Flight muscle enzymes and metabolic flux rates during hovering flight of the nectar bat, Glossophaga soricina: Further evidence of convergence with hummingbirds

Abstract

Given their high metabolic rates, nectarivorous diet, and ability to directly fuel their energetically-expensive flight using recently-ingested sugar, we tested the hypothesis that Pallas long tongued nectar bats (Glossophaga soricina) possess flight muscles similar to those of hummingbirds with respect to enzymatic flux capacities in bioenergetic pathways. In addition, we compared these biochemical capacities with flux rates achieved in vivo during hovering flight. Rates of oxygen consumption (V̇_O2) were measured during hover-feeding and used to estimate rates of ATP turnover, glucose and long-chain fatty acid oxidation per unit mass of flight muscle. Enzyme V_max values at key steps in glucose and fatty acid oxidation obtained in vitro from pectoralis muscle samples exceed those found in the locomotory muscles of other species of small mammals and resemble data obtained from hummingbird flight muscles. The ability of nectar bats and hummingbirds to hover in fed and fasted states, fueled almost exclusively by carbohydrate or fat, respectively, allowed the estimation of fractional velocities (v/V_max) at both the hexokinase and carnitine palmitoyltransferase-2 steps in glucose and fatty acid oxidation, respectively. The results further support the hypothesis of convergent evolution in biochemical and physiological traits in nectar bats and hummingbirds.

Introduction

Nectarivorous bats have converged with hummingbirds in evolving to be small and in feeding on floral nectar. Pallas long tongued nectar bats (Glossophaga soricina, referred to, henceforth, as “nectar bats”), in particular, are able to engage in energetically expensive hovering flight for up to several seconds while feeding (Voigt and Winter, 1999, Winter et al., 1998, Welch et al., 2008). Recent studies revealed that nectar bats are able to make use of recently-ingested sugars to directly fuel their metabolism (Voigt and Speakman, 2007). This is made possible, at least in part, by their high intestinal capacities for sugar assimilation (Hernández and Martínez del Rio, 1992, Winter, 1998), a physiological trait shared with hummingbirds (McWhorter et al., 2006). Previously, we performed experiments to determine whether nectar bats could, like hummingbirds (Welch et al., 2006, Welch et al., 2007), fuel hover-feeding using recently-ingested sugar. These studies yielded further evidence of their evolutionary convergence with hummingbirds: close to 80% of the energy required for hovering flight in nectar bats is provided by the oxidation of recently-ingested sugar (Welch et al., 2008). This is a remarkable feat for a mammal, given that humans can fuel only about 30% of exercise metabolism (Jentjens et al., 2004), while hummingbirds (Selasphorus rufus and Calypte ana) can fuel virtually all of their hovering metabolism directly using recently ingested sugar (Welch et al., 2007).

We measured the maximum capacities for flux, i.e, V_max values, in vitro at key steps in muscle energy metabolism to gain insights into the biochemical bases for the high rates of sugar oxidation estimated in vivo in hovering nectar bats and to further probe the extent of their convergence with hummingbirds. In addition, rates of glucose and fatty acid oxidation in the flight muscles, estimated from respirometry data, are compared with enzyme V_max values estimated in vitro to gain insights into the relationships between biochemical flux capacities and physiological flux rates during flight.