RESUMEN

Muscle shortening underpins most skeletal motion and ultimately animal performance. Most animal muscle generates its greatest mechanical output over a small, homogeneous range of shortening magnitudes and speeds. However, homogeneous muscle shortening is difficult to achieve for swimming fish because the whole body deforms like a bending beam: as the vertebral column flexes laterally, longitudinal muscle strain increases along a medio-lateral gradient. Similar dorsoventral strain gradients have been identified as the vertebral column flexes dorsally during feeding in at least one body location in one fish. If fish bodies also deform like beams during dorsoventral feeding motions, this would suggest the dorsal body (epaxial) muscles must homogenize both dorsoventral and mediolateral strain gradients. We tested this hypothesis by measuring curvature of the anterior vertebral column with XROMM and muscle shortening in 14 epaxial subregions with fluoromicrometry during feeding in rainbow trout (Oncorhynchus mykiss). We compared measured strain with the predicted strain based on beam theory's curvature-strain relationship. Trout flexed the vertebrae dorsally and laterally during feeding strikes, yet when flexion in both planes was included, the strain predicted by beam theory was strongly and significantly correlated with measured strain (P<0.01, R2=0.60). Beam theory accurately predicted strain (slope=1.15, compared with ideal slope=1) across most muscle subregions, confirming that epaxial muscles experience dorsoventral and mediolateral gradients in longitudinal strain. Establishing this deformation-curvature relationship is a crucial step to understanding how these muscles overcome orthogonal strain gradients to produce powerful feeding and swimming behaviours.

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RESUMEN

Nearly all fish have flexible bodies that bend as a result of internal muscular forces and external fluid forces that are dynamically coupled with the mechanical properties of the body. Swimming is therefore strongly influenced by the body's flexibility, yet we do not know how fish species vary in their flexibility and in their ability to modulate flexibility with muscle activity. A more fundamental problem is our lack of knowledge about how any of these differences in flexibility translate into swimming performance. Thus, flexibility represents a hidden axis of diversity among fishes that may have substantial impacts on swimming performance. Although engineers have made substantial progress in understanding these fluid-structure interactions using physical and computational models, the last biological review of these interactions and how they give rise to fish swimming was carried out more than 20 years ago. In this Review, we summarize work on passive and active body mechanics in fish, physical models of fish and bioinspired robots. We also revisit some of the first studies to explore flexural stiffness and discuss their relevance in the context of more recent work. Finally, we pose questions and suggest future directions that may help reveal important links between flexibility and swimming performance.

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RESUMEN

Most fish species use concentric epaxial and hypaxial contractions to suction feed, whereby both muscle groups produce cranial expansion and negative intraoral pressures. In contrast, channel catfish (Ictalurus punctatus) suction feed with little to no cranial elevation and epaxial shortening, generating suction power primarily with hypaxial shortening and pectoral girdle retraction. We hypothesized that channel catfish (1) actively anchor the head via isometric contraction of the epaxials and (2) vary feeding performance by modulating the absolute and relative outputs of the co-contracting muscles. We used a combination of electromyography, intraoral pressure recordings and specimen manipulation, and developed a new dual-lever model to explore this idea. We detected epaxial and hypaxial co-contraction prior to suction force development in all strikes. Our model revealed that the differential between the co-contracting muscles may be used to modulate suction pressure and strike accuracy.

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RESUMEN

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.

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RESUMEN

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.

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RESUMEN

The axial musculature of many fishes generates the power for both swimming and suction feeding. In the case of the epaxial musculature, unilateral activation bends the body laterally for swimming, and bilateral activation bends the body dorsally to elevate the neurocranium for suction feeding. But how does a single muscle group effectively power these two distinct behaviours? Prior electromyographic (EMG) studies have identified fishes' ability to activate dorsal and ventral epaxial regions independently, but no studies have directly compared the intensity and spatial activation patterns between swimming and feeding. We measured EMG activity throughout the epaxial musculature during swimming (turning, sprinting, and fast-starts) and suction feeding (goldfish and pellet strikes) in largemouth bass (Micropterus salmoides). We found that swimming involved obligate activation of ventral epaxial regions whereas suction feeding involved obligate activation of dorsal epaxial regions, suggesting regional specialization of the epaxial musculature. However, during fast-starts and suction feeding on live prey, bass routinely activated the whole epaxial musculature, demonstrating the dual function of this musculature in the highest performance behaviours. Activation intensities in suction feeding were substantially lower than fast-starts which, in conjunction with suboptimal shortening velocities, suggests that bass maximize axial muscle performance during locomotion and underuse it for suction feeding.

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RESUMEN

Many suction-feeding fish use neurocranial elevation to expand the buccal cavity for suction feeding, a motion necessarily accompanied by the dorsal flexion of joints in the axial skeleton. How much dorsal flexion the axial skeleton accommodates and where that dorsal flexion occurs may vary with axial skeletal morphology, body shape and the kinematics of neurocranial elevation. We measured three-dimensional neurocranial kinematics in three species with distinct body forms: laterally compressed Embiotoca lateralis, fusiform Micropterus salmoides, and dorsoventrally compressed Leptocottus armatus The area just caudal to the neurocranium occupied by bone was 42±1.5%, 36±1.8% and 22±5.5% (mean±s.e.m.; N=3, 6, 4) in the three species, respectively, and the epaxial depth also decreased from E. lateralis to L. armatus Maximum neurocranial elevation for each species was 11, 24 and 37°, respectively, consistent with a hypothesis that aspects of axial morphology and body shape may constrain neurocranial elevation. Mean axis of rotation position for neurocranial elevation in E. lateralis, M. salmoides and L. armatus was near the first, third and fifth intervertebral joints, respectively, leading to the hypothesis of a similar relationship with the number of intervertebral joints that flex. Although future work must test these hypotheses, our results suggest the relationships merit further inquiry.