The ecology of stress: effects of the social environment

Abstract

Summary Many aspects of the social environment affect hypothalamic‐pituitary‐adrenal (HPA) axis function and increase circulating glucocorticoid concentrations. In this review, we examine the relationships between the social environment and the function of the HPA axis in vertebrates. First, we explore the effects of the social environment on glucocorticoid secretion in territorial (primarily non‐social) species, with an emphasis on the effects of variation in population density, as modified by environmental factors such as predation risk and food availability. In general, high population density or frequent territorial intrusions are associated with increased glucocorticoid secretion in a wide range of taxa, including mammals, birds, fish and reptiles, although there is considerable variability across species. Second, we consider the effects of social interactions and dominance rank on glucocorticoid secretion in social species, mostly in birds and mammals. We review studies that have detected an association between social status and glucocorticoid levels – sometimes with higher glucocorticoid levels in low‐ranking individuals, and sometimes with higher glucocorticoid levels in dominant individuals. The relationship between dominance and glucocorticoid levels varies among species, populations and years, in a manner that depends on the stability of the social hierarchy, environmental conditions, the type of breeding system, and the manner in which high rank is obtained and maintained. Finally, we discuss the concept of allostasis and consider interactions between social effects and other environmental factors, noting that there is relatively little research on these interactions to date. For both non‐social and social species, we identify priorities of future research. These priorities include more complete descriptions of HPA function that move beyond measurements of basal glucocorticoid concentrations (which will generally require field experiments), to studies that examine organizational effects of social stressors, that directly test the relationship between HPA function and fitness, and that examine how glucocorticoid responses affect population dynamics. Although several lines of evidence suggest that glucocorticoid responses can affect the fitness of individuals and therefore can alter the dynamics of populations, the effect of glucocorticoid responses on population dynamics remains essentially unstudied.

Mean fecal glucocorticoid metabolites are associated with vigilance, whereas immediate cortisol levels better reflect acute anti-predator responses in meerkats

“…Meerkats forage in cohesive groups and therefore, within groups, individuals experience similar local environmental conditions including predation pressure.Sex, body condition, reproductive stage (Keay et al, 2006;Millspaugh and Washburn, 2004), and social context (Creel et al, 2013) are all likely to affect both adrenal activity and time required to respond to potential predators. In meerkats, dominance status (Carlson et al, 2004) and the presence of pups can influence plasma GC , and reproductive stage affects mean fGC concentrations (Barrette et al, 2012).…”

“…Harvey et al, 1984, Bush and Hayward, 2009, Zanchi et al, 2010, Goymann 2012), which in turn, can affect individuals" response to internal and external stimuli (Dowle et al, 2012). Under challenging conditions, such as food deprivation, social instability or predation risk (Dallman et al, 1993;Creel et al, 2009Creel et al, , 2013 adrenal activity increases the production of glucocorticoids (GCs) to mobilize energy and resolve stressful stimuli (Harvey et al, 1984;McEwen and Wingfield, 2003;Wingfield, 2005;Romero et al, 2009). In turn, GCs can modulate the intensity of behavioral responses to stimuli such as presence of predators (Sapolsky et al, 2000).…”

How birds cope physiologically and behaviourally with extreme climatic events

“…Specific individual characteristics such as social status, body condition and territory quality can also influence Egained in terms of access to food and variation of quality with habitat. Given these diverse contributions to energy available to the individual we consider the cumulative resources available (Ecr) that ultimately affect an individual and are critical for the allostasis concept but are largely ignored in other discussions of allostasis and reactive scope [14,16,[41][42][43]. In the absence of considering Ecr, then the assumption must be that food and access to it is ad libitum.…”

Responses to social and environmental stress are attenuated by strong male bonds in wild macaques

“…Because most males compete for opportunities to fertilize females (30) the focus of studies investigating correlates of male physiological stress have historically been on reproductive competition and hierarchical status (31)(32)(33). Nevertheless, recent and increasing evidence has shown that males of some vertebrate species also form strong social bonds that can enhance their fitness (refs.…”