Extremely Low Maximal Force-Generating Ability in Hummingbird Flight Muscle Fibers

Abstract

Hummingbird flight muscle has the highest mass-specific mechanical power output among all vertebrates. The wingbeat kinematics and aerodynamics of hummingbird flight have been studied in multiple species, but little is known about fundamental contractile properties of these remarkable muscles. The objective of this study was to measure the maximal force-generating ability (maximal force per unit of fiber cross-sectional area, Po/CSA) of single muscle fibers from the pectoralis muscle, which powers the wing downstroke, in adult hummingbirds and in another similarly-sized species, zebra finch, which does not hover but also has a very high wingbeat frequency during routine flight. Single, skinned pectoralis fibers were maximally calcium-activated and Po/CSA was measured across a range of temperatures. Po/CSA in hummingbird pectoralis fibers was 1.1 ± 0.4 (mean ± SEM), 5.2 ± 1.6, and 10.8 ± 2.4 kN/m2, at 10, 15, and 20°C, respectively. Po/CSA in zebra finch pectoralis fibers was 2.0 ± 0.4 (mean ± SEM), 10.4 ± 1.6, and 21.6 ± 3.2 kN/m2, at 10, 15, and 20°C, respectively. For comparison, Po/CSA in adult mammalian limb muscle fibers at 15°C is typically 100-120 kN/m2. The mean Po/CSA in hummingbird leg muscles fibers, which are used for perching, was 73.4 ± 11.6 kN/m2 at 10°C. These results indicate that hummingbird pectoralis fibers have an extremely low force-generating ability, compared to mammalian limb muscle fibers and hummingbird leg muscle fibers, even when maximally activated, and have an unusually high temperature-dependence of force generation. The unusually low force-generating ability of hummingbird and zebra finch pectoralis fibers may reflect a constraint imposed by a need for extremely high contraction frequencies, especially during hovering flight in hummingbirds. Supported by the National Science Foundation.