Flight and Dietary Antioxidants Influence Antioxidant Expression and Activity in a Migratory Bird

Abstract

Ecologically-relevant factors such as exercise and diet quality can directly influence how physiological systems work including those involved in maintaining oxidative balance; however, to our knowledge, no studies to date have focused on how such factors directly affect expression of key components of the endogenous antioxidant system (i.e., transcription factors, select antioxidant genes, and corresponding antioxidant enzymes) in several metabolically active tissues of a migratory songbird. We conducted a 3-factor experiment that tested the following hypotheses: (H1) Daily flying over several weeks increases the expression of transcription factors NRF2 and PPARs as well as endogenous antioxidant genes (i.e., CAT, SOD1, SOD2, GPX1, GPX4), and upregulates endogenous antioxidant enzyme activities (i.e., CAT, SOD, GPx). (H2) Songbirds fed diets composed of more 18:2n-6 PUFA are more susceptible to oxidative damage and thus upregulate their endogenous antioxidant system compared to when fed diets with less PUFA. (H3) Songbirds fed dietary anthocyanins gain additional antioxidant protection and thus upregulate their endogenous antioxidant system less compared to songbirds not fed anthocyanins. Flight training increased the expression of 3 of the 6 antioxidant genes and transcription factors measured in the liver, consistent with H1, but for only one gene (SOD2) in the pectoralis. Dietary fat quality had no effect on antioxidant pathways (H2) whereas dietary anthocyanins increased the expression of select antioxidant enzymes in the pectoralis, but not in the liver (H3). These tissue-specific differences in response to flying and dietary antioxidants are likely explained by functional differences between tissues as well as fundamental differences in their turnover rates. The consumption of dietary antioxidants along with regular flying enables birds during migration to stimulate the expression of genes involved in antioxidant protection likely through increasing the transcriptional activity of NRF2 and PPARs, and thereby demonstrates for the first time that these relevant ecological factors affect the regulation of key antioxidant pathways in wild birds. What remains to be demonstrated is how the extent of these ecological factors (i.e., intensity or duration of flight, amounts of dietary antioxidants) influences the regulation of these antioxidant pathways and thus oxidative balance.

Experimental evidence that EPA and DHA are dietary requirements in a migratory shorebird, but they do not affect muscle oxidative capacity

“…However, without significant differences in oxidative enzymes among diets, dietary n-3 PUFAs likely do not greatly influence lipid metabolism at this level in western sandpipers. Previously, the role of dietary PUFAs in migratory birds focused on the class of PUFA (n-3 versus n-6 PUFAs: Dick and Guglielmo, 2019 ; Price and Guglielmo, 2009 ) or specifically on the role of the n-6 PUFA 18:2 n-6 ( Carter et al, 2020 ; DeMoranville et al, 2021 ; Price et al, 2022 ). Generally, these studies found that dietary PUFAs have little to no influence on lipid oxidative capacity and that seasonal changes and/or exercise may have larger impacts on muscle physiology ( Carter et al, 2021 ; Dick and Guglielmo, 2019 ; Price et al, 2022 ).…”

Fat Stores and Antioxidant Capacity Affect Stopover Decisions in Three of Four Species of Migratory Passerines With Different Migration Strategies: An Experimental Approach

“…During short-term captivity, ad lib-fed Blackpoll Warblers and Red-eyed Vireos increased their fat stores and nonenzymatic antioxidant capacity more than individuals of the same species fed at maintenance levels, indicating that food availability on stopover allows individuals to increase nonenzymatic antioxidant capacity. Although the exact mechanism is unknown, it is likely that increased food availability on stopover leads to higher levels of non-enzymatic antioxidant capacity either directly via dietary antioxidants (DeMoranville et al, 2021;McWilliams et al, 2021) or through upregulation of endogenous antioxidants to combat an increase in RS production from lipid peroxidation . These results confirm previous work from Block Island that found fat stores were positively correlated with nonenzymatic antioxidant capacity in free-living Red-eyed Vireos and Blackpoll Warblers (Skrip et al, 2015).…”

Oxidative physiology of two small and highly migratory Arctic seabirds: Arctic terns (Sterna paradisaea) and long-tailed jaegers (Stercorarius longicaudus)

“…However, more data are needed to link oxidative stress to foraging or migration performance. In non-migratory species, flight performance has been linked to oxidative stress ( Costantini, 2008 ; Larcombe et al, 2008 ; Costantini et al, 2013 ; DeMoranville et al, 2022 ), but quantifying oxidative stress during migratory flight is challenging because animals are difficult to access mid-migration unless at a stopover site, especially for species that migrate over oceans. Studies in songbirds at their stopover sites showed increased antioxidants (blackbirds; ( Eikenaar et al, 2017 )), increased oxidative damage (garden warblers; ( Skrip et al, 2015 )) or both increased oxidative damage and antioxidants (European robins ( Jenni-Eiermann et al, 2014 )).…”