Season, anthocyanin supplementation, and flight training have mixed effects on the antioxidant system of migratory European Starlings

Abstract

Migratory birds engage in 2 periods of endurance flight annually as they travel between summer breeding and overwintering grounds, and such endurance flights likely incur oxidative costs. These costs may differ between fall and spring migration, especially for females who must prepare for breeding and egg laying in spring. The objective of this study of a migratory bird was to test proposed hypotheses about how key components of the female’s antioxidant system differ in response to flight training in the fall and spring and to dietary antioxidant supplementation. We hand raised female European Starlings (Sturnus vulgaris) and fed them either a diet supplemented with dietary anthocyanins or a diet without added anthocyanins. We flew females in a wind tunnel for 15 days during fall and spring migration seasons and measured over time oxidative lipid damage (d-ROMs) and 3 components of the antioxidant system: nonenzymatic antioxidant capacity (OXY), uric acid, and glutathione peroxidase (GPx) activity. Prior to flight training, OXY and oxidative damage were lower in females during spring compared with fall, and females fed a low-antioxidant diet had consistently higher circulating uric acid. GPx activity decreased more in spring immediately after a long-duration flight. Females fed a high-antioxidant diet had a greater decrease in OXY after the 15-day flight training. Flight-trained females had higher circulating uric acid than untrained females immediately after the longest-duration flight and decreased GPx activity after the 15-day flight training. In sum, females upregulated enzymatic and nonenzymatic endogenous antioxidants in spring, and females fed a diet with less antioxidants appear to compensate by increasing circulating uric acid. Our findings emphasize the important role of dietary antioxidants for birds during migration, and similar flights in fall and spring likely represent distinct oxidative challenges in the life history of female birds.

How Birds During Migration Maintain (Oxidative) Balance

“…In contrast, flight duration (range: 65-205 min) was not related to d-ROMs levels in Northern Bald Ibis on a managed migration (Geronticus eremita; Bairlein et al, 2015). Similarly, several wind-tunnel studies on starlings (S. vulgaris) that involved weeks of flight training leading to long final flights up to 6 h have not found any change in d-ROMs associated with flight, either within individuals preand post-flight or between individuals that were either flown or not flown (McWilliams et al, 2020;Frawley et al, 2021). In contrast, starlings involved in a similar 2-week wind-tunnel flight training decreased d-ROMs after flight compared to pre-flight indicating a potential hormetic response (DeMoranville, 2020).…”

“…European Starlings also reduced OXY (and oxidative damage, noted above) immediately after flights in a wind tunnel, and the extent of this change was more apparent in birds that expended more energy during their longest flights (DeMoranville, 2020). OXY also changed in European Starlings immediately after flights, although the direction and extent of the change depended on season (fall vs. spring migration) and whether diets were supplemented with antioxidants (Frawley et al, 2021).…”

“…For example, European Robins caught during nocturnal migratory flight had higher GPx activity compared to birds on stopover (Jenni-Eiermann et al, 2014), and Yellow-rumped Warblers flown in a wind tunnel had higher SOD after flight than individuals at rest (Dick and Guglielmo, 2019). The response of enzymatic antioxidants in flight-trained European Starlings to an approximately 3-h flight in a wind tunnel depended on availability of dietary antioxidants (Frawley et al, 2021). Specifically, starlings fed a diet not supplemented with anthocyanin, a dietary antioxidant, had decreased GPx activity immediately after flight, whereas GPx activity did not change after flight for starlings fed a diet supplemented with anthocyanins (Frawley et al, 2021).…”

“…The response of enzymatic antioxidants in flight-trained European Starlings to an approximately 3-h flight in a wind tunnel depended on availability of dietary antioxidants (Frawley et al, 2021). Specifically, starlings fed a diet not supplemented with anthocyanin, a dietary antioxidant, had decreased GPx activity immediately after flight, whereas GPx activity did not change after flight for starlings fed a diet supplemented with anthocyanins (Frawley et al, 2021). Furthermore, Zebra Finches flown for short bursts had similar serum GPx, CAT, and SOD activity after flight compared to unflown control birds (Costantini et al, 2013).…”

“…Uric acid, a byproduct of protein catabolism and a powerful antioxidant, has been found to consistently increase after flight in several field and lab studies. European Starlings flown in wind tunnels had elevated serum uric acid immediately after up to 6 h of flight (Carter et al, 2020;McWilliams et al, 2020;Frawley et al, 2021). Whitecrowned Sparrows (Zonotrichia leucophrys) that were flown at high speeds in a hop/hover wheel (Tsahar et al, 2006) and pigeons flown for 4 h (Gannes et al, 2001) also had increased uric acid concentrations after flight.…”