Abstract
The axial musculature of fishes has historically been characterized as the powerhouse for explosive swimming behaviors. However, recent studies show that some fish also use their ‘swimming’ muscles to generate over 90% of the power for suction feeding. Can the axial musculature achieve high power output for these two mechanically distinct behaviors? Muscle power output is enhanced when all of the fibers within a muscle shorten at optimal velocity. Yet, axial locomotion produces a mediolateral gradient of muscle strain that should force some fibers to shorten too slowly and others too fast. This mechanical problem prompted research into the gearing of fish axial muscle and led to the discovery of helical fiber orientations that homogenize fiber velocities during swimming, but does such a strain gradient also exist and pose a problem for suction feeding? We measured muscle strain in bluegill sunfish, Lepomis macrochirus, and found that suction feeding produces a gradient of longitudinal strain that, unlike the mediolateral gradient for locomotion, occurs along the dorsoventral axis. A dorsoventral strain gradient within a muscle with fiber architecture shown to counteract a mediolateral gradient suggests that bluegill sunfish should not be able to generate high power outputs from the axial muscle during suction feeding—yet prior work shows that they do, up to 438 W kg−1. Solving this biomechanical paradox may be critical to understanding how many fishes have co-opted ‘swimming’ muscles into a suction feeding powerhouse.
Highlights
Of suction feeding performance across species[29,30,31,32]
We measured muscle shortening using sonomicrometry to determine whether the dorsal half of the axial musculature, the epaxial musculature, of bluegill sunfish exhibits a dorsoventral gradient of longitudinal strain in suction feeding and a mediolateral gradient of longitudinal strain in locomotion
We found that locomotor behaviors produced a mediolateral gradient of longitudinal strain in the epaxial muscle, while feeding behaviors produced a dorsoventral gradient of longitudinal strain (Figs. 2 and 3; see supplementary Fig. S1 for sample EMG traces)
Summary
Of suction feeding performance across species[29,30,31,32]. The lever model infers from specimen manipulation that the fulcrum is at the level of a joint within the pectoral girdle and makes the simplifying assumption that the input muscle force acts on a single point of the neurocranium, implying that epaxial muscle shortens uniformly[30]. We hypothesize that suction feeding is powered by beam-like bending that produces a dorsoventral gradient of longitudinal strain in the epaxial musculature, where muscle strain decreases from dorsal to ventral during any given bout of muscle shortening (Fig. 1d). If muscle fiber architecture is specialized to homogenize fiber strain within the musculature as it undergoes heterogeneous longitudinal strain during locomotion, high muscle power outputs are unlikely during suction feeding because the muscle fibers would be oriented to counteract a mediolateral gradient, not a dorsoventral gradient. Behaviors with motions that produce anatomically orthogonal strain gradients in the muscle might have gearing solutions that conflict with each other, preventing the muscle from generating maximum power output for both locomotion and suction feeding, and perhaps limiting peak muscle performance to only one of these vital behaviors. We measured muscle shortening using sonomicrometry to determine whether the dorsal half of the axial musculature, the epaxial musculature, of bluegill sunfish exhibits a dorsoventral gradient of longitudinal strain in suction feeding and a mediolateral gradient of longitudinal strain in locomotion
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