Oxidative stress and mitochondrial responses to stress exposure suggest that king penguins are naturally equipped to resist stress

Abstract

Exposure to unpredictable environmental stressors could influence animal health and fitness by inducing oxidative stress, potentially through downstream effects of glucocorticoid stress hormones ( e.g . corticosterone) on mitochondrial function. Yet, it remains unclear whether species that have evolved in stochastic and challenging environments may present adaptations to alleviate the effects of stress exposure on oxidative stress. We tested this hypothesis in wild king penguins by investigating mitochondrial and oxidative stress responses to acute restraint-stress, and their relationships with baseline (potentially mirroring exposure to chronic stress) and stress-induced increase in corticosterone levels. Acute restraint-stress did not significantly influence mitochondrial function. However, acute restraint-stress led to a significant increase in endogenous antioxidant defences, while oxidative damage levels were mostly not affected or even decreased. High baseline corticosterone levels were associated with an up-regulation of the glutathione antioxidant system and a decrease in mitochondrial efficiency. Both processes might contribute to prevent oxidative damage, potentially explaining the negative relationship observed between baseline corticosterone and plasma oxidative damage to proteins. While stress exposure can represent an oxidative challenge for animals, protective mechanisms like up-regulating antioxidant defences and decreasing mitochondrial efficiency seem to occur in king penguins, allowing them to cope with their stochastic and challenging environment.

Beyond corticosterone: The acute stress response increases DNA damage in house sparrows

“…In this study, we have shown that an acute period of restraint‐induced stress resulted in a significant increase in DNA damage in house sparrows (Figures 2a and 3). This study extends previous findings that draw connections between acute stress and DNA damage in wild animals (Malandrakis et al, 2016; Stier et al, 2014, 2019). Although brief physiological doses of cortisol, epinephrine, and norepinephrine—which mimic aspects of the acute stress response—induce significant DNA damage within 10 min in vitro (Flaherty et al, 2017; Flint et al, 2007), cell culture and whole animal are very different experimental systems.…”

“…Malandrakis et al (2016) found that gilthead seabream ( Sparus aurata ) that were confined had elevated levels of DNA damage measured in liver cells within 1 min. In addition, acutely restrained king penguins ( Aptenodytes patagonicus ; 30 min) had increased levels of oxidative DNA damage markers in their plasma, but not their red blood cells (Stier et al, 2019). Finally, acute (24 hr) cold exposure in zebra finches ( Taeniopygia guttata ) increased oxidative DNA damage markers in plasma samples (Stier et al, 2014).…”

“…These studies have used DNA damage to assess the effects of longer term stressors, including environmental pollution, radiation exposure, and captivity. A minority of studies have also examined the impacts of short‐term stressors—including immune activation (Meitern et al, 2013), cold exposure (Stier, Massemin, & Criscuolo, 2014), and restraint (Malandrakis et al, 2016; Stier et al, 2019)—on DNA damage. In this study, we tested the hypothesis that DNA damage increases acutely in the whole blood of house sparrows when exposed to standardized restraint stress.…”

“The stressed bird in the hand”: Influence of sampling design on the physiological stress response in a free-living songbird

“…We would, therefore, like to emphasise that we only recorded data over a short time frame and encourage follow-up studies to measure the recovery from capture and handling induced stress over a more extended period. Moreover, additional measures for stress, representing different physiological aspects within the stress response such as oxidative stress, should be applied and tested in future studies (Costantini, 2008; Stier et al, 2019).…”

Is there an oxidative cost of acute stress? Characterization, implication of glucocorticoids and modulation by prior stress experience

“…While GiOS itself has not been studied in much detail, other studies in domestic chickens ( Gallus gallus ) and prairie voles ( Microtus ochrogaster ) have also demonstrated increased oxidative stress in response to an acute stressor in the form of increased levels of oxidative damage [7,20,28]. However, studies in wild king penguins ( Aptenodytes patagonicus [29]) and a captive population of house sparrows ( Passer domesticus [30]) saw either no significant change or even a decrease in oxidative damage levels in response to acute stress. We therefore need more research across diverse vertebrate taxa to determine the shared nature of the stress response and oxidative stress in order to better understand the extent to which GiOS is conserved.…”