Sex-specific effects of inbreeding and early life conditions on the adult oxidative balance.

Inbreeding negatively affects various life-history traits, with inbred individuals typically having lower fitness than outbred individuals (= inbreeding depression). Inbreeding depression is often emphasized under environmental stress, but the underlying mechanisms and potential long-lasting consequences of such inbreeding-environment interactions remain poorly understood. Here, we hypothesize that inbreeding-environment interactions that occur early in life have long-term physiological effects, in particular on the adult oxidative balance. We applied a unique experimental design to manipulate early life conditions of inbred and outbred songbirds (Serinus canaria) that allowed us to separate prenatal and postnatal components of early life conditions and their respective importance in inbreeding-environment interactions. We measured a wide variety of markers of oxidative status in adulthood, resulting in a comprehensive account for oxidative balance. Using a Bayesian approach with Markov chain Monte Carlo, we found clear sex-specific effects and we also found only in females small yet significant long-term effects of inbreeding-environment interactions on adult oxidative balance. Postnatal components of early life conditions were most persuasively reflected on adult oxidative balance, with inbred females that experienced disadvantageous postnatal conditions upregulating enzymatic antioxidants in adulthood. Our study provides some evidence that adult oxidative balance can reflect inbreeding-environment interactions early in life, but given the rather small effects that were limited to females, we conclude that oxidative stress might have a limited role as mechanism underlying inbreeding-environment interactions.

Ambient anthropogenic noise but not light is associated with the ecophysiology of free-living songbird nestlings.

Urbanization is associated with dramatic increases in noise and light pollution, which affect animal behaviour, physiology and fitness. However, few studies have examined these stressors simultaneously. Moreover, effects of urbanization during early-life may be detrimental but are largely unknown. In developing great tits (Parus major), a frequently-used model species, we determined important indicators of immunity and physiological condition: plasma haptoglobin (Hp) and nitric oxide (NOx) concentration. We also determined fledging mass, an indicator for current health and survival. Associations of ambient noise and light exposure with these indicators were studied. Anthropogenic noise, light and their interaction were unrelated to fledging mass. Nestlings exposed to more noise showed higher plasma levels of Hp but not of NOx. Light was unrelated to Hp and NOx and did not interact with the effect of noise on nestlings' physiology. Increasing levels of Hp are potentially energy demanding and trade-offs could occur with life-history traits, such as survival. Effects of light pollution on nestlings of a cavity-nesting species appear to be limited. Nonetheless, our results suggest that the urban environment, through noise exposure, may entail important physiological costs for developing organisms.

Neither artificial light at night, anthropogenic noise nor distance from roads are associated with oxidative status of nestlings in an urban population of songbirds.

Increasing urbanization is responsible for road-related pollutants and causes an unprecedented increase in light and noise pollution, with potential detrimental effects for individual animals, communities and ecosystems. These stressors rarely act in isolation but studies dissecting the effects of these multiple stressors are lacking. Moreover, studies on urban stressors have mainly focused on adults, while exposure in early-life may be detrimental but is largely ignored. To fill this important knowledge gap, we studied if artificial light at night, anthropogenic noise and road-related pollution (using distance from roads as a proxy) explain variation in oxidative status in great tit nestlings (Parus major) in an urban population. Artificial light at night, anthropogenic noise and distance from roads were not associated with variation of the nine studied metrics of oxidative status (superoxide dismutase-SOD-, glutathione peroxidase-GPX, catalase-CAT-, non-enzymatic total antioxidant capacity-TAC-, reduced glutathione-GSH-, oxidized glutathione-GSSG-, ratio GSH/GSSG, protein carbonyls and thiobarbituric acid reactive substances-TBARS). Interestingly, for all oxidative status metrics, we found that there was more variation in oxidative status among individuals of the same nest compared to between different nests. We also showed an increase in protein carbonyls and a decrease of the ratio GSH/GSSG as the day advanced, and an increase of GPX when weather conditions deteriorated. Our study suggests that anthropogenic noise, artificial light at night and road-related pollution are not the most important sources of variation in oxidative status in great tit nestlings. It also highlights the importance of considering bleeding time and weather conditions in studies with free-living animals.

Elevated reproduction does not affect telomere dynamics and oxidative stress.

ABSTRACT: Oxidative stress and telomere dynamics are considered to be powerful biomarkers quantifying a potential trade-off between current reproduction and self-maintenance. Recent studies confirmed the negative impact of elevated reproduction on telomeres, but the evidence for the cost of reproduction in terms of oxidative stress remains equivocal. In order to induce reproductive costs, we experimentally manipulated reproductive effort by increasing brood size in captive zebra finches (Taeniopygia guttata) and additionally challenged all birds by a low ambient temperature to facilitate detection of these costs. We were not able to show any negative effects of elevated reproductive effort on telomere dynamics and oxidative stress among parents, although brood enlargement was effective in terms of total mass and number of fledged young. Interestingly, irrespective of brood size treatment, we found a significant increase in antioxidant capacity at peak breeding while oxidative damage did not change with time. Our results may suggest that reproduction, instead of generating costs, may stimulate physiological functions promoting self-maintenance in terms of higher protection against free radicals. Possibly, opportunistic breeders such as zebra finches may not impede their future performance for the sake of current reproduction. SIGNIFICANCE STATEMENT: This study interrogates a molecular background behind one of the most intriguing trade-offs that potentially occurs between self-maintenance and reproduction. We manipulated breeding effort in zebra finches to understand if the cost of reproduction can be mediated by telomere dynamics and oxidative stress. In our study system, we did not detect the direct reproductive costs in terms of parental oxidative damage and telomere loss; instead, these costs were paid by the offspring in terms of their inhibited growth rate. Moreover, we found that entering into the reproductive state strongly stimulated self-maintenance by increasing antioxidant capacity in parents. Our results emphasize that current reproductive success is not always prioritized over investment in body maintenance preventing the oxidative cost of reproduction.

Artificial light at night affects body mass but not oxidative status in free-living nestling songbirds: an experimental study.

Artificial light at night (ALAN), termed light pollution, is an increasingly important anthropogenic environmental pressure on wildlife. Exposure to unnatural lighting environments may have profound effects on animal physiology, particularly during early life. Here, we experimentally investigated for the first time the impact of ALAN on body mass and oxidative status during development, using nestlings of a free-living songbird, the great tit (Parus major), an important model species. Body mass and blood oxidative status were determined at baseline (=13 days after hatching) and again after a two night exposure to ALAN. Because it is very difficult to generalise the oxidative status from one or two measures we relied on a multi-biomarker approach. We determined multiple metrics of both antioxidant defences and oxidative damage: molecular antioxidants GSH, GSSG; antioxidant enzymes GPX, SOD, CAT; total non-enzymatic antioxidant capacity and damage markers protein carbonyls and TBARS. Light exposed nestlings showed no increase in body mass, in contrast to unexposed individuals. None of the metrics of oxidative status were affected. Nonetheless, our study provides experimental field evidence that ALAN may negatively affect free-living nestlings' development and hence may have adverse consequences lasting throughout adulthood.

Early life exposure to artificial light at night affects the physiological condition: An experimental study on the ecophysiology of free-living nestling songbirds.

Light pollution or artificial light at night (ALAN) is increasingly recognised to be an important anthropogenic environmental pressure on wildlife, affecting animal behaviour and physiology. Early life experiences are extremely important for the development, physiological status and health of organisms, and as such, early exposure to artificial light may have detrimental consequences for organism fitness. We experimentally manipulated the light environment of free-living great tit nestlings (Parus major), an important model species in evolutionary and environmental research. Haptoglobin (Hp) and nitric oxide (NOx), as important indicators of immunity, health, and physiological condition, were quantified in nestlings at baseline (13 days after hatching) and after a two night exposure to ALAN. We found that ALAN increased Hp and decreased NOx. ALAN may increase stress and oxidative stress and reduce melatonin which could subsequently lead to increased Hp and decreased NOx. Haptoglobin is part of the immune response and mounting an immune response is costly in energy and resources and, trade-offs are likely to occur with other energetically demanding tasks, such as survival or reproduction. Acute inhibition of NOx may have a cascading effect as it also affects other physiological aspects and may negatively affect immunocompetence. The consequences of the observed effects on Hp and NOx remain to be examined. Our study provides experimental field evidence that ALAN affects nestlings' physiology during development and early life exposure to ALAN could therefore have long lasting effects throughout adulthood.

Does reproduction protect against oxidative stress?

A central principle of life-history theory is that parents trade investment in reproduction against that in body maintenance. One physiological cost thought to be important as a modulator of such trade-off is oxidative stress. Experimental support for this hypothesis has, however, proved to be contradictory. In this study, we manipulated the nestling rearing effort of captive canaries (Serinus canaria) soon after the hatching of their nestlings using a brood-size manipulation to test whether an increase in nestling rearing effort translates into an increase in oxidative damage, an increase in ceruloplasmin (which is upregulated in response to oxidative damage) and a decrease in thiol antioxidants. We also compared the blood oxidative stress level of reproducing birds with that of non-reproducing birds, a crucial aspect that most studies have invariably failed to include in tests of the oxidative cost of reproduction. Compared with non-breeding canaries and pre-manipulation values, plasma oxidative damage (reactive oxygen metabolites and protein carbonyls) decreased in breeding canaries irrespective of sex and brood size. In contrast, oxidative damage did not change in non-breeding birds over the experiment. Ceruloplasmin activity in plasma and both non-protein and protein thiols in red blood cells did not change throughout the experiment in both treatment groups. Our results suggest that reproduction may result in decreased rather than increased blood oxidative stress. Our results may explain some of the inconsistencies that have so far been reported in experimental tests of the oxidative cost of reproduction hypothesis.