Age, oxidative stress exposure and fitness in a long‐lived seabird

Abstract

Article (refereed) -postprintHerborn, Katherine A.; Daunt, Francis; Heidinger, Britt J.; Granroth-Wilding, Hanna M.V.; Burthe, Sarah J.; Newell, Mark A.; Monaghan, Pat. 2016. Age, oxidative stress exposure and fitness in a long-lived seabird. Functional Ecology, 30 (6). 913-921. 10.1111/1365-2435.12578 Contact CEH NORA team at noraceh@ceh.ac.ukThe NERC and CEH trademarks and logos ('the Trademarks') are registered trademarks of NERC in the UK and other countries, and may not be used without the prior written consent of the Trademark owner. Accepted ArticleThis article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. Accepted ArticleThis article is protected by copyright. All rights reserved.Key Words: Life history trade-off, Senescence, Oxidative stress, Phalacrocorax aristotelis Summary 1) The need to manage exposure to oxidative stress, which can damage macromolecules, is thought to influence the resolution of life history trade-offs. Oxidative damage is expected to increase with age as a consequence of changes in the optimal investment in defences or repair, and/or because of senescence in antioxidant defence systems, though the pattern might differ between short and long-lived species. However, data on age related changes in damage levels in wild populations are rare.2) Using cross-sectional and longitudinal data collected over three years, we examine variation in a measure of oxidative damage exposure in known age, wild European Shags (Phalacrocorax aristotelis), a relatively long lived species.3) The cross-sectional data showed a quadratic relationship between oxidative damage exposure and age: both relatively young and old adults had higher levels than those in middle age. In contrast, a measure of non-enzymatic antioxidant levels did not vary with age.4) The cross-sectional increase in oxidative damage exposure in later life was consistent with longitudinal patterns observed within older birds (more than 10 years old).5) However, the apparent decline in oxidative damage in early adulthood was not consistent with longitudinal patterns in younger birds, which showed individual variation but no consistent age-related change in the marker. This suggests that cross-sectional patterns reflect instead higher disappearance of individuals with high exposure to oxidative damage at this life stage 6) Our data further show that oxidative damage levels are predictive of attendance at the colony in all age classes: juveniles fledging with a high damage exposure index were less likely to be resighted in the breeding colony two years later, and adults with high levels at the end of the breeding season had reduced return rates, irrespective of age. Since this is a species that shows high colony fidelity, this is likely to reflect mortality patterns. Accepted ArticleThis article is protected by copyright. All rights reserved.7) These d...

Environmental conditions can modulate the links among oxidative stress, age, and longevity

“…Interestingly, our results are somewhat in contrast with recent findings in wild European Shags (Phalacrocorax aristotelis), a relatively long-lived bird species. In this species, an increase in oxidative stress exposure, was only evident at old age (Herborn et al 2015). Such inter-specific differences might arise as a consequence of lifehistory related differences in the pattern of investment in somatic tissue defences.…”

“…For example, studies in mice genetically modified to increase exposure to ROS via altering specific antioxidants, generally showed no effect on the probability of survival, but rather contributed to the progression of diseases (Salmon et al 2010). The recent growing body of work in un-manipulated individuals primarily carried out in free-living bird populations has also shown mixed results (reviewed in Costantini, 2014), with some studies supporting the idea of negative association among markers of oxidative damage and survival (Freeman-Gallant et al 2011;Noguera et al 2012, Costantini et al 2015a, Herborn et al 2015, and others reporting no association (Beaulieu et al 2011;Stier et al 2014c;Costantini et al 2015b). The variable outcomes may be due to several factors, including species-specific patterns, differences in life-stages between individuals (e.g.…”

“…early mortality of poor quality individuals - Nussey et al 2008;Bouwhuis et al 2009). This can mask the true within-individual pattern of age-related variation in oxidative stress (Herborn et al 2015). Though not always possible for a variety of reasons, repeated sampling of the same individual through time is essential to examine age-related changes in oxidative stress levels.…”

“…Though not always possible for a variety of reasons, repeated sampling of the same individual through time is essential to examine age-related changes in oxidative stress levels. To date only a few studies in the laboratory (Matsuo et al 1993;Alonso-Alvarez et al 2006) and in the wild (Bize et al 2014;Herborn et al 2015) have used such longitudinal sampling designs. These within-individual studies do find that selective disappearance of individuals with high oxidative stress levels does occur (Herborn et al 2015), but generally also find evidence of age-related increases in oxidative stress exposure or agerelated decreases in cell resistance to oxidative stress (Matsuo et al 1993;Bize et al 2014).…”

Family-transmitted stress in a wild bird

“…In birds, prenatal elevation of corticosterone levels is associated with postnatal oxidative costs (40), agreeing with our result of the longterm effect of early exposure to corticosterone on oxidative damage. Importantly, high levels of oxidative damage at fledging are related to a reduction in adult survival in seabirds (41,42).…”