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First published online June 6, 2005
Journal of Experimental Biology 208, 2377-2387 (2005)
Published by The Company of Biologists 2005
doi: 10.1242/jeb.01618

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Patterns of red muscle strain/activation and body kinematics during steady swimming in a lamnid shark, the shortfin mako (Isurus oxyrinchus)

Jeanine M. Donley^1,*, Robert E. Shadwick¹, Chugey A. Sepulveda², Peter Konstantinidis³ and Sven Gemballa³

¹ Marine Biology Research Division, Scripps Institution of Oceanography, University of California, San Diego, La Jolla, CA 92093-0202, USA
² Pfleger Institute of Environmental Research, Oceanside, CA 92054, USA
³ Department of Zoology, University of Tübingen, Auf der Morgenstelle 28, 72076 Tübingen, Germany

View larger version (49K): [in a new window]   Fig. 1. Sample sonomicrometric and electromyogram (EMG) traces from swimming I. oxyrinchus. (A) Lateral view of a 91 cm mako swimming at 1 L s–1 in the swim tunnel. Red and blue arrows correspond to the axial positions shown in B–D. (B) Mako cross sections at 0.4 and 0.6L, showing the difference in size and location of the red muscle mass at the two axial positions. Sample of EMG and sonomicrometric data recorded simultaneously over several consecutive tailbeat cycles in the anterior (C) and posterior (D) axial positions.

View larger version (16K): [in a new window]   Fig. 2. Timing of electromyogram (EMG) offset (A) and onset (B) of activation relative to the strain cycle in all makos (N=7; open symbols) at anterior and posterior body positions, illustrating the lack of longitudinal variation in the phase of activation. Values shown for each individual represent a mean (± S.E.M.) of multiple tailbeat cycles. Also shown are mean EMG/strain phases for the leopard shark (filled symbols), modified from Donley and Shadwick (2003). Inset in B is a diagrammatic representation of activation phase relative to sinusoidal strain cycle in mako (red) and leopard shark (black).

View larger version (38K): [in a new window]   Fig. 3. Anterior red muscle strain (red trace), measured by sonomicrometry, superimposed onto predicted strain (open circles), calculated from midline curvature (K) at 0.6L for four consecutive tailbeat cycles in an 80 cm mako. Red muscle strain at 0.4L was in phase with curvature and predicted strain at 0.6L. The mako image, modified from Compagno (1998), is used to illustrate the relative positions of synchronized strain and body curvature.

View larger version (41K): [in a new window]   Fig. 4. Simultaneous recordings of red muscle (red trace) and adjacent white muscle (gray trace) strain at 0.4L during passive simulated swimming movements (A) and active steady swimming (0.5 L s–1) (B) in I. oxyrinchus.

View larger version (33K): [in a new window]   Fig. 5. Simultaneous recordings of red muscle (RM; red traces) and white muscle (WM; gray traces) strain at 0.6L on the right and left sides of the body during passive and active swimming in the mako. Numbers in A represent locations of implanted sonomicrometric crystals (1, WM near backbone on right side of the body; 2, RM on right side; 3, RM on left side). During passive simulated swimming movements (B), shortening in the red and white muscle on the right side of the body are in phase but 180° out of phase with shortening on the left side (vertical line), as expected. During active swimming (C), shortening in WM precedes shortening in RM by nearly 50% of the tailbeat cycle (box).

View larger version (42K): [in a new window]   Fig. 6. Dorsal midline curvature (K) and lateral displacement (D) calculated at five axial positions (0.4, 0.5, 0.6, 0.7 and 0.8L: positions shown in A) for multiple consecutive complete tailbeat cycles. To illustrate the degree of lateral motion along the body during steady swimming, the dorsal midline through one tailbeat cycle is shown in B. Colors for each data trace in C–F correspond to the axial positions indicated in A. Scale bar, 8 cm. One tailbeat cycle is magnified to show the difference in the rates of propagation of the waves of curvature (E) and lateral displacement (F) along the body.

View larger version (23K): [in a new window]   Fig. 7. Dorsal midline curvature as a function of time for several consecutive tailbeat cycles in the mako (solid lines) and leopard shark (broken lines; data from Donley and Shadwick, 2003). Data are presented for three body positions, as indicated by arrows in A: (B) 0.45L, (C) 0.6L and (D) 0.8L.

View larger version (40K): [in a new window]   Fig. 8. Patterns of red (red traces) and white (gray trace) muscle strain at 0.6L during active swimming, illustrating variation in amplitude and phase of strain within the RM mass. The locations of implanted sonomicrometric crystals are indicated as numbers 1–3 in the body cross-section in A and correspond to the data traces in B. Scale bar, 1 cm.

View larger version (163K): [in a new window]   Fig. 9. Vertical parasagittal histological sections of medial (A) and lateral (B) edges of red muscle (RM) mass at 0.6L, illustrating the difference in development of lubricative sheath (LS). The lubricative sheath that surrounds the RM mass is thicker and more well-developed on the medial surface of the RM. Scale bar, 0.2 cm. WM, white muscle.

View larger version (68K): [in a new window]   Fig. 10. Myotendinous architecture of the posterior region in the mako. (A) Diagram illustrating the myoseptal sheet (gray shaded region) and the relative position of the band of red muscle (RM; red) and hypaxial lateral tendon (black line); anterior to left. (B) Longitudinal section of RM (anterior to left; length of box is 5 cm), showing increase in hypaxial lateral tendon lengths (white) along the body. Enlarged image in C.

View larger version (18K): [in a new window]   Fig. 11. Correlation between body kinematics and red muscle (RM) dynamics during steady swimming. (A) Dorsal midline traces from 0.4L to the tail tip (1.0L) for selected time intervals through one complete tailbeat cycle in an 87 cm L mako. Numbers indicate points in time as the tailbeat cycle progresses; dots indicate positions along the body (green is 0.6L, aqua is 1.0L) for which data are illustrated in B and C. (B) Lateral displacement (D) as a function of time for the tailbeat cycle shown in A. (C) Curvature (K) calculated at 0.6L (dotted line) superimposed on lateral displacement for 0.6L (solid line as in B) for the single tailbeat cycle. (D) RM strain for 0.4L (broken red line) and 0.6L (solid red line) on the left side of the body.