The oxidative debt of fasting: evidence for short to medium-term costs of advanced fasting in adult king penguins

In response to prolonged periods of fasting, animals have evolved metabolic adaptations helping to mobilize body reserves and/or reducing metabolic rate, to ensure a longer usage of reserves. Those metabolic changes can however be associated with higher exposure to oxidative stress, raising the question how species that naturally fast during their life cycle avoid an accumulation of oxidative damage over time. King penguins repeatedly cope with fasting periods up to several weeks. Here we investigated how adult male penguins deal with oxidative stress after an experimentally induced moderate fasting period (PII) or an advanced fasting period (PIII). After fasting in captivity, birds were released to forage at sea. We measured plasmatic oxidative stress on the same individuals at the start and end of the fasting period and when they returned from foraging at sea. We found an increase in activity of the antioxidant enzyme superoxide dismutase along with fasting. However, PIII individuals showed higher oxidative damage at the end of the fast compared to PII individuals. When they returned from re-feeding at sea, all birds had recovered their initial body mass and exhibited low levels of oxidative damage. Notably, levels of oxidative damage after the foraging trip were correlated to the rate of mass gain at sea in PIII individuals but not in PII individuals. Altogether, our results suggest that fasting induces a transitory exposure to oxidative stress and that effort to recover in body mass after an advanced fasting period may be a neglected carry-over cost of fasting.