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

Abstract

In response to prolonged periods of fasting, animals have evolved metabolic adaptations helping to mobilize body reserves and/or reduce metabolic rate to ensure a longer usage of reserves. However, those metabolic changes can be associated with higher exposure to oxidative stress, raising the question of how species that naturally fast during their life cycle avoid an accumulation of oxidative damage over time. King penguins repeatedly cope with fasting periods of 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 with 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 carryover cost of fasting.

Decreased mitochondrial metabolic requirements in fasting animals carry an oxidative cost

“…However, mitochondria are also a major source of reactive oxygen species (ROS) that have the potential to cause oxidative damage (Brand, ). Temporary reductions in mitochondrial energy requirements, while providing short‐term energetic benefits, could potentially lead to associated increases in ROS levels, resulting in the long‐term costs of oxidative stress (Schull et al., ; Sorensen et al., ), potentially faster organismal senescence and hence constraints on future life history (Dowling & Simmons, ; Midwood, Larsen, Aarestrup, & Cooke, ; Monaghan, Metcalfe, & Torres, ; Selman, Blount, Nussey, & Speakman, ; Speakman et al., ). However, surprisingly little is known about these interactions as studies of mitochondrial energetics are generally conducted separately from those of ROS production (Sorensen et al., ; Zhang, Wu, & Klaassen, ; but see Brown & Staples, ; Chausse et al., ).…”

Using whole-group metabolic rate and behaviour to assess the energetics of courtship in red-sided garter snakes

“…Likewise, the evolution of femaleemale sex roles, the coincident sex differences in longevity and the strength of sexual selection are attributed to differential allocation of energy beginning with gamete production and continuing through parental care (Barrett & Richardson, 2011;Bateman, 1948;Parker, 2014;Trivers, 1972). The challenges of courtship and direct maleemale competition may require significant energetic expenditure and optimized performance, both of which have implications for reproductive fitness (Clark, 2012;Lailvaux & Irschick, 2006;Ryan, 1988). To minimize these physiological costs and maximize fitness, males are expected to fine-tune courtship and competition effort relative to the potential for fitness payoffs (Barske, Schlinger, & Fusani, 2015;Byrne, 2008;Kahn, Dolstra, Jennions, & Backwell, 2013;deCarvalho, Watson, & Field, 2004).…”

Breeding phased dependent oxidative balance in a small High Arctic seabird, the little auk

“…OS level is lower and/or ROMs is mitigated by the anti-oxidant barrier (van Noordwijk and de Jong 1986). In penguins, OS level in birds returning from the feeding areas is lower than before foraging trip (Schull et al 2016), suggesting a body resources restoration of the breeding adults during the foraging trips. Little auks also seem to restore their body reserves during the foraging trips during the chick rearing period (Welcker et al 2012).…”