Dexamethasone treatment supports age‐related maturation of the stress response in altricial nestling birds

Abstract

In birds, the magnitude of the adrenocortical stress response can be down‐regulated during specific life‐history stages. Such modulation likely occurs when the effects of mounting robust corticosterone (Cort) elevations interfere with the normal progression of critical lifecycle activities (e.g. development, molt, migration, reproduction). The developmental hypothesis posits that altricial birds should display a ‘stress hyporesponsive period’ during the early post‐natal life stages, characterized by reduced adrenocortical stress responses compared to adult birds and a gradual age‐related increase. Such modulation would allow avoiding the potential deleterious effects that long‐term elevations of circulating Cort might exert on growth and development, when the physiological and behavioral abilities to cope with disturbance are limited. Two proximate hypotheses have been proposed to explain this age‐dependent pattern of Cort secretion. The ‘maturation hypothesis’ proposes a progressive age‐related growth, maturation and enhanced sensitivity to sensory input of the Hypothalamic‐Pituitary‐Adrenal (HPA) axis tissues, whereas the ‘negative feedback attenuation hypothesis’ proposes a gradual attenuation in the intensity of the negative feedback in the HPA axis. Here we tested these hypotheses by experimentally inducing negative feedback on the HPA axis via dexamethasone (DEX) treatment in nestling white storks Ciconia ciconia. Nestling age positively affected stress‐induced plasma Cort (STRESS‐Cort) levels during experimental handling and restraint, thus supporting the developmental hypothesis. DEX treatment significantly reduced STRESS‐Cort levels compared to saline (SAL) treatment, thus eliciting the expected negative feedback on the HPA axis. However, inter‐ and intra‐individual comparisons indicated no age effects on the intensity of the negative feedback exerted by DEX. Our results do not support the negative feedback attenuation hypothesis and suggest that progressive maturation of the HPA axis tissues is the proximate mechanism responsible for age‐related changes in the stress response during avian post‐natal development. We encourage further tests of the proposed proximate mechanisms during migration, breeding and molt.

Corticosterone release in very young siblicidal seabird chicks (Rissa tridactyla) is sensitive to environmental variability and responds rapidly and robustly to external challenges

“…Though altered sensitivity to negative feedback has been proposed as a potential mechanism to explain ontogenetic changes in HPA activity in chicks, this hypothesis was not supported in white storks (Torres Medina et al, 2019). Similarly, our study suggests that it does not explain variation in HPA activity between young kittiwake chicks from supplemented and nonsupplemented nests, though age-related changes have not yet been tested.…”

“…Thus, while endogenous secretion of corticosterone in 5 day old chicks is sensitive to environmental context, other aspects of HPA function are not: rapid negative feedback and/or the ability to clear acute exogenous elevations in corticosterone. Though changes in sensitivity to negative feedback has been proposed as a potential mechanism to explain ontogenetic changes in HPA activity in chicks, this hypothesis was not supported in white storks (Torres-Medina et al, 2019). Similarly, our study suggests that it does not explain variation in HPA activity between young kittiwake chicks from fed and unfed nests, though age-related changes have not yet been tested.…”

“…Many altricial and some semi-altricial species have a post-hatch “hypo-responsive” period (the “stress non-responsive period” in mammals) of relatively low HPA axis responsiveness (Bebus et al, 2020; Blas et al, 2006; Fiske et al, 2013, Jones et al, 2021; Sims and Holberton, 2000; Tilgar et al 2009; Wada et al, 2009, 2007). This developmental pattern is thought to protect young chicks who are both vulnerable to excessive glucocorticoid exposure and too early in development to benefit from elevated glucocorticoids because they have life-histories that leave them unable to change physiology or behavior in sufficiently rapid or appropriate ways to increase fitness (Fiske et al, 2013; Sims and Holberton, 2000; TorresLMedina et al, 2019; Wada, 2008; Wada et al, 2007). However, some species have life-histories that involve complex early-life social dynamics that may be influenced by glucocorticoids (reviewed in Smiseth et al, 2011) and would therefore be expected to activate the HPA axis early in life.…”

“…Lynn and Kern, 2018, 2014). The existence and duration of a post-hatch “hypo-sensitive” period (the “stress non-responsive period” in mammals) of relatively low HPA axis responsiveness in many altricial (Bebus et al, 2020; Jones et al, 2021; Sims and Holberton, 2000; Wada et al, 2009, 2007) and some semi-altricial (Blas et al, 2006; Fiske et al, 2013) species is thought to protect young chicks who are both vulnerable to excessive glucocorticoid exposure and too early in development to benefit from elevated glucocorticoids because they have life-histories that leave them unable to change physiology or behavior in sufficiently rapid or appropriate ways to increase fitness (Fiske et al, 2013; Sims and Holberton, 2000; Torres-Medina et al, 2019; Wada, 2008; Wada et al, 2007). In this study, we examined sources of variation in HPA axis activity in very young semi-precocial seabird chicks with a life-history that involves complex early-life social dynamics that may be influenced by glucocorticoids (reviewed in Smiseth et al, 2011).…”