The role of the antioxidant system during intense endurance exercise: lessons from migrating birds

Abstract

During migration, birds substantially increase their metabolic rate and burn fats as fuel and yet somehow avoid succumbing to overwhelming oxidative damage. The physiological means by which vertebrates such as migrating birds can counteract an increased production of reactive species (RS) are rather limited: they can upregulate their endogenous antioxidant system and/or consume dietary antioxidants ( prophylactically or therapeutically). Thus, birds can alter different components of their antioxidant system to respond to the demands of long-duration flights, but much remains to be discovered about the complexities of RS production and antioxidant protection throughout migration. Here, we use bird migration as an example to discuss how RS are produced during endurance exercise and how the complex antioxidant system can protect against cellular damage caused by RS. Understanding how a bird's antioxidant system responds during migration can lend insights into how antioxidants protect birds during other life-history stages when metabolic rate may be high, and how antioxidants protect other vertebrates from oxidative damage during endurance exercise.

The effects of dietary linoleic acid and hydrophilic antioxidants on basal, peak, and sustained metabolism in flight‐trained European starlings

“…The accumulation of oxidative damage from the byproducts of aerobic metabolism is expected to reduce whole‐animal performance either directly, through reduced cellular and organismal function (Eikenaar, Isaksson, & Hegemann, ), or indirectly, as resources are directed to endogenous antioxidant responses rather than oxidative capacity (Cooper‐Mullin & McWilliams, ; Larcombe, Herborn, Alexander, & Arnold, ). The potential for reduced performance is particularly high for individuals with high tissue PUFA concentrations, due to elevated risk of peroxidation (Hulbert, ; Skrip & McWilliams, ).…”

“…This negative result could be the product of a low accumulation of oxidative damage from flight training and/or the high‐PUFA diet as was found in a previous wind tunnel study (Dick & Guglielmo, ), although the variance in PUFA content of the diets in that study was much smaller. It is also possible that the hydrophilic antioxidants used to supplement the diets simply did not remain in circulation at high enough concentrations to prophylactically counter oxidative damage and failed to support recovery from oxidative damage (Beaulieu & Schaefer, ; Cooper‐Mullin & McWilliams, ). One other speculative explanation is that endogenous antioxidants such as uric acid (Alan & McWilliams, ; Machin, Simoyi, Blemings, & Klandorf, ) could be preferentially used to counter high RS production.…”

“…Functionally, dietary antioxidants act to reduce oxidative damage (Beaulieu & Schaefer, ; Catoni, Peters, & Schaefer, ; Skrip & McWilliams, ), as well as influence immune function (Catoni, Schaefer, & Peters, ; Marri & Richner, ), investment in reproduction (Royle, Surai, & Hartley, ; Skrip, Seeram, Yuan, Ma, & McWilliams, ), reproductive hormones and behavior (Carbeck et al, ), and ability to meet the oxidative costs of flight (Larcombe et al, ; Skrip et al, ). However, as with fatty acids, results have differed among studies that used different measures of performance and that supplemented diets with different antioxidants, with hydrophilic antioxidants being largely untested (Cooper‐Mullin & McWilliams, ).…”

“…We experimentally tested how dietary linoleic acid (18:2n6), a leading candidate to mediate the effects of dietary fatty acid composition on metabolism in songbirds (Pierce & McWilliams, ; Pierce et al, ; Price & Guglielmo, ; Price et al, ), and the dietary anthocyanins, hydrophilic antioxidants common in the diets of wild songbirds (Bolser et al, ; Cooper‐Mullin & McWilliams, ), interact to affect exercise performance of European starlings ( Sturnus vulgaris ). We measured performance in terms of metabolic rates and tissue catabolism during sustained flight in a wind tunnel to allow us to assess the effect of diet on basal, peak, and sustained metabolism as well as the relationship between these measures.…”

Primary dermal fibroblasts and pectoralis muscle show similar patterns of oxidative stress in tropical and temperate birds despite differing life‐histories

“…However, in Jimenez et al (2013), we have previously found that primary fibroblasts from tropical birds cell lines are more resistant to damage chemically ensued by cadmium, H 2 O 2 , paraquat, tunicamycin and methane methylsulfonate compared with temperate bird cell lines. It is known that during times of stress, such as migration, birds can upregulate aspects of their antioxidant system to compensate for the increase in oxidative stressors (Cooper-Mullin and McWilliams 2016). It is known that during times of stress, such as migration, birds can upregulate aspects of their antioxidant system to compensate for the increase in oxidative stressors (Cooper-Mullin and McWilliams 2016).…”