Fuel metabolism in Canada geese: effects of glucagon on glucose kinetics

Abstract

During prolonged fasting, birds must rely on glucose mobilization to maintain normoglycemia. Glucagon is known to modulate avian energy metabolism during prolonged fasting, but the metabolic effects of this hormone on long-distance migrant birds have never been investigated. Our goal was to determine whether glucagon regulates the mobilization of the main lipid and carbohydrate fuels in migrant birds. Using the Canada goose (Branta canadensis) as a model species, we looked for evidence of fuel mobilization via changes in metabolite concentrations. No changes could be found for any lipid fraction, but glucagon elicited a strong increase in glucose concentration. Therefore, we aimed to quantify the effects of this hormone on glucose kinetics using continuous infusion of 6-[(3)H]-d-glucose. Glucagon was found to cause a 50% increase in glucose mobilization (from 22.2 ± 2.4 μmol·kg(-1)·min(-1) to 33.5 ± 3.3 μmol·kg(-1)·min(-1)) and, together with an unchanged rate of carbohydrate oxidation, led to a 90% increase in plasma glucose concentration. This hormone also led to a twofold increase in plasma lactate concentration. No changes in plasma lipid concentration or composition were observed. This study is the first to demonstrate how glucagon modulates glucose kinetics in a long-distance migrant bird and to quantify its rates of glucose mobilization.

Keywords: Branta canadensis; hepatic glucose production; in vivo tracer infusion; indirect calorimetry; metabolic substrates.

Fig. 1.

Plasma nonesterified fatty acid (A), phospholipid (A), triacylglycerol (A), glycerol (B), glucose (B), and lactate (B) concentration in adult Canada geese before, during, and after glucagon infusion. *Significant difference from baseline (P < 0.05). **Significant difference from baseline (P < 0.01). ***Significant difference from baseline (P < 0.001). Values are expressed as means ± SE (n = 5).

Fig. 2.

Rates of oxygen consumption (Ṁ_O2) (A), carbon dioxide production (Ṁ_CO2) (B), and respiratory exchange ratio (RER) (C) of adult Canada geese before, during, and after glucagon infusion. *Significantly different from baseline (P < 0.05). Values are expressed as means ± SE (n = 5).

Fig. 3.

Rates (A) and relative contribution to Ṁ_O2 (B) of lipid and carbohydrate oxidation (CHO) in adult Canada geese before, during, and after glucagon infusion. Values are expressed as means ± SE (n = 5).

Fig. 4.

Plasma glucose specific activity (A) and rate of mobilization (B) in adult Canada geese before, during, and after glucagon infusion. Note that, at steady state, glucose mobilization is synonymous with glucose flux, glucose turnover rate (R_t), hepatic glucose production, and rate of appearance (R_a) of glucose. ***Significant differences from baseline (P < 0.001). Values are expressed as means ± SE (n = 5).

Fig. 5.

Relative contribution of glucose to total energy expenditure (A) and carbohydrate oxidation (B) of adult Canada geese before, during, and after glucagon infusion, assuming 100% (▲) or 50% (○) of the glucose undergoing turnover is oxidized. *Significant difference from baseline (P < 0.05). ***Significant difference from baseline (P < 0.001). Values are expressed as means ± SE (n = 5).