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

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-[(3)H]-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 O(2)kg(-1) min(-1) to 65.2+/-8.1 ml O(2) kg(-1) min(-1)), almost solely by stimulating lipid oxidation (33.3+/- 3.3 ml O(2) kg(-1) min(-1) to 48.2+/-6.8 ml O(2) kg(-1) min(-1)) because carbohydrate oxidation remains close to 11.5+/- 0.5 ml O(2) kg(-1) min(-1). Sandpipers support an unusually high lipolytic rate of 55-60 micromol 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.