Motor control in the epaxial musculature of bluegill sunfish in feeding and locomotion

ABSTRACT Fishes possess an impressive repertoire of feeding and locomotor behaviors that in many cases rely on the same power source: the axial musculature. As both functions employ different skeletal systems, head versus body, integrating these functions would likely require modular motor control. Although there have been many studies of motor control in feeding or locomotion in fishes, only one study to date has examined both functions in the same individuals. To characterize bilateral motor control of the epaxial musculature in feeding and locomotion, we measured muscle activity and shortening in bluegill sunfish (Lepomis macrochirus) using electromyography and sonomicrometry. We found that sunfish recruit epaxial regions in a dorsal-to-ventral manner to increase feeding performance, such that high-performance feeding activates all the epaxial musculature. In comparison, sunfish seemed to activate all three epaxial regions irrespective of locomotor performance. Muscle activity was present on both sides of the body in nearly all feeding and locomotor behaviors. Feeding behaviors used similar activation intensities on the two sides of the body, whereas locomotor behaviors consistently used higher intensities on the side undergoing muscle shortening. In all epaxial regions, fast-starts used the highest activation intensities, although high-performance suction feeding occasionally showed near-maximal intensity. Finally, active muscle volume was positively correlated with the peak rate of body flexion in feeding and locomotion, indicating a continuous relationship between recruitment and performance. A comparison of these results with recent work on largemouth bass (Micropterus salmoides) suggests that centrarchid fishes use similar motor control strategies for feeding, but interspecific differences in peak suction-feeding performance are determined by active muscle volume.

A biomechanical paradox in fish: swimming and suction feeding produce orthogonal strain gradients in the axial musculature

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.

Kinematic integration during prey capture varies among individuals but not ecological contexts in bluegill sunfish, Lepomis macrochirus (Perciformes: Centrarchidae)

The general ability of components of an organism to work together to achieve a common goal has been termed integration and is often studied empirically by deconstructing organisms into component parts and quantifying covariation between them. Kinematic traits describing movement are useful for allowing organisms to respond to ecological contexts that vary over short time spans (milliseconds, minutes, etc.). Integration of these traits can contribute to the maintenance of the function of the whole organism, but it is unclear how modulation of component kinematic traits affects their integration. We examined the integration of swimming and feeding during capture of alternative prey types in bluegill sunfish (Lepomis macrochirus). Despite the expected modulation of kinematics, integration within individuals was inflexible across prey types, suggesting functional redundancy for solving a broad constraint. However, integration was variable among individuals, suggesting that individuals vary in their solutions for achieving whole-organism function and that this solution acts as a ‘top-down’ regulator of component traits, which provides insight into why kinematic variation is observed. Additionally, variation in kinematic integration among individuals could serve as an understudied target of environmental selection on prey capture, which is a necessary first step towards the observed divergence in integration among populations and species.