Muscle strain histories in swimming milkfish in steady and sprinting gaits

Abstract

Adult milkfish (Chanos chanos) swam in a water-tunnel flume over a wide range of speeds. Fish were instrumented with sonomicrometers to measure shortening of red and white myotomal muscle. Muscle strain was also calculated from simultaneous overhead views of the swimming fish. This allowed us to test the hypothesis that the muscle shortens in phase with local body bending. The fish swam at slow speeds [U<2.6 fork lengths s-1 (=FL s-1)] where only peripheral red muscle was powering body movements, and also at higher speeds (2. 6>U>4.6 FL s-1) where they adopted a sprinting gait in which the white muscle is believed to power the body movements. For all combinations of speeds and body locations where we had simultaneous measurements of muscle strain and body bending (0.5 and 0.7FL), both techniques were equivalent predictors of muscle strain histories. Cross-correlation coefficients for comparisons between these techniques exceeded 0.95 in all cases and had temporal separations of less than 7 ms on average. Muscle strain measured using sonomicrometry within the speed range 0.9-2.6 FL s-1 showed that muscle strain did not increase substantially over that speed range, while tail-beat frequency increased by 140 %. While using a sprinting gait, muscle strains became bimodal, with strains within bursts being approximately double those between bursts. Muscle strain calculated from local body bending for a range of locations on the body indicated that muscle strain increases rostrally to caudally, but only by less than 4 %. These results suggest that swimming muscle, which forms a large fraction of the body volume in a fish, undergoes a history of strain that is similar to that expected for a homogeneous, continuous beam. This has been an implicit assumption for many studies of muscle function in many fish, but has not been tested explicitly until now. This result is achieved in spite of the presence of complex and inhomogeneous geometry in the folding of myotomes, collagenous myosepta and tendon, and the anatomical distinction between red and white muscle fibers.

Muscle power production during intermittent swimming in bluegill sunfish

“…The timing of red muscle length changes at the site of the EMG electrodes was estimated from body curvature (Coughlin et al, 1996; Katz et al, 1999; van Leeuwen et al, 1990). Sequential midline positions for propulsive tailbeats were traced from high‐speed video using Image J (National Institutes of Health).…”

Tunable stiffness in fish robotics: mechanisms and advantages

“…Virtually every component of the locomotor system in fishes has some degree of flexibility and undergoes both bending and longitudinal strain during swimming [96][97][98][99][100][101][102]. Undulatory motion of the fish body results in an obvious wave of bending that progresses from head to tail during forward locomotion [103][104][105].…”

Beam theory predicts muscle deformation and vertebral curvature during feeding in rainbow trout (Oncorhynchus mykiss)

“…As fish bend their bodies from side to side, the axial muscle tissue deforms like a simple beam (e.g. Coughlin et al, 1996 ; Goldbogen et al, 2005 ; Katz et al, 1999 ; van Leeuwen et al, 1990 ). This deformation forms a mediolateral strain gradient whereby longitudinal muscle strain at any given location is a product of both its distance from, and the curvature of, the neutral axis: the vertebral column ( Fig.…”

“…Advances in X-ray imaging methods allow direct measurement of vertebral curvature and muscle strain during feeding. Swimming studies have successfully used dorsal or ventral view, standard (light) video to measure lateral vertebral curvature by measuring the midline of the fish ( Coughlin et al, 1996 ; Katz et al, 1999 ; Shadwick et al, 1998 ), but this method is not reliable for measuring dorsoventral curvature ( Jimenez et al, 2021 ). Instead, X-ray reconstruction of moving morphology (XROMM) ( Brainerd et al, 2010 ) can be used to visualize and measure the 3D motion of the vertebral column in vivo ( Camp, 2021 ).…”

“…Longitudinal muscle deformation can be measured throughout many locations with fluoromicrometry: using biplanar X-ray videos to measure muscle deformation as the change in distance between radio-opaque markers ( Camp et al, 2016 ). Previous swimming studies have typically measured longitudinal muscle strain ( Coughlin et al, 1996 ; Goldbogen et al, 2005 ; Katz et al, 1999 ; Wakeling and Johnston, 1999 ) or muscle fibre strain ( Ellerby and Altringham, 2001 ) in only 2–3 locations simultaneously with sonomicrometry. Fluoromicrometry markers in fish have been oriented to measure longitudinal strain, not muscle fibre strain ( Camp and Brainerd, 2014 ; Camp et al, 2018 , 2020 ; Li et al, 2022 ).…”