Stress, the HPA axis, and nonhuman primate well-being: A review

Abstract

Numerous stressors are routinely encountered by wild-living primates (e.g., food scarcity, predation, aggressive interactions, and parasitism). Although many of these stressors are eliminated in laboratory environments, other stressors may be present in that access to space and social partners is often restricted. Stress affects many physiological systems including the hypothalamic-pituitary-adrenocortical (HPA) axis, which is the focus of this review. The glucocorticoid, cortisol, is the ultimate output of this system in nonhuman primates, and levels of this hormone are used as an index of stress. Researchers can measure cortisol from several sampling matrices that include blood, saliva, urine, faeces, and hair. A comparison of the advantages and disadvantages of each sampling matrix is provided to aid researchers in selecting an optimal strategy for their research. Stress and its relationship to welfare have been examined in nonhuman primates using two complimentary approaches: comparing baseline cortisol levels under different conditions, or determining the reactivity of the system through exposure to a stressor. Much of this work is focused on colony management practices and developmental models of abnormal behaviour. Certain colony practices are known to increase stress at least temporarily. Both blood sampling and relocation are examples of this effect, and efforts have been made to reduce some of the more stressful aspects of these procedures. In contrast, other colony management practices such as social housing and environmental enrichment are hypothesized to reduce stress. Testing this hypothesis by comparing baseline cortisol levels has not proved useful, probably due to “floor” effects; however, social buffering studies have shown the powerful role of social housing in mitigating reactions of nonhuman primates to stressful events. Models of abnormal behaviour come from two sources: experimentally induced alterations in early experience (e.g., nursery rearing), and the spontaneous development of behavioural pathology (e.g., self-injurious behaviour). Investigators have often assumed that abnormal behaviour is a marker for stress and thus such monkeys are predicted to have higher cortisol levels than controls. However, an emerging finding is that monkeys with abnormal behaviour are more likely to show a pattern of lowered cortisol concentrations which may reflect either an altered set point or a blunting of the stress response system. These findings parallel human clinical studies demonstrating that neuropsychiatric disorders may be associated with either increased or decreased activity of the HPA system, depending on the aetiology and manifestation of the disorder and their potential influence in provoking allostatic shifts in system functioning.

Robust gene expression changes in the ganglia following subclinical reactivation in rhesus macaques infected with simian varicella virus

“…This is in line with the incidence rate of HZ in bone marrow transplant patients, which had been reported to reach 43%(Chen et al , 2014; Koc et al , 2000; Novak et al , 2013). However, our reactivation rates are lower than those observed in macaques that have undergone whole body irradiation coupled with immune suppressive treatments (Mahalingam et al , 2010), in line with the reduced severity of immune suppression due to accelerated senescence of only one T cell compartment.…”

“…Also, fecal cortisol increases have also been observed in chimpanzees moved to a new facility (Reimers et al, 2007). In addition, temporary moves of two days or less have also been shown to increase cortisol levels in rhesus, bonnet and cynomolgus macaques as well (Novak et al, 2013). …”

Hair cortisol and dehydroepiandrosterone concentrations in naturally Taenia solium infected pigs in Tanzania

“…Furthermore, steroids measurement in hair allows a long-term evaluation of chronic stress with a negligible influence of acute stress events (Novak et al, 2013). Hair sampling is a non-invasive, easy and painless procedure and has a low level of invasiveness associated with the sample collection.…”

Population density-dependent hair cortisol concentrations in rhesus monkeys (Macaca mulatta)

“…This technique has since been applied in studies of chronic HPA axis activity (i.e., accumulation of cortisol into the hair shaft over the past several months, as opposed to minutes or hours as in the point samples mentioned above) in both animals (Bechchøft et al, 2012; Davenport et al, 2008; Malcom et al, 2012; Meyer and Novak, 2012; Novak et al, 2013) and humans (O’Brien et al, 2012; Vanaelst et al, 2013). Studies utilizing hair cortisol have shown that HCCs decline during the first several years of life in several nonhuman primate species including rhesus monkeys (Dettmer et al, 2012; Feng et al, 2011), vervets (Laudenslager et al, 2012), and baboons (Fourie & Bernstein, 2011), and one study also demonstrated sex differences in HCCs in nonhuman primates during puberty and adulthood (Laudenslager et al, 2012).…”