Migrating songbirds on stopover prepare for, and recover from, oxidative challenges posed by long‐distance flight

Abstract

Managing oxidative stress is an important physiological function for all aerobic organisms, particularly during periods of prolonged high metabolic activity, such as long-distance migration across ecological barriers. However, no previous study has investigated the oxidative status of birds at different stages of migration and whether that oxidative status depends on the condition of the birds. In this study, we compared (1) energy stores and circulating oxidative status measures in (a) two species of Neotropical migrants with differing migration strategies that were sampled at an autumn stopover site before an ecological barrier; and (b) a species of trans-Saharan migrant sampled at a spring stopover site after crossing an ecological barrier; and (2) circulating oxidative measures and indicators of fat metabolism in a trans-Saharan migrant after stopovers of varying duration (0–8 nights), based on recapture records. We found fat stores to be positively correlated with circulating antioxidant capacity in Blackpoll Warblers and Red-eyed Vireos preparing for fall migration on Block Island, USA, but uncorrelated in Garden Warblers on the island of Ponza, Italy, after a spring crossing of the Sahara Desert and Mediterranean Sea. In all circumstances, fat stores were positively correlated with circulating lipid oxidation levels. Among Garden Warblers on the island of Ponza, fat anabolism increased with stopover duration while oxidative damage levels decreased. Our study provides evidence that birds build antioxidant capacity as they build fat stores at stopover sites before long flights, but does not support the idea that antioxidant stores remain elevated in birds with high fuel levels after an ecological barrier. Our results further suggest that lipid oxidation may be an inescapable hazard of using fats as the primary fuel for flight. Yet, we also show that birds on stopover are capable of recovering from the oxidative damage they have accrued during migration, as lipid oxidation levels decrease with time on stopover. Thus, the physiological strategy of migrating songbirds may be to build prophylactic antioxidant capacity in concert with fuel stores at stopover sites before a long-distance flight, and then repair oxidative damage while refueling at stopover sites after long-distance flight.

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

“…Eiermann et al, 2014). Levels of hydroperoxides -indicators of oxidative damage caused by peroxidation of lipids, proteins and DNA -were 54% higher in the plasma of homing pigeons (Columba livia) after flights of 60-200 km and were higher in plasma from garden warblers (Sylvia borin) newly arrived at stopover sites than in those that had rested for up to 8 h (Skrip et al, 2015). Overall, these studies indicate that migratory flights cause oxidative damage to the cells and tissues of birds (Table 1).…”

“…Far fewer studies in ecology have examined how short-term increases in metabolic rate (such as those observed during exercise) change RS production within an individual. The metabolic rate of birds is high during migratory flights (Bishop and Butler, 2015;Hedenström et al, 2009), which could lead to an increase in RS production and an increase in damage to cells and tissues Jenni-Eiermann et al, 2014;Skrip et al, 2015).…”

“…Most mammals primarily use carbohydrates as fuel during exercise, whereas birds primarily burn fats to fuel flight, and this reliance on fatty acid oxidation results in relatively lower RS production in exercising birds than in mammals (Kuzmiak et al, 2012;Montgomery et al, 2012;Weber, 2009). Although burning fat may result in lower RS production in muscle mitochondria, stored fat is highly susceptible to lipid peroxidation, and, during migration, birds must build and store large amounts of fat (Costantini, 2014;Costantini et al, 2007;Pierce and McWilliams, 2014;Skrip et al, 2015). Thus, the amount of RS produced during exercise may be different if measured in a bird as opposed to a non-flying mammal, and birds may be more susceptible to RS damage via lipid peroxidation of stored fats.…”

“…2) that work synergistically to protect against oxidative damage Costantini, 2008;Costantini et al, 2007Costantini et al, , 2011Jenni-Eiermann et al, 2014;. For birds in migration, the relationship between RS production, antioxidant protection and oxidative damage is not straightforward, and various aspects of the antioxidant system may respond differently depending on the type of damage, the duration of flight or the physiological state of the bird (Cohen and McGraw, 2009;Costantini et al, 2007;Jenni-Eiermann et al, 2014;Skrip et al, 2015).…”

“…Instead, most studies examine the damage caused by RS (e.g. products of lipid peroxidation or protein oxidation) and probe various aspects of the antioxidant system (Abuja and Albertini, 2001;Costantini, 2014;Costantini et al, 2007;Dalle-Donne et al, 2003;Jenni-Eiermann et al, 2014;Prior and Cao, 1999;Skrip et al, 2015). Interpreting oxidative damage and antioxidant capacity without direct measures of RS production can be complicated, because if antioxidant levels are adequately high, they may limit damage even when RS production is high ( Fig.…”