High Plasma Triglyceride Levels in Small Birds during Migratory Flight: A New Pathway for Fuel Supply during Endurance Locomotion at Very High Mass-Specific Metabolic Rates?

For long migrations, birds must rely on high flux capacities at all steps of lipid metabolism, from the mobilization of adipose reserves to fatty acid oxidation in flight muscle mitochondria. Substrate kinetics and indirect calorimetry were used to investigate key parameters of lipid metabolism in a highly aerobic shorebird: the ruff sandpiper Philomachus pugnax. In this study, we have quantified the effects of cold exposure because such measurements are presently impossible during flight. Lipolytic rate was monitored by continuous infusion of 2-[3H]-glycerol and lipid oxidation by respirometry. Plasma lipid concentrations (non-esterified fatty acids, neutral lipids and phospholipids) and their fatty acid composition were also measured to assess whether cold exposure causes selective metabolism of specific lipids. Results show that shivering leads to a 47% increase in metabolic rate (44.4±3.8 ml O2kg–1min–1 to 65.2±8.1 ml O2kg–1 min–1), almost solely by stimulating lipid oxidation (33.3± 3.3 ml O2 kg–1min–1 to 48.2±6.8 ml O2kg–1 min–1) because carbohydrate oxidation remains close to 11.5± 0.5 ml O2 kg–1min–1. Sandpipers support an unusually high lipolytic rate of 55–60 μmol glycerol kg–1 min–1. Its stimulation above thermoneutral rates is unnecessary during shivering when the birds are still able to re-esterify 50% of released fatty acids. No changes in plasma lipid composition were observed, suggesting that cold exposure does not lead to selective metabolism of particular fatty acids. This study provides the first measurements of lipolytic rate in migrant birds and shows that their capacity for lipid mobilization reaches the highest values measured to date in vertebrates. Extending the limits of conventional lipid metabolism has clearly been necessary to achieve long-distance migrations.

Section: Plasma Lipid Compositionmentioning

confidence: 82%

Lipid mobilization of long-distance migrant birdsin vivo: the high lipolytic rate of ruff sandpipers is not stimulated during shivering

Vaillancourt

Weber

2007

“…In mammals, lipolysis is not thought to limit fatty acid oxidation during exercise , and the very high lipolysis rates of birds suggest that this may also be true for birds. Changes in plasma albumin concentration are unlikely to be important for enhancing fatty acid transport because excess albumin would be detrimental to blood viscosity and fluid homeostasis (Jenni-Eiermann and Jenni, 1992). Migrating songbirds captured in mid-flight were found to have elevated plasma triacylglycerol and very low-density lipoproteins (VLDL) compared with fasted or fed birds Jenni, 1991, 1992), leading to the hypothesis that some fatty acids mobilized from adipocytes during flight may be cleared from the plasma by the liver, re-esterified to triacylglycerol (and possibly phospholipids), and packaged into VLDL for re-release to the circulation (JenniEiermann and Jenni, 1992).…”

Section: Meeting the Challenge Of Fat-fueled Flightmentioning

confidence: 99%

“…Once reaching the muscle capillaries, triacylglycerol would be hydrolyzed by lipoprotein lipase, releasing NEFA in high local concentrations for uptake by myocytes (Ramenofsky, 1990). This could increase overall fatty acid flux by keeping the availability of albumin binding sites high and creating an alternative pathway for the delivery of fatty acids to muscle by lipoproteins (Jenni-Eiermann and Jenni, 1992). Further support for the lipoprotein hypothesis was found in bar-tailed godwits (Limosa lapponica taymyrensis) that had greater plasma triacylglycerol concentrations immediately after arrival from a long migratory flight than after five hours of inactivity (Landys et al, 2005).…”

Section: Meeting the Challenge Of Fat-fueled Flightmentioning

confidence: 99%

Obese super athletes: fat-fueled migration in birds and bats

Guglielmo

2018

127

112

Migratory birds are physiologically specialized to accumulate massive fat stores (up to 50-60% of body mass), and to transport and oxidize fatty acids at very high rates to sustain flight for many hours or days. Target gene, protein and enzyme analyses and recent -omic studies of bird flight muscles confirm that high capacities for fatty acid uptake, cytosolic transport, and oxidation are consistent features that make fat-fueled migration possible. Augmented circulatory transport by lipoproteins is suggested by field data but has not been experimentally verified. Migratory bats have high aerobic capacity and fatty acid oxidation potential; however, endurance flight fueled by adipose-stored fat has not been demonstrated. Patterns of fattening and expression of muscle fatty acid transporters are inconsistent, and bats may partially fuel migratory flight with ingested nutrients. Changes in energy intake, digestive capacity, liver lipid metabolism and body temperature regulation may contribute to migratory fattening. Although control of appetite is similar in birds and mammals, neuroendocrine mechanisms regulating seasonal changes in fuel store set-points in migrants remain poorly understood. Triacylglycerol of birds and bats contains mostly 16 and 18 carbon fatty acids with variable amounts of 18:2n-6 and 18:3n-3 depending on diet. Unsaturation of fat converges near 70% during migration, and unsaturated fatty acids are preferentially mobilized and oxidized, making them good fuel. Twenty and 22 carbon n-3 and n-6 polyunsaturated fatty acids (PUFA) may affect membrane function and peroxisome proliferator-activated receptor signaling. However, evidence for dietary PUFA as doping agents in migratory birds is equivocal and requires further study.

“…Few studies have documented how concentrations of plasma metabolites change in a migratory songbird following intense exercise (Jenni-Eiermann and Jenni, 1991, 1992). Plasma metabolite changes in a migratory songbird are most commonly studied by comparisons of free-living birds captured at night during their annual migration (post-exercise) and freeliving birds captured and maintained overnight (at rest).…”

Section: Fuel Use During Exercisementioning

confidence: 99%

Effect of dietary fatty acid composition on depot fat and exercise performance in a migrating songbird, the red-eyed vireo

Pierce

McWilliams

O’Connor

et al. 2005

105

SUMMARY Most migrating birds accumulate lipid stores as their primary source of energy for fueling long distance flights. Lipid stores of birds during migration are composed of mostly unsaturated fatty acids; whether such a fatty acid composition enhances exercise performance of birds is unknown. We tested this hypothesis by measuring metabolic rate at rest and during intense exercise in two groups of red-eyed vireos, a long-distance migratory passerine, fed either a diet containing 82% unsaturated fat (82%U), or one containing 58% unsaturated fat (58%U). Vireos fed the 82%U diet had fat stores containing (77%) unsaturated fatty acids, whereas vireos fed the 58% U diet had fat stores containing less (66%) unsaturated fatty acids. Blood metabolites measured prior to and immediately following exercise confirmed that vireos were metabolizing endogenous fat during intense exercise. Mass-specific resting metabolic rate (RMR) was similar for vireos fed the 58%U diet (2.75±0.32 ml O2 g–1h–1) and for vireos fed the 82%U diet (2.30±0.30 ml O2 g–1 h–1). However,mass-specific peak metabolic rate (MRpeak) was 25% higher in vireos fed the 58%U diet (28.55±1.47 ml O2 g–1h–1) than in vireos fed the 82%U diet (21.50±1.76 ml O2 g–1 h–1). Such whole-animal energetic effects of fatty acid composition of birds suggest that the energetic cost of migration in birds may be affected by the fatty acid composition of the diet.