Oxidative Challenges of Avian Migration: A Comparative Field Study on a Partial Migrant

Abstract

Most avian migrants alternate flight bouts, characterized by high metabolic rates, with stopovers, periods of fuel replenishment through hyperphagia. High-energy metabolism and excessive calorie intake shift the balance between damaging prooxidants and antioxidants toward the former. Hence, migration likely affects the oxidative balance of birds. Migratory flight indeed appears to cause oxidative damage; however, whether migration affects the oxidative state of birds at stopover is unclear. Therefore, we compared total nonenzymatic antioxidant capacity (AOX) and malondialdehyde concentration (MDA; a measure of lipid peroxidation) in the plasma of migrant and resident common blackbirds. We also determined plasmatic uric acid (UA) and fatty acid (FA) concentrations and calculated a FA peroxidation index. Birds were sampled during autumn migration at a stopover site that also supports a sedentary blackbird population. Migrants had higher AOX than residents, also after correcting for UA concentration. Migrants tended to have higher FA peroxidation indexes than residents, indicating that the energy source of migrants contains higher concentrations of peroxidizable FAs. However, the two groups did not differ in MDA concentration, also not after correcting for peroxidation index. Peroxidation-corrected MDA concentration was negatively correlated with UA-corrected AOX. In other words, individuals with low nonenzymatic AOX suffered more from lipid peroxidation than individuals with high nonenzymatic AOX. These results together indicate that migrant blackbirds invest in antioxidant defenses to reduce oxidative damage to lipids, likely representing an adaptation to diminish the physiological costs of migration.

A hidden cost of migration? Innate immune function versus antioxidant defense

“…Ten newly caught birds that were resighted only within 19 days of color‐ringing (range: 1–11 days) have most likely been migrants. Yet, to reduce the possibility of misassignment in status and to make our assignment as conservative as possible, we excluded these birds from this study (after Eikenaar et al., ). The fact that immigration and emigration rates in the Helgoland blackbird breeding population are very low (Sacher, ), increases the likelihood of accurate assignment of status.…”

“…MDA concentration was measured after Eikenaar et al. () by coupled gas chromatography and electron ionization mass spectrometry (GC/EI/MS) analysis after derivatization with O‐(2,3,4,5,6‐pentafluorbenzyl) hydroxylamine hydrochloride (PFBHA·HCl). BKA (against Escherichia coli ) was determined following the method described by French and Neuman‐Lee () with a few modifications (see Eikenaar & Hegemann, ).…”

“…The study of Eikenaar and Hegemann () thus supports the hypothesis that birds may be forced to compromise immune function during physiologically demanding migrations (Buehler & Piersma, ). Interestingly, in the same blackbird study system, migrating individuals had higher nonenzymatic antioxidant capacities than sedentary individuals, that is migrants produce or ingest more antioxidants, suggesting that they boost their antioxidants to counteract the increased pro‐oxidant exposure (Eikenaar, Källstig, Andersson, Herrera‐Dueñas, & Isaksson, ). The antioxidant defenses were then highly efficient as migrating and sedentary individuals did not differ in oxidative damage to lipids (Eikenaar et al., ).…”

“…Interestingly, in the same blackbird study system, migrating individuals had higher nonenzymatic antioxidant capacities than sedentary individuals, that is migrants produce or ingest more antioxidants, suggesting that they boost their antioxidants to counteract the increased pro‐oxidant exposure (Eikenaar, Källstig, Andersson, Herrera‐Dueñas, & Isaksson, ). The antioxidant defenses were then highly efficient as migrating and sedentary individuals did not differ in oxidative damage to lipids (Eikenaar et al., ). Together, these data suggest that due to elevated energetic and physiological demands, migrants may trade off investment in baseline innate immune function against investment in antioxidant defense.…”

Species-Dependent Effects of the Urban Environment on Fatty Acid Composition and Oxidative Stress in Birds

“…The direction of this association in tree sparrows is in contrast to our prediction, and also to the results at the population level (where both MDA and PI were higher in the urban compared to the rural environment). Possibly, individual tree sparrows with a high PI have a corresponding increase in dietary antioxidants (Eikenaar et al, 2016(Eikenaar et al, , 2017. This could prevent lipid peroxidation to some degree, but not enough to override the population/habitat effect.…”