temporal and signaled predictability were added to four daily husbandry events: morning and afternoon feeding, enrichment distribution, and room cleaning. Temporally predictable husbandry events occurred reliably at the same time daily, while signaled predictable husbandry events were preceded by a distinct event-specific signal in the form of a doorbell. Informal tests prior to study onset found the doorbells not to be aversive to the subjects. Subjects received each of four treatments: unpredictable events, temporally predictable events, signaled predictable events, and temporally and signaled predictable events. Change in stress was evaluated by monitoring changes in motor stereotypies and displacement behaviors. Our results showed that subjects displayed less stress and anticipatory behaviors related to feeding and enrichment events when the events were temporally predictable (P < 0 .0001). When husbandry events were preceded by a reliable signal, subjects vocalized less prior to the event and were less responsive to activity outside of the room (P < 0 .01). However this may have come at a cost as the animals were extremely reactive to the doorbell signals and showed a heightened stress response during the actual husbandry events (P < 0 .01). Similar to temporal predictability alone, when temporal predictability was combined with signaled predictability subjects displayed less stress and anticipatory behaviors related to feeding and enrichment events (P < 0 .0001). In addition, when both forms of predictability were combined subjects showed less stress behaviors while waiting for daily room cleaning (P < 0 .01). When signaled predictability was paired with temporal predictability subjects no longer had the negative response to the doorbell signal, as they were able to predict and anticipate when the events would occur. Because these results are not necessarily applicable to animals that are given control over their environment or housed in a group setting, the management recommendation that can be made from this study is that temporal predictability of feeding reduces stress and anxiety and is thus beneficial to captive indoor single-housed rhesus macaques.

Variation in the emission rate of sounds in a captive group of false killer whales Pseudorca crassidens during feedings: possible food anticipatory vocal activity?

“…Conversely, other studies have found that making feeding sessions predictable is an eff ective way to decrease the stress associated with both waiting for and experiencing these events (Krishnamurthy, 1994;Ulyan et al, 2006;Gottlieb et al, 2013). These fi ndings are contrary to the common idea that animals fed on a predictable schedule undergo a high level of anticipation and stress (Bassett and Buchanan-Smith, 2007).…”

“…These fi ndings are contrary to the common idea that animals fed on a predictable schedule undergo a high level of anticipation and stress (Bassett and Buchanan-Smith, 2007). Gottlieb et al (2013) suggested that a predictable schedule removes the "unknown" of the session, and even though it builds anticipation, it is less stressful than not knowing when food will be delivered. Moreover, when animals are fed on a temporal unpredictable schedule, they activate responses that can be adaptive when the individuals have a degree of control over the environment, for example by increasing the amount of exploration (Reneerkens et al, 2002).…”

“…Amongst the variety of behavioral changes that are considered indicative of FAA (Howell et al, 1993;Carlstead, 1998;Jensen et al, 2013), the variation of vocalizations is also a factor infl uenced by the schedule of feeding sessions (Krishnamurthy, 1994;Waitt and Buchanan-Smith, 2001;Ulyan et al, 2006;Gilbert-Norton et al, 2009; Polizzi di Sorrentino et al, 2010;Gottlieb et al, 2013). The false killer whales' group at Qingdao Polar Ocean World showed changes in acoustic activity approximately 30 minutes before the feeding sessions.…”

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

“…Full body repetitive behaviors, known as motor stereotypic behaviors (MSBs), are the most commonly seen abnormal behavior in rhesus macaques (Lutz et al, 2003); in a survey of three National Primate Research Centers, 18-49% of singly housed rhesus monkeys were reported as displaying some form of MSB, such as repetitive pacing, bouncing, swaying, rocking, or somersaulting (Lutz et al, 2011). Because they are often linked to frustration, lack of stimulation, lack of environmental control, and/or unavoidable stress (Mason, 1991; Mason and Latham, 2004; Mench and Mason, 1997), MSBs are frequently used as a behavioral metric to help evaluate captive primate well-being (e.g., Bayne et al, 1991; Gottlieb et al, 2013b; Novak et al, 1998). Common remediation strategies include foraging enrichment and socialization.…”

Coping with Change: A Closer Look at the Underlying Attributes of Change and the Individual Response to Unstable Environments

“…When these predictions are no longer accurate, due to shifts in food peaks or changes in weather patterns, the behaviours that were adaptive during many species' evolutionary history can become a problem [33,48]. In addition, animals' inability to predict events increases their stress response, and as such lowers their overall health [49]. Since predictability of environmental events is limited not only to the frequency and regularity of the events, but also to the cognitive abilities and experience of the individual, prediction affects whether and how an individual might respond, and as such can be considered a relevant attribute of the process of change.…”