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Mechanical properties of red and white swimming muscles as a function of the position along the body of the eel Anguilla anguilla

K. D’Août^1,*, N. A. Curtin², T. L. Williams³ and P. Aerts¹

¹ Department of Biology, University of Antwerp (U.I.A.), Universiteitsplein 1, B-2610 Wilrijk, Belgium,
² Division of Biomedical Sciences, Imperial College School of Medicine, London SW7 2AZ, UK and
³ Department of Physiology, St George’s Hospital Medical School, University of London, London SW17 0RE, UK

View larger version (18K): [in a new window]   Fig. 1. Phase of onset of electromyographic (EMG) activity recorded at different locations along the body of fish during steady swimming. From published data, we calculated phase as the time from the start of shortening to the start of EMG activity, expressed as a percentage of the cycle time (see Fig.3). 1Skipjack tuna Katsuwonus pelamis, red muscle (Shadwick et al., 1999); 2Pacific bonito Sardo chiliensis, slow-twitch muscle (Ellerby et al., 2000); 3carp Cyprinus carpio, red muscle (van Leeuwen et al., 1990); 4rainbow trout Oncorhynchus mykiss, slow muscle (Hammond et al., 1998); 5Atlantic mackerel Scomber scombrus, red muscle (Wardle and Videler, 1993); 6Pacific mackerel Scomber japonicus, red muscle (Shadwick et al., 1998); 7largemouth bass Micropterus salmoides, red muscle (Jayne and Lauder, 1995); 8scup Stenotomus chrysops, red muscle (Rome et al., 1993); 9lamprey Lampetra fluviatilis (Williams et al., 1989); 10American eel Anguilla rostrata swimming at 1BLs-1, red muscle (Gillis, 1998); 11American eel Anguilla rostrata swimming at 0.75BLs-1, red muscle (Gillis, 1998). BL is body length.

View larger version (17K): [in a new window]   Fig. 2. Time required for relaxation of force of muscle fibres isolated from different locations along the length of the fish. We calculated relaxation times as multiples of the relaxation time for the muscle from the rostral end of the fish. 1Time from twitch stimulus to 90% relaxation of white muscle from saithe Pollachius virens (Altringham et al., 1993); 2time from last stimulus to 50% relaxation after a brief tetanus of fast fibres from short-horned sculpin Myoxocephalus scorpius (Johnston et al., 1993); 3time from twitch stimulus to 90% relaxation of slow fibres from trout Oncorhynchus mykiss (Hammond et al., 1998); 4time for relaxation from 90% to 10% of force after a brief tetanus of red muscle from scup Stenotomus chrysops (Rome et al., 1993); 5time for relaxation from 90% to 10% of force after a brief tetanus of red muscle from scup Stenotomus chrysops (Swank et al., 1997); 6time from twitch stimulus to 90% relaxation of red muscle from scup Stenotomus chrysops (Swank et al., 1997); 7time from last stimulus to 50% relaxation after a tetanus of red fibres from eel (Anguilla anguilla, this study). Values are means ± S.E.M., N=3–6. See Fig.5A and text. 8Time from twitch stimulus to 50% relaxation of white fibres from eel (Anguilla anguilla, this study). Values are means ± S.E.M., N=6–15. See Fig.5B and text.

View larger version (20K): [in a new window]   Fig. 3. Strain and stimulation pattern during the sinusoidal strain experiments. Strain was constant at L0±10%, where L0 is the length giving maximum isometric force. Stimulation duration was 0.4s (0.4 cycle) and was given at four different phases, -20%, -10%, 0% and +10%. Phase is the time from the start of shortening to the time of the first stimulus, expressed as a percentage of cycle duration.

View larger version (12K): [in a new window]   Fig. 4. Sarcomere lengths from different locations along the body length. Sarcomere lengths were measured by laser diffraction. Values are means ± S.E.M. for six fibres randomly selected from the fibre preparation concerned. 1–3 fibre preparations were measured. (A) Red fibres; (B) white fibres.

View larger version (11K): [in a new window]   Fig. 5. Time from first stimulus to 50% and 100% peak force and time from last stimulus to 50% peak force during relaxation in isometric stimulations. Each point is the mean of observations made on one fibre preparation. +, time to peak force; x, time to 50% peak force; s, time to 50% relaxation. (A) Results from eight red fibre preparations using tetanus stimulation. Regressions: for time to 50% peak force, y=(0.174±0.017)+(0.02±0.03)x, r2=0.067, P=0.535; for time to 100% peak force, y=(0.459±0.010)+ (0.01±0.02x)x, r2=0.091, P=0.460; for time to 50% relaxation, y=(0.281±0.039)+(0.07±0.07)x, r2=0.140, P=0.360, where y is time in seconds and x is fraction of body length. Values are means ± S.E.M. (B) Results from 13 white fibre preparations using twitch stimulation. The lines are regressions: for time to 50% peak force, y=(0.039±0.011)+(0.0002±0.0002)x, r2=0.050, P=0.464; for time to 100% peak force, y=(0.075±0.020)+(0.0003±0.0004)x, r2=0.055, P=0.441; for time to 50% relaxation, y=(0.170±0.054)+(0.0009±0.0011)x, r2=0.066, P=0.395.

View larger version (19K): [in a new window]   Fig. 6. Red fibre preparations: work loops (force versus length change) during movement at 1Hz and with a stimulation duty cycle of 0.4 at four different stimulation phases, as shown in the diagrams on the left. Fibres were taken from four different positions along the body, as shown in the diagram at the bottom. BL, body length. The scale for the different work loops is given on the left of the loop: vertical, 10mN; horizontal, 0.1 mm. The arrow on each work loop indicates the movement direction. The sign in the loop indicates whether the net work was positive or negative. The ripple on the force recordings from 0.2 and 0.8BL, where BL is body length, is noise from the recording circuit. It is prominent in these recordings because these muscle preparations were small and therefore produced low active force. All recordings are from fibre preparations from the same eel.

View larger version (28K): [in a new window]   Fig. 7. Red fibre preparations: superimposed time courses of power (thick line) and cumulative work (thin line) during one cycle of movement at 1Hz. Stimulation with a duty factor of 0.4 was given at four different stimulation phases, as shown in the diagrams on the left. Fibres were taken from four different positions along the body, as shown in the diagram at the bottom. BL, body length. The power scale is shown on the left axis and the work scale on the right axis. All recordings are from fibre preparations from the same eel.

View larger version (13K): [in a new window]   Fig. 8. Net work in one cycle of movement at 1Hz with a stimulation duty factor of 0.4 at four different stimulus phases. Different colors refer to results for different muscle preparations. Net work is expressed relative to the average work for that fibre preparation over all phase conditions applied. (A) Results for six red fibre preparations; (B) results for six white fibre preparations. BL, body length.

View larger version (18K): [in a new window]   Fig. 9. White fibre preparations: work loops (force versus length change) during movement at 1Hz and with a stimulation duty factor of 0.4 at four different stimulation phases, as shown in the diagrams on the left. Fibres were taken from four different positions along the body, as shown in the diagram at the bottom. BL, body length. The scale for the different work loops is given on the left of the loop: vertical, 10mN; horizontal, 0.1 mm. The arrow on each work loop indicates the movement direction. The sign in the loop indicates whether the net work was positive or negative. All recordings are from fibre preparations from the same eel.

View larger version (27K): [in a new window]   Fig. 10. White fibre preparations: superimposed time courses of power (thick line) and cumulative work (thin line) during one cycle of movement at 1Hz. Stimulation with a duty factor of 0.4 was given at four different stimulation phases, as shown in the diagrams on the left. Fibres were taken from four different positions along the body, as shown in the diagram at the bottom. The power scale is shown on the left axis and the work scale on the right axis. All recordings are from fibre preparations from the same eel. BL, body length.