Season, anthocyanin supplementation, and flight training have mixed effects on the antioxidant system of migratory European starlings (Sturnus vulgaris)

Migratory birds engage in two 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 then fed them either a diet supplemented with dietary anthocyanins or a diet without added anthocyanins. We then flew females in a windtunnel for 15 days during fall and spring migration seasons and measured over time oxidative damage (d-ROMs) and three components of the antioxidant system—non-enzymatic antioxidant capacity (OXY), uric acid, and glutathione peroxidase (GPx) activity. Prior to flight training, non-enzymatic antioxidant capacity and oxidative damage were lower in females during spring compared to 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 non-enzymatic antioxidant capacity 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 non-enzymatic 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 that similar flights in fall and spring likely represent distinct oxidative challenges in the life history of female birds.

候鸟每年会经历两段长距离持续飞行周期，往返于夏季繁殖地与越冬地之间，而这类长距离持续飞行很可能会产生氧化应激代价。这类氧化应激代价在秋季与春季迁徙期间可能存在差异，尤其对于需要在春季筹备繁殖与产卵的雌性个体而言。本研究以一种候鸟为研究对象，旨在验证相关假说：即雌性个体的抗氧化系统核心组分，在应对秋季与春季的飞行训练以及膳食抗氧化补充时，会产生怎样的差异变化。我们人工手养了雌性欧洲椋鸟（Sturnus vulgaris），随后将其分为两组，分别饲喂添加了花青素（anthocyanins）的膳食与未添加花青素的基础膳食。随后在秋季与春季迁徙季期间，让雌性椋鸟在风洞（windtunnel）环境中接受为期15天的飞行训练，并在训练周期内定期检测两项指标：氧化损伤（oxidative damage）水平（d-ROMs）以及抗氧化系统的三个核心组分——非酶抗氧化能力（non-enzymatic antioxidant capacity, OXY）、尿酸水平与谷胱甘肽过氧化物酶（glutathione peroxidase, GPx）活性。飞行训练前，春季组雌性个体的非酶抗氧化能力与氧化损伤水平均低于秋季组；而饲喂低抗氧化膳食的个体，其循环尿酸水平始终处于较高水平。在单次长时间飞行结束后即刻检测时，春季组雌性个体的谷胱甘肽过氧化物酶活性下降幅度更大。经过15天的系统性飞行训练后，饲喂高抗氧化膳食的雌性个体，其非酶抗氧化能力的下降幅度更为显著。在单次最长时长的飞行结束后即刻，接受飞行训练的雌性个体循环尿酸水平高于未接受训练的个体；且经过15天飞行训练后，其谷胱甘肽过氧化物酶活性出现明显下降。综上，雌性个体在春季会上调内源性酶促与非酶促抗氧化系统的活性；而饲喂低抗氧化膳食的个体，似乎可通过提升循环尿酸水平来代偿氧化应激压力。本研究结果凸显了膳食抗氧化剂在候鸟迁徙过程中的重要作用，同时表明秋季与春季的同类飞行，对雌性鸟类的生活史而言，代表着截然不同的氧化应激挑战。