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First published online May 2, 2008
Journal of Experimental Biology 211, 1603-1611 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.013250
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Thunniform swimming: muscle dynamics and mechanical power production of aerobic fibres in yellowfin tuna (Thunnus albacares)

Robert E. Shadwick1,* and Douglas A. Syme2

1 Department of Zoology, University of British Columbia, Vancouver, BC, V6T 2A9, Canada
2 Department of Biological Sciences, University of Calgary, Calgary, AB, T2N 1N4, Canada


Figure 1
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  		Fig. 1. (A) Lateral view of a yellowfin tuna, indicating the region where sonomicrometry and muscle fibre sample sites were located (0.45–0.65 L, where L is fork length). (B) View of caudal penduncle with skin removed showing lateral tendons that transmit forces from the muscle to the tail and the tendon buckle transducer used to measure force in the tendons. (C) View of one side of a yellowfin in cross-section at 0.55 L showing the deep location of the aerobic red muscle and illustrating the positioning of a sonomicrometer crystal in the red muscle.

 

Figure 2
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  		Fig. 2. (A) Summary of tail beat frequency vs swim speed for 95 swimming bouts from 12 yellowfin tuna used in this study (mean length=0.450±0.05 m; mean mass=1.53±0.54 kg). Solid line is a fitted regression (y=1.22x+0.85; R2=0.91) with 95% confidence intervals (broken lines). (B) Stride length vs swim speed derived from data in A.

 

Figure 3
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  		Fig. 3. (A) Example of length changes recorded by sonomicrometry in red muscle at three axial positions in a 54 cm yellowfin tuna swimming at 1.3 L s–1. (B) Expanded section of traces in A with length changes expressed as % strain. Vertical lines show the progressive time delay from anterior to posterior positions: coloured lines indicate time of minimum muscle length during the cycle, black lines indicate time that the muscle passed through resting length.

 

Figure 4
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  		Fig. 4. Velocity of strain wave in deep red muscle, calculated as the distance between recording sites divided by the time shift (N=6; R2=0.59). Each individual is represented by a different symbol.

 

Figure 5
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  		Fig. 5. Comparison of red muscle strain at 0.5 L measured by sonomicrometry (solid line) vs strain calculated from midline curvature (symbols). Note these two waveforms differ in amplitude and phase.

 

Figure 6
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  		Fig. 6. Example of EMG and length change in red muscle at 0.5 L of a 39 cm yellowfin tuna swimming at 2.6 L s–1. (A) Sixteen consecutive tail beat cycles during steady swimming. (B) Expanded time scale for two typical cycles showing that muscle activation begins during the latter part of lengthening (solid vertical lines) and ends about half way through shortening (broken vertical lines). Activation phases for these two cycles are indicated.

 

Figure 7
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  		Fig. 7. (A) Example of force measured in the caudal tendons and red muscle length change (expressed as strain) measured at 0.5 L in a 45 cm yellowfin tuna swimming at 2.2 L s–1. (B) In vivo work loop resulting from plot of tendon force and muscle length for three cycles of traces in A.

 

Figure 8
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  		Fig. 8. Examples of work loops obtained from yellowfin tuna red muscle fibers sampled from 0.5 L. Rest length was 4.0 mm, strain amplitude for each was ±5.5%; stimulus phase and duration were adjusted to produce maximum net work at each frequency. Values of net work, in J kg–1, are shown in italic type for each frequency. All work loops progress in an anti-clockwise direction (arrows), signifying net positive work. Experiments were conducted at 25°C.

 

Figure 9
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  		Fig. 9. The effect of strain amplitude on work loops from red muscle taken from 0.5 L. Cycle frequency was 3 Hz, strains used were ±2.75, ±5.5, ±8%, and temperature was 25°C. Net work for each strain is shown in J kg–1. Solid line portions of each cycle represent the period when stimulus was on, broken portions are the period when stimulus was off, and arrows indicate stimulus onset.

 

Figure 10
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  		Fig. 10. (A) Net work per cycle vs cycle frequency from work loops of yellowfin tuna red muscle optimized for maximum work at 25°C. (B) Net power calculated from data in A. Strains are ±5.5% (black circles), ±2.75% (blue triangles), ±8% (red squares). Values are means ± s.e.m. (N=5).

 

Figure 11
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  		Fig. 11. Net power vs strain amplitude for yellowfin tuna red muscle, determined from work loops performed at 3 Hz. Values are means ± s.e.m. (N=5). Pairwise comparisons show that power output at ±5.5% and ±8% are not significantly different (P>0.05) but both are significantly higher than power at ±2.75% strain (P<0.01).

 

Figure 12
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  		Fig. 12. (A) Stimulus duty cycle and (B) stimulus phase used to obtain maximal work from yellowfin tuna red muscle taken from 0.5 L when strain amplitude was ±5.5%. Values are means ± s.e.m. (N=5). For comparison, data from skipjack red muscle (Syme and Shadwick, 2002Go) are included (broken lines). In both cases temperature was held at 25°C.

 

Figure 13
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  		Fig. 13. A comparison of isometric twitch properties of yellowfin tuna red muscle (shaded bars, N=5) at 0.5 L and 0.65 L, and white muscle (white bars, N=2) at 0.45 L and 0.65 L, at 25°C; values are means ± s.e.m. Time to peak force for red muscle was significantly longer at 0.65 L (asterisk: t-test, P=0.03). Twitch times for skipjack red muscle at 0.44 L and 0.70 L (diamonds) are shown for comparison (Syme and Shadwick, 2002Go).

 

Figure 14
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  		Fig. 14. Comparison of power curves for red muscle from yellowfin (solid line) and skipjack (broken line), normalized by maximum power for each. Both at 25°C. Horizontal bars represent the range of tail beat frequencies observed during unrestrained cruise swimming in yellowfin (solid line) and skipjack (broken line). Data for skipjack are from previous work (Syme and Shadwick, 2002Go).

 

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© The Company of Biologists Ltd 2008