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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.
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Beam theory predicts muscle deformation and vertebral curvature during feeding in rainbow trout ( Oncorhynchus mykiss )
ABSTRACT 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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- Award ID(s):
- 2208916
- PAR ID:
- 10516045
- Publisher / Repository:
- The Company of Biologists
- Date Published:
- Journal Name:
- Journal of Experimental Biology
- Volume:
- 226
- Issue:
- 20
- ISSN:
- 0022-0949
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1242/jeb.245788
