Flight muscle protein damage during endurance flight is related to energy expenditure but not dietary polyunsaturated fatty acids in a migratory bird

Abstract

Migration poses many physiological challenges for birds, including sustaining high intensity aerobic exercise for hours or days. A consequence of endurance flight is the production of reactive oxygen species (ROS). ROS production may be influenced by dietary polyunsaturated fatty acids (PUFA), which, although prone to oxidative damage, may limit mitochondrial ROS production and increase antioxidant capacity. We examined how flight muscles manage oxidative stress during flight, and whether dietary long-chain PUFA influence ROS management or damage. Yellow-rumped warblers were fed diets low in PUFA, or high in long-chain n-3 or n-6 PUFA. Flight muscle was sampled from birds in each diet treatment at rest or immediately after flying for up to a maximum of 360 min in a wind tunnel. Flight increased flight muscle superoxide dismutase activity but had no effect on catalase activity. The ratio of glutathione to glutathione disulphide decreased during flight. Oxidative protein damage, indicated by protein carbonyls, increased with flight duration (Pearson r=0.4). Further examination of just individuals that flew for 360 min (N=15) indicates that oxidative damage was related more to total energy expenditure (Pearson r=0.86) than to flight duration itself. This suggests that high quality individuals with higher flight efficiency have not only lower energy costs but also potentially less oxidative damage to repair after arrival at the destination. No significant effects of dietary long-chain PUFA were observed on antioxidants or damage. Overall, flight results in oxidative stress and the degree of damage is likely driven more by energy costs than fatty acid nutrition.

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

“…In contrast to these predictions, we found no influence of dietary antioxidants on any of our measures of whole‐animal performance. 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, ).…”

Migrant blackbirds, Turdus merula, have higher plasma levels of polyunsaturated fatty acids compared to residents, but not enhanced fatty acid unsaturation index

“…Paradoxically, the molecular structure linked to exercise enhancement, PUFAs’ multiple double bonds, also makes them prone to peroxidation by the ROS, increasing the risk of oxidative stress (Hulbert, Pamplona, Buffenstein, & Buttemer, 2007). Migratory white‐throated sparrows ( Z. albicollis ) fed with PUFAs (both α‐linolenic and linoleic acid) showed an increase in oxidative damage (Alan & McWilliams, 2013) and similar results have been found also in other species (Labbe, Trick, & Bearerogers, 1991; Sies, Stahl, & Sevanian, 2005, but see also; Andersson et al., 2018; Dick & Guglielmo, 2019b). Comparable to the dietary preference for unsaturated FAs, birds may also consume more fruits with high antioxidant levels at stopover sites during migration (Bolser et al., 2013).…”

“…Possibly an experimental increase in PUFAs makes it difficult to retain the unsaturation level, hence the increase in damages. Another study reported no effects of ω‐3 or ω‐6 PUFA‐rich diets on oxidative damages to proteins in flight muscles at rest and after endurance flight in yellow‐rumped warblers (Dick & Guglielmo, 2019b). Although lipid peroxidation was not measured, the lack of increased protein damage suggests that PUFA diet did not increase oxidative stress overall.…”

Understanding how birds rebuild fat stores during migration: insights from an experimental study

“…These data indicate that upregulation of aerobic capacity is not diet-controlled, or that n-3 and n-6 PUFA can show a similar or no effect. Furthermore, yellow-rumped warblers Setophaga coronate supplemented with n-3 PUFA showed no effect of PUFA on their flight performance, contradicting the natural doping hypothesis 17,18 . Overall, some studies did not support the natural doping hypothesis, or the PUFA benefits on migratory performance 12,17,18 .…”