First published online April 18, 2008
Journal of Experimental Biology 211, 1463-1474 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.017160
Mechanical specialization of the obliquely striated circular mantle muscle fibres of the long-finned squid Doryteuthis pealeii
Joseph T. Thompson1,*,
John A. Szczepanski2 and
Joshua Brody2
1 Department of Biology, Franklin & Marshall College, PO Box 3003,
Lancaster, PA 17604-3003, USA
2 Department of Biology, St Joseph's University, 5600 City Avenue, Philadelphia,
PA 19131, USA
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Fig. 1. Mantle morphology. (A) Photograph of a cross section of the formalin-fixed
mantle of a juvenile Doryteuthis pealeii. The section was taken
approximately from the midpoint along the length of the mantle. The diameter
of the mantle is about 25 mm. Ctenidia (Ct), mantle (M), mantle cavity (MC),
and viscera (V). (B) A schematic illustrating only the mantle muscles. The
circular muscles compose the majority of the mantle musculature but regularly
spaced bands of radial muscle fibres (RM) are also present. There are two
types of circular muscles: central mitochondria poor (CMP) and superficial
mitochondria rich (SMR). The schematic exaggerates the size of the muscle
fibres and the proportion of SMR to CMP fibres. In an adult D.
pealeii, the outer and inner layers of SMR fibres together compose only
4–6% of the thickness of the mantle wall. (C) A schematic of a muscle
preparation illustrating the foil clips and the muscle. The gray ovals
represent the cut ends of the radial muscle fibres.
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Fig. 2. Electron micrographs of cross sections of SMR (A) and CMP (B) circular
muscle fibres to illustrate differences in the cells. Note the large core of
mitochondria (M) in the SMR fibres and the more extensive sarcoplasmic
reticulum (arrows) in the CMP fibres. Scale bars, 2 µm (A); 1 µm (B).
(C,D) Electron micrographs of longitudinal sections of the SMR (C) and CMP (D)
circular muscle fibres. Scale bar for C and D, 0.5 µm. Note the longer
thick filaments (arrows) in the SMR fibre.
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Fig. 3. Thick filament length in the two types of muscle fibres. The thick
filaments of the SMR fibres (black) were significantly longer than those of
the CMP fibres (white) (ANOVA with Tukey HSD post hoc test). The box
plots illustrate the median (the horizontal line), the upper and lower
quartile (the box), and the range of the data (the `whiskers'). There were no
outliers. We measured 270 SMR thick filaments and 260 CMP thick filaments from
5 animals. *Significantly different (P<0.001).
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Fig. 4. Comparison of cross sectional areas of the whole fibre, the core of
mitochondria, and the myofilaments between SMR (black) and CMP (white) fibre
preparations. The plots illustrate the median (the horizontal line), the upper
and lower quartile (the box), and the range of the data (the `whiskers').
There were no outliers. Approximately 40 SMR and 40 CMP fibres were measured
from each of five different animals. *Significantly different
(P<0.001; ANOVA with Tukey HSD post hoc test).
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Fig. 5. Force–time relationship in twitch (2 ms pulse, 1 Hz; gray line) and
tetanus (2 ms pulse, 400 Hz, 100 ms duration; black line) for CMP (A) and SMR
(B) preparations. The tetanus trace in B also illustrates the temporal aspects
of force that we measured. The lowest black line illustrates the timing of
electrical stimuli. Please note that the scale of the time axis does not
permit accurate depiction of the timing of electrical stimuli.
TL, latent period, measured as the time from the beginning
of the first rectangular pulse stimulation to the initial rise in force;
TP, time from the initial rise in force to the peak force;
T50, time required for force to fall from the peak to 50%
peak.
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Fig. 6. Variation of peak isometric stress (A) and twitch:tetanus ratio (B) between
the two different muscle fibre preparations in tetanus (400 Hz, 100 ms) at
20°C. CMP fibres produced significantly less isometric stress than SMR
fibres (P<0.0001; ANOVA with Tukey HSD post hoc test).
CMP fibres had a significantly higher twitch:tetanus ratio than SMR fibres
(P=0.046; ANOVA with Tukey HSD post hoc test). The numbers
above each bar are the mean ± s.d. P0 is reported
as mN mm–2 physiological cross section.
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Fig. 7. Comparison of maximum unloaded shortening velocity
(Vmax) in brief tetanus (50 Hz, 100 ms) at 20°C. (A)
Slack step test data for one CMP (open circles) and one SMR (filled circles)
preparation. (B) Maximum unloaded shortening velocity for the two different
muscle fibre preparations. The numbers above each bar are the mean ±
s.d. CMP fibres had a significantly higher Vmax than SMR
fibres (P=0.0003; ANOVA with Tukey HSD post hoc test).
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Fig. 8. Comparison of typical active (in brief tetanus) and passive forces for CMP
(A) and SMR (B) preparations. Note that the passive force is higher in the SMR
than in the CMP preparations.
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Fig. 9. Illustration of how mantle diameter and thickness change during a jet. The
lower schematic slightly exaggerates the increase in mantle wall thickness
that occurs as the mantle contracts. ti, initial (i.e.
resting) mantle wall thickness; tf, final wall thickness
(i.e. at the end of contraction during the exhalant phase of the jet);
ri, initial radius of the outer edge of the mantle;
rf, the final radius of the outer edge of the mantle.
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© The Company of Biologists Ltd 2008
