Muscle Strain in Swimming Milkfish
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The Journal of Experimental Biology 202, 529–541 (1999) 529 Printed in Great Britain © The Company of Biologists Limited 1999 JEB1633 MUSCLE STRAIN HISTORIES IN SWIMMING MILKFISH IN STEADY AND SPRINTING GAITS STEPHEN L. KATZ*, ROBERT E. SHADWICK AND H. SCOTT RAPOPORT Center for Marine Biotechnology and Biomedicine and Marine Biology Research Division, Scripps Institution of Oceanography, La Jolla, CA 92093-0204, USA *Present address and address for correspondence: Zoology Department, Duke University, PO Box 90325, Durham, NC 27708-0325, USA (e-mail: [email protected]) Accepted 10 December 1998; published on WWW 3 February 1999 Summary Adult milkfish (Chanos chanos) swam in a water-tunnel over that speed range, while tail-beat frequency increased flume over a wide range of speeds. Fish were instrumented by 140 %. While using a sprinting gait, muscle strains with sonomicrometers to measure shortening of red and became bimodal, with strains within bursts being white myotomal muscle. Muscle strain was also calculated approximately double those between bursts. Muscle strain from simultaneous overhead views of the swimming fish. calculated from local body bending for a range of locations This allowed us to test the hypothesis that the muscle on the body indicated that muscle strain increases rostrally shortens in phase with local body bending. The fish swam to caudally, but only by less than 4 %. These results suggest at slow speeds [U<2.6 fork lengths s−1 (=FL s−1)] where only that swimming muscle, which forms a large fraction of the peripheral red muscle was powering body movements, and body volume in a fish, undergoes a history of strain that is also at higher speeds (2.6>U>4.6 FL s−1) where they similar to that expected for a homogeneous, continuous adopted a sprinting gait in which the white muscle is beam. This has been an implicit assumption for many believed to power the body movements. For all studies of muscle function in many fish, but has not been combinations of speeds and body locations where we had tested explicitly until now. This result is achieved in spite simultaneous measurements of muscle strain and body of the presence of complex and inhomogeneous geometry bending (0.5 and 0.7FL), both techniques were equivalent in the folding of myotomes, collagenous myosepta and predictors of muscle strain histories. Cross-correlation tendon, and the anatomical distinction between red and coefficients for comparisons between these techniques white muscle fibers. exceeded 0.95 in all cases and had temporal separations of less than 7 ms on average. Muscle strain measured using Key words: fish, swimming, Chanos chanos, milkfish, sonomicrometry within the speed range 0.9–2.6 FL s−1 sonomicrometry, locomotion, musculo-skeletal mechanics, showed that muscle strain did not increase substantially biomimetics. Introduction The myotomal swimming muscle of fish is arranged as a assumptions that each myotome is mechanically linked to its series of interconnected blocks that lie along each side of the neighbors and that the force trajectories that they generate must body. Anatomically, this represents a departure from the pass from one myotome to the next along the body. In this familiar vertebrate locomotor design, and understanding the model, the wave of undulation represents the accumulation of mechanical consequences of the myotomal system is an muscle strain history along the body. As a consequence, each important goal of current research in fish biomechanics. The muscle acts locally – i.e. lateral bending produced by muscle present study investigates the magnitude and phase contraction occurs at approximately the same location on the relationships between the strain of myotomal muscle and local body as the muscle itself. If true, then one can calculate muscle body curvature in a representative teleost, the milkfish (Chanos strain amplitude and phase from body kinematics, specifically, chanos). from midline curvature. Over a hundred years ago Sir George Cayley proposed that Importantly, fish myotomes are not cubic blocks but are the swimming movements of trout resulted from the sequential highly folded and nested together in the longitudinal body axis activation of the blocks of muscle segments on each side of the (Nursall, 1956; Jayne and Lauder, 1995b). Consequently, one body, thus generating a wave of undulation that traveled myotome may span several intervertebral joints. Furthermore, posteriorly (Bone et al., 1995). This synthesis was based on the adjacent myotomes are separated by collagenous myoseptal 530 S. L. KATZ, R. E. SHADWICK AND H. S. RAPOPORT sheets that serve as insertion sites for the muscle fibers within captured with nets and transported to the Kewalo Basin each myotome and attach to the vertebral midline and the skin laboratory facility of the National Marine Fisheries Service in (Wainwright, 1980; Westneat et al., 1993). An additional Honolulu, Hawaii, USA. Of all individual fish examined in this feature is the anatomical distinction between functionally study (eight), only four produced data that met the selection different muscle fiber types. In most fishes, red fibers (used for criteria for all components of this study. Therefore, the sample low-intensity sustained swimming) are located in a lateral size for all statistical comparisons or descriptions represents wedge of parallel-fibered muscle close to the skin. White fibers the contribution of four fish. Fish were maintained in circular (used for high-intensity burst swimming) comprise the bulk of ponds 7 m in diameter and 1.2 m deep with a constant flow- the nested cones of muscle in the myotomes (Bone, 1966; through of sea water. Fish were fed frozen squid and mackerel Rome et al., 1984; Jayne and Lauder, 1993). This complex daily and also consumed green algae in the tanks. All fish used geometry makes it difficult to identify discrete force in this study were maintained in good health and feeding for trajectories across myotomes a priori, and therefore difficult long periods (more than 3 months) before being used in to accept or reject Cayley’s model. experiments. The temperature was maintained at ambient Although several studies of fish muscle dynamics have used ocean temperatures (approximately 20–24 °C) and ambient body curvature to calculate muscle strain amplitude and phase light cycles. Fish chosen for this study ranged from 1440 to (Videler and Hess, 1984; van Leeuwen et al., 1990; Rome et al., 2160 g in mass and from 45.6 to 51.3 cm in fork length (FL). 1993; Johnson et al., 1994), i.e. accepting Cayley’s assumption Post mortem examination indicated that the lateral red muscle that muscle contractions cause local bending, very few have extended from 0.25FL to the caudal peduncle at 0.95FL. attempted to verify the validity of this approach by comparison However, the wedge of lateral red muscle tapers at its rostral with direct strain measurements. One such method involves and caudal terminations. Rostral to a location of 0.3FL, the sonomicrometry, a technique that gives very accurate cross-sectional area of red muscle is 0.6 cm2, or less than 2 % measurements of the distance between two small piezoelectric, of total muscle area, and less than 10 % of the average red ultrasound probes that can be implanted in live tissue. If the muscle cross-sectional area from 0.3FL to 0.85FL. Caudal to probes are aligned with the shortening axis of muscle fibers, they a location of 0.85FL, the red muscle tapers to less than 0.4 cm2. give a direct and real-time measurement of the muscle strain. In Surgical procedures followed guidelines for animal care laid a sonomicrometry study of steady swimming in scup Stenotomus out by the animal subjects committee of the University of crysops, Coughlin et al. (1996) concluded that local body California, San Diego, CA, USA. Fish were anesthetized via bending, using simple beam theory, accurately predicted strains immersion in an oxygenated solution of MS-222 in superficial red muscle. In contrast, sonomicrometry of fast- [Finquel:methane tricaine sulfonate (Argent Chemical starts in trout Oncorhynchus mykiss led Covell et al. (1991) to Laboratories), 1:1000 (w/v) in sea water] buffered with sodium conclude that shortening of deep white muscle produced bending bicarbonate or Tris base (pH≈7.8). During surgery, the animal at more caudal locations and thus that local curvature was not a was supported on a chamois cradle and ventilated with a more good predictor of muscle strain. These two results are not dilute solution of oxygenated, buffered MS-222 (1:17500). necessarily incompatible and may, in fact, represent differences Swimming protocols were performed in a swim-channel in the organization of force transduction pathways in the treadmill described previously (Korsmeyer et al., 1997). The different fiber types. However, at this point, we cannot resolve tunnel has a volume of 3000 l. It is instrumented to monitor whether it is valid to calculate white muscle strain from midline and maintain temperature and O2 content. The maximum kinematics or whether the complex myotomal geometry working section dimensions are 113 cm (length) × 22.5 cm constrains the muscle from deforming as a homogeneous beam. (width) × 32.5 cm (height) (cross-sectional area 731 cm2). The In this study, we have used video image analysis and water tunnel has a mirror above the working section tilted at sonomicrometry to determine the time course and amplitude of 45 ° so that a camera located to the side of the tunnel can obtain strain in red and white muscle of milkfish during steady dorsal views of the swimming fish. A correction for solid swimming gaits powered by red muscle, as well as in high- blocking was employed in the manner of Bell and Terhune speed burst swimming involving white muscle. By comparing (1970) to correct the swimming speeds of the fish.