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

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...

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Autores principales:	Yordano E. Jimenez, Richard L. Marsh, Elizabeth L. Brainerd
Formato:	article
Lenguaje:	EN
Publicado:	Nature Portfolio 2021
Materias:	Medicine R Science Q
Acceso en línea:	https://doaj.org/article/47005f9049294cdca3d044c1ae974c2b
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spelling	oai:doaj.org-article:47005f9049294cdca3d044c1ae974c2b2021-12-02T17:16:14ZA biomechanical paradox in fish: swimming and suction feeding produce orthogonal strain gradients in the axial musculature10.1038/s41598-021-88828-x2045-2322https://doaj.org/article/47005f9049294cdca3d044c1ae974c2b2021-05-01T00:00:00Zhttps://doi.org/10.1038/s41598-021-88828-xhttps://doaj.org/toc/2045-2322Abstract 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.Yordano E. JimenezRichard L. MarshElizabeth L. BrainerdNature PortfolioarticleMedicineRScienceQENScientific Reports, Vol 11, Iss 1, Pp 1-9 (2021)
institution	DOAJ
collection	DOAJ
language	EN
topic	Medicine R Science Q
spellingShingle	Medicine R Science Q Yordano E. Jimenez Richard L. Marsh Elizabeth L. Brainerd A biomechanical paradox in fish: swimming and suction feeding produce orthogonal strain gradients in the axial musculature
description	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.
format	article
author	Yordano E. Jimenez Richard L. Marsh Elizabeth L. Brainerd
author_facet	Yordano E. Jimenez Richard L. Marsh Elizabeth L. Brainerd
author_sort	Yordano E. Jimenez
title	A biomechanical paradox in fish: swimming and suction feeding produce orthogonal strain gradients in the axial musculature
title_short	A biomechanical paradox in fish: swimming and suction feeding produce orthogonal strain gradients in the axial musculature
title_full	A biomechanical paradox in fish: swimming and suction feeding produce orthogonal strain gradients in the axial musculature
title_fullStr	A biomechanical paradox in fish: swimming and suction feeding produce orthogonal strain gradients in the axial musculature
title_full_unstemmed	A biomechanical paradox in fish: swimming and suction feeding produce orthogonal strain gradients in the axial musculature
title_sort	biomechanical paradox in fish: swimming and suction feeding produce orthogonal strain gradients in the axial musculature
publisher	Nature Portfolio
publishDate	2021
url	https://doaj.org/article/47005f9049294cdca3d044c1ae974c2b
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A biomechanical paradox in fish: swimming and suction feeding produce orthogonal strain gradients in the axial musculature

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