The energy savings-oxidative cost trade-off for migratory birds during endurance flight

Scott Mcwilliams,Sophia Engel,Lisa Trost,Andrea Wittenzellner,Amadeusz Bryla,Edyta Sadowska,John R Speakman,Olivia Fatica,Kristen Demoranville,Ulf Bauchinger,Wolfgang Goymann,Lillie Langlois,Barbara Pierce,Maciej Dzialo

doi:10.7554/elife.60626

Abstract

Elite human and animal athletes must acquire the fuels necessary for extreme feats, but also contend with the oxidative damage associated with peak metabolic performance. Here, we show that a migratory bird with fuel stores composed of more omega-6 polyunsaturated fats (PUFA) expended 11% less energy during long-duration (6 hr) flights with no change in oxidative costs; however, this short-term energy savings came at the long-term cost of higher oxidative damage in the omega-6 PUFA-fed birds. Given that fatty acids are primary fuels, key signaling molecules, the building blocks of cell membranes, and that oxidative damage has long-term consequences for health and ageing, the energy savings-oxidative cost trade-off demonstrated here may be fundamentally important for a wide diversity of organisms on earth.

Highlights

Endurance exercise challenges the physiology of athletes because high metabolism must be fueled and sustained while avoiding the build-up of metabolites that cause oxidative stress and fatigue
We took advantage of this feature of fat metabolism and used diet manipulations to produce European starlings (Sturnus vulgaris) with distinct differences in certain essential fatty acids (Figure 1). Such differences in fatty acid composition of fat stores in starlings, the relative amounts of 18:1, 18:2, and 18:3, are among the primary longer chain fatty acids that compose the fat stores of wild songbirds especially during migration (Blem, 1990; Pierce and McWilliams, 2005; Pierce and McWilliams, 2014). We used these two groups of starlings with different fatty acid composition of their fat stores to directly test the hypothesis that birds with more essential omega-6 and À3 polyunsaturated fats (PUFA) (18:2 and 18:3) comprising their fat depot have enhanced exercise performance during long-duration flights, as previously shown for short-duration flights of a few minutes
After 15 days of ramping up flight-training, we flew starlings (n = 33) for 6 hr (±5 min) in a windtunnel set at a fixed speed of 12–12.5 m/s, the equivalent of a ca. 260 km non-stop flight, and used doubly labeled water to measure energy expended during the 6 hr flight

Summary

Introduction

Endurance exercise challenges the physiology of athletes because high metabolism must be fueled and sustained while avoiding the build-up of metabolites that cause oxidative stress and fatigue. Birds use fats as their primary fuel (about 95%) for high-intensity endurance exercise such as migratory flights (Jenni and Jenni-Eiermann, 1998; Guglielmo, 2010; Guglielmo, 2018), and these fats are highly susceptible to oxidative damage (Skrip and McWilliams, 2016). Biochemistry and Chemical Biology Ecology few essential fatty acids, can reduce the energy cost of endurance flight; such beneficial energy savings comes at the cost of longer term oxidative damage. This energy savings-oxidative cost trade-off has important implications for the ecology and physiology of birds, as well as potentially for other, non-avian, athletes

Results and discussion

Materials and methods

Funding Funder National Science Foundation