Hummingbirds rely on both paracellular and carrier-mediated intestinal glucose absorption to fuel high metabolism

Abstract

Twenty years ago, the highest active glucose transport rate and lowest passive glucose permeability in vertebrates were reported in Rufous and Anna's hummingbirds (Selasphorus rufus, Calypte anna). These first measurements of intestinal nutrient absorption in nectarivores provided an unprecedented physiological foundation for understanding their foraging ecology. They showed that physiological processes are determinants of feeding behaviour. The conclusion that active, mediated transport accounts for essentially all glucose absorption in hummingbirds influenced two decades of subsequent research on the digestive physiology and nutritional ecology of nectarivores. Here, we report new findings demonstrating that the passive permeability of hummingbird intestines to glucose is much higher than previously reported, suggesting that not all sugar uptake is mediated. Even while possessing the highest active glucose transport rates measured in vertebrates, hummingbirds must rely partially on passive non-mediated intestinal nutrient absorption to meet their high mass-specific metabolic demands.

Figure 1

Fractional absorption, or bioavailability, of radio-labelled l-glucose in hummingbirds was significantly correlated with the ratio of the blood plasma label concentration (P) to label ingestion rate (I), an observation expected from pharmacokinetic models of absorption that allows one to infer the effect of diet treatment on l-glucose fractional absorption. Absorption of this non-transported glucose stereoisomer is an indicator of the passive (non-mediated) permeability of the gut to glucose.

Figure 2

(a) Radio-labelled l-glucose ingestion rate was significantly greater when broad-tailed hummingbirds were feeding on the more energy-dilute 292 mM sucrose diet. This is expected, because food intake rate is inversely correlated with energy density in many vertebrates. (b) There was a relatively high concentration of radio-labelled l-glucose in the blood plasma of hummingbirds feeding at steady state, indicating absorption. Plasma label concentration did not differ significantly between birds feeding on the 292 and 876 mM sucrose diets. (c) The ratio of blood plasma label concentration (P) to label ingestion rate (I), and hence l-glucose fractional absorption, increased in stepwise fashion with diet sucrose concentration when data from both experiments were combined. This suggests that fractional absorption of l-glucose is correlated with the retention time of digesta in the gut. Error bars indicate ±1 s.e.m. Letters above error bars indicate statistically significant differences.