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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
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
* Author for correspondence (e-mail: joseph.thompson{at}fandm.edu)
Accepted 7 March 2008
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIXReferences |
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Key words: cephalopod, obliquely striated muscle, circular muscles, thick filaments, mechanical properties, kinematics
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIXReferences |
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), Brachiopoda
(Kuga and Matsuno, 1988),
Bryozoa (Bouligand, 1966),
Echinodermata (Carnevali et al.,
1986), Mollusca (e.g. Kawaguti
and Ikemoto, 1957; Matsuno and
Kuga, 1989), Nematoda (e.g.
Rosenbluth, 1965), Nemertea
(Norenburg and Roe, 1997),
Platyhelminthes (MacRae, 1965;
Ward et al., 1986), Rotifera
(Bouligand, 1966), Sipunculida
(DeEguileor and Valvassori,
1977) and Urochordata (Bone and
Ryan, 1974). Despite the ubiquity of obliquely striated muscles,
their specialization has received relatively little attention. Two different
fibre types have been reported for the longitudinal muscles of leeches
(Rowlerson and Blackshaw,
1991), earthworms (D'Haese and
Carlhoff, 1987), and the mantle and fins of some cephalopods
(Bone et al., 1981;
Mommsen et al., 1981;
Kier, 1989), but both the
mechanisms and performance consequences of specialization are virtually
unknown.
Mantle muscle specialization
The mantle of squids is a conical muscular sac that encloses the organs and
the mantle cavity. Its functions include providing mechanical support for the
fins and power for respiratory ventilation movements and jet locomotion. The
muscles of the mantle are arranged primarily in two orientations
(Marceau, 1905;
Williams, 1909;
Young, 1938):
circumferentially (the circular muscles) and radially (the radial muscles;
Fig. 1). Contraction of the
circular muscles drives water out of the mantle cavity via the funnel
while contraction of the radial muscles helps to refill the mantle cavity with
water at the end of the power stroke
(Young, 1938). Many squid
species possess two types of circular muscle cells: centrally located,
mitochondria-poor (CMP) fibres and superficially located, mitochondria-rich
(SMR) fibres (Figs 1,
2)
(Bone et al., 1981;
Mommsen et al., 1981)
[terminology from Preuss et al. (Preuss et
al., 1997)]. Both fibre types are obliquely striated
(Marceau, 1905;
Hanson and Lowy, 1957).
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;
Mommsen et al., 1981;
Bartol, 2001a). Conversely, the
CMP circular muscle fibres are hypothesized to provide power for more vigorous
and rapid jets, including escape jets (Bone
et al., 1981; Mommsen et al.,
1981; Gosline et al.,
1983; Bartol,
2001a). The hypothesized functions of the SMR and CMP circular
muscle fibres are based on several lines of evidence. (1) Although both fibre
types contain a core of mitochondria, SMR muscle fibres have a much larger
core with more numerous mitochondria and mainly use oxidative metabolism,
while CMP fibres are primarily glycolytic
(Bone et al., 1981;
Mommsen et al., 1981); (2) an
extensive network of capillaries supplies the SMR fibres while the CMP fibres
have less vascularisation (Bone et al.,
1981); (3) electromyographic recordings in loliginid squids
indicate that SMR fibres are active during the low amplitude contractions of
the mantle commonly used for respiration and slow jetting while the CMP fibres
are quiescent (Bartol, 2001a).
In contrast, the CMP fibres are active during rapid jetting
(Gosline et al., 1983;
Bartol, 2001a).
The distinction between SMR and CMP fibres may not be entirely
straightforward. Mommsen and colleagues suggested that enzymatic differences
between SMR and CMP fibres vary with lifestyle
(Mommsen et al., 1981). For
example, unlike the nektonic and pelagic squids in their study, the one
benthic species they examined showed few differences in oxidative and
glycolytic enzyme activity between the two fibre types. There may be at least
two types of CMP fibres that differ in sodium conductance
(Gilly et al., 1996).
There are striking differences in the dimensions of the thick myofilaments
in the SMR and CMP fibres of the loliginid squid Sepioteuthis
lessoniana. In newly hatched S. lessoniana, the thick filament
lengths of both the SMR and CMP fibres average only 1 µm, ranging in length
from 0.7 to 1.4 µm (Thompson and Kier,
2006). In juvenile S. lessoniana, the thick filament
length of the SMR fibres averages 2 µm and ranges up to 4 µm, while the
CMP fibres average 1.5 µm but range only up to 2.2 µm
(Thompson and Kier, 2006).
Thus, there is an ontogenetic increase in thick filament length in S.
lessoniana, and this increase in the SMR fibres occurs more rapidly than
in the CMP fibres. Because thick filament length is proportional to the peak
isometric tension generated by a striated muscle fibre but inversely
proportional to maximum unloaded shortening velocity (e.g.
Josephson, 1975;
Kier and Curtin, 2002),
differences in thick filament length between SMR and CMP circular muscle
fibres may result in differences in contractile properties, assuming other
aspects of the two types are similar.
The dimensions of the myofilaments, however, are but one factor that may
affect the contractile properties of the SMR and CMP muscle fibres. The
contractile properties of striated muscle fibres may be altered in a variety
of ways including, but not limited to, expression of different isoforms of the
myofilament lattice proteins (e.g.
Kendrick-Jones et al., 1976;
Sweeney et al., 1988;
Marden et al., 1998;
Schiaffino and Reggiani, 1996;
Toniolo et al., 2007). In
contrast to mammals, in which nine myosin heavy chain (MyHC) genes are
expressed in skeletal and cardiac muscle and 38 orthologs of MyHC have been
putatively identified (Maccatrozzo et al.,
2007), only a single MyHC gene has been identified to date in
loliginid squid, although it may have two splice variants
(Matulef et al., 1998). It is
possible, then, that muscle fibre specialization in loliginid squids occurs
through alteration in thick filament length, rather than biochemically
(Kier and Schachat, 1992;
Kier and Curtin, 2002;
Kier and Schachat, 2008).
Specific questions addressed
The goals of the present study were to characterize the mechanical
properties of the two types of mantle muscle fibres, examine the extent to
which thick filament length predicts muscle fibre mechanical properties, and
evaluate the roles of the two fibre types in locomotion. We used transmission
electron microscopy (TEM) to measure the dimensions of the thick filaments of
the SMR and CMP muscle fibres and made predictions about the contractile
properties of each fibre type based solely on differences in thick filament
length. We tested these hypotheses by measuring contractile properties of
partially isolated bundles of SMR and CMP muscle fibres. Finally, we used
mantle kinematics data to analyze the roles of the two fibre types in jet
locomotion.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIXReferences |
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We caught male and female D. pealeii at night from lighted piers in South Bristol and Walpole, Maine, USA, between 1 June and 10 August 2006. The animals were sexually mature and ranged in size from 112 to 295 mm dorsal mantle length (mean ± s.d.=167±46 mm). Most animals were trapped with a 4.2 m diameter cast net, though some were caught with squid jigs. Squid were housed in a 1 mx2 mx0.5 m tank provided with flow-through seawater at 15°C. The animals were fed small live fish (Clupea sp. and Notemigonus sp.) daily. No squid was kept in captivity for more than one week. We used only squid that had no visible damage to the skin or mantle and that appeared to be healthy.
Tissue preparation for mechanical tests
Each squid was killed by decapitation and its mantle transferred
immediately to the top of a frozen foam freezer pack. We excised a small
portion of the ventral mantle at a position of 1/4 to 1/2 of the dorsal mantle
length from the anterior mantle margin. We then peeled the skin from the
sample and glued it (using n-butyl cyanoacrylate; Vetbond, 3M, St Paul, MN,
USA) to the temperature-controlled stage of a vibratome (Vibratome, St Louis,
MO, USA). Immediately after gluing, we filled the bath surrounding the stage
with a modified squid saline solution at 4°C. The temperature of the bath
was maintained at 4°C for the duration of cutting. The modified solution
contained (in mmol l–1): NaCl (450),
MgCl2·6H2O (10), Hepes (10), EGTA (10), pH
adjusted to 7.8 with 2 mol l–1 NaOH
(Milligan et al., 1997).
For the superficial mitochondria-rich (SMR) preparations, we cut sheets of the mantle 0.8–0.1 mm thick using the vibratome. The sheets were cut parallel to the frontal plane of the mantle. Each sheet, therefore, was composed primarily of intact circular muscle fibres, though fragments of radial muscle fibres and connective tissue fibres were also present (Fig. 1). We made no attempt to remove the outer tunic.
Using the vibratome allowed us to isolate SMR and CMP fibres in different muscle preparations and also severed the radial muscles fibres, thereby interfering with their ability to contract. It is important to note, however, that mantle is a complex, muscular organ. Although we took care to segregate SMR and CMP fibres into two types of preparations, we conducted tests on tissue preparations that included both muscle and short sections of connective tissue fibres. Nonetheless, we believe the preparations were suitable for highlighting important mechanical differences between the two muscle fibre types.
We trimmed the mantle sheets into pieces 5–10 mm long and 2–4
mm wide. We glued T-shaped foil clips
(Milligan et al., 1997) to
each end of the mantle slice using Vetbond
(Fig. 1C) and then transferred
the preparation to a temperature-controlled muscle bath. The muscle bath was
filled with standard squid saline containing (in mmol l–1):
NaCl (470), KCl (10), CaCl2 (10),
MgCl2·6H2O (50), Glucose (20), Hepes (10), pH
adjusted to 7.8 with 2 mol l–1 NaOH
(Milligan et al., 1997). The
temperature of the muscle bath was maintained at 20±0.2°C. This
temperature was 5–7°C warmer than the seawater from which the D.
pealeii squid were captured but was within the normal range of
temperatures encountered by this species in the field. We chose 20°C,
partly because preparation survival was higher than at 13–15°C and
partly because we hope in the future to compare the results of experiments on
the CMP fibres between D. pealeii and two other species of loliginid
squids that live in 20–27°C water.
For CMP preparations, we cut 0.1–0.15 mm thick sheets from the central zone of the mantle (Fig. 1) with the vibratome, trimmed them, and then attached foil clips as described above. We were unable to compare SMR and CMP preparations from the same animal.
Muscle mechanics experiments
Once in the muscle bath, one foil clip was attached to a force transducer
(404A Transducer System, Aurora Scientific, Ontario, CA, USA) and the other to
a computer-controlled servomotor (322C Muscle Lever System, Aurora
Scientific). We allowed muscle preparations to equilibrate in the standard
squid saline for 30 min prior the start of the experiment.
We followed the protocols outlined elsewhere
(Milligan et al., 1997;
Kier and Curtin, 2002) for
conducting the mechanical tests. We stimulated the muscle preparations with
rectangular constant current pulses via platinum plate electrodes
that were of sufficient size to cover the length of preparation. The
length–force relationship of the preparation was determined using
supramaximal brief tetanic (2 ms pulses, 50 Hz, 200 ms duration) and twitch
stimulations. Once we determined the length (L0) of the
preparation that yielded peak tetanic force (P0), we next
studied the stimulus frequency–force relationship using brief tetani (2
ms pulse, 200 ms duration, 300 s between successive tetani) at a range of
frequencies between 1 and 500 Hz. We calculated the peak tetanic stress of the
fibres by dividing P0 by the physiological cross section
of the preparation (see following sections for details). With the preparation
maintained at L0, we then used slack step tests
(Edman, 1979) to estimate the
maximum unloaded shortening velocity (Vmax) in brief
tetanus. We used four different step lengths for each preparation that varied
from 1% to 6% of L0. Step length data were plotted against
the corresponding time of force recovery. The data were fit with a linear
regression. The slope of the regression was the maximum unloaded shortening
velocity (Edman, 1979). Each
slope was then divided by L0 to normalize for variations
in preparation length. We conducted all of the above tests on seven SMR and
ten CMP preparations.
We also analyzed three temporal aspects of the brief tetanic contraction at L0. First, we measured the latent period (TL) as the time from the beginning of the first rectangular pulse stimulation to the initial rise in force (see Fig. 5B for illustrations). Second, we measured the time to peak (TP) as the initial rise in force to the peak force produced. Finally, we measured the time required for force to fall from the peak to 50% peak (T50).
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Control for radial muscle function
The radial muscles serve as antagonists to the circular muscles. The muscle
preparations we studied were composed of both circular fibres and fragments of
radial fibres. Simultaneous contraction of both fibre types may have affected
the magnitude of force produced by the circular muscles. Therefore, we treated
several of our preparations with 20 µmol l–1 acetylcholine
mixed in standard squid saline. Because acetylcholine serves as a
neurotransmitter for radial muscles but not for the circular muscles, any
change in the dimensions of the muscle preparations would have indicated
radial muscle shortening (Bone et al.,
1982; Collins and Tsutsui,
2003). We saw no measurable change in any of the preparations and
therefore concluded that vibratome sectioning disabled the radial muscle
fibres.
Determination of physiological cross section of the fibre preparations
Immediately following the mechanical testing, the preparations were fixed
at L0 at 4°C in either 3.0% glutaraldehyde, 0.065 mol
l–1 phosphate buffer, 0.5% tannic acid and 6% sucrose
(Kier, 1985) or modified
Karnovsky's fixative [2.5% paraformaldehyde, 3% glutaraldehyde, 0.065 mol
l–1 phosphate buffer and 2.5% sucrose
(Bozzola and Russell, 1992)]
for 12–24 h. The tissue was rinsed in chilled 0.065 mol
l–1 phosphate buffer for 30 min, dehydrated in a graded
series of ethanol up to 95%, and then embedded in glycol methacrylate plastic
(JB-4 Plus, Polysciences, Inc., Warrington, PA, USA). The tissue blocks were
sectioned at 0.5–1.0 µm in a plane perpendicular to the long axes of
the circular muscle fibres and stained in an aqueous solution of 0.1%
Toluidine Blue and 0.1% sodium borate.
The stained slides were photographed under bright-field microscopy. Both the total cross sectional area of the preparation and the portion occupied by radial muscles were measured using ImageJ (public domain software; National Institutes of Health, USA). We then subtracted the radial muscle area from the total cross-sectional area to get the physiological cross section. The physiological cross section, therefore, included the areas occupied by the myofilaments and the core of mitochondria of the circular muscle fibres.
Determination of thick filament lengths
A small piece of the fixed tissue preparation was post-fixed for 45 min at
4°C in a 1:1 solution of 2% osmium tetroxide and 2% potassium ferrocyanide
in 0.13 mol l–1 cacodylate buffer
(Kier, 1985). The tissue was
rinsed in chilled 0.13 mol l–1 cacodylate buffer for 15 min,
dehydrated in a graded series of acetones and embedded in epoxy resin.
The processes of fixation, dehydration and embedding may cause shrinkage of
cells and connective tissues. A-band lengths of various frog cross-striated
skeletal muscles suffered minimal shrinkage relative to other methods when
fixed in buffered glutaraldehyde and dehydrated in acetone
(Page and Huxley, 1963). Thus,
we adopted their protocol to minimize the effects of tissue processing on
myofilament lengths.
We followed the protocol (Thompson and
Kier, 2006) for measuring thick filament lengths. Briefly,
embedded tissue blocks were sectioned in a plane perpendicular to the
longitudinal axis of the mantle (i.e. parallel to the long axes of the
circular muscles) using a diamond knife. Thick sections (0.5–1 µm)
were cut initially and stained in an aqueous solution of 0.1% Methylene Blue
and 0.1% Azure II. Sections were then examined using bright-field microscopy
to determine if the long axes of the circular muscle fibres were parallel to
the knife edge. Once alignment was achieved, thin sections (silver
interference color) were cut, mounted on grids, and stained with 2% aqueous
uranyl acetate (Bozzola and Russell,
1992) and 0.4% lead citrate
(Venable and Coggeshall,
1965). Thin sections were examined with a Zeiss EM-902
transmission electron microscope and portions of the sections that met our
criteria (see below) were photographed.
Because the circular muscle fibres of squid are fusiform in shape
(Bone et al., 1995) and
obliquely striated (Hanson and Lowy,
1957; Lowy and Hanson,
1962; Millman,
1967), it is often difficult to confirm that the section plane is
parallel to the longitudinal axis of the fibre and thus to ensure that an
individual thick filament remains in the section plane along its entire
length. As described above, an attempt was made to carefully align the section
plane during ultramicrotomy, and care was taken to measure thick filaments
only from fibres (1) in which the diameter of the mitochondrial core remained
constant over the length of the fibre (suggesting that the long axis of the
fibre was parallel to the section plane) and (2) that spanned at least two
bars of a 300 mesh grid. Because of the difficulties associated with section
plane alignment, however, the thick filament lengths we report here may be
underestimates.
The electron micrograph negatives were scanned at 4800 d.p.i. and thick filament lengths measured using ImageJ software. We measured thick filaments from at least five muscle fibres per preparation. We measured a total of 270 thick filaments from SMR fibres and 260 from CMP fibres from 5 animals. The mean thick filament length per fibre type per animal was used for the statistical comparisons.
Determination of cross-sectional areas of individual muscle fibres
To analyze the cellular basis for differences in the mechanical properties
of the SMR and CMP muscle fibres, we measured cross-sectional areas of (1) the
whole fibre, (2) the area occupied by the myofilaments and (3) the
mitochondrial core from transmission electron micrographs of cross sections of
the muscle cells. Because both the SMR and CMP fibres taper longitudinally and
adjacent fibres are not in register, cross sections of the cells reveal fibres
of different sizes and with different relative mitochondrial and myofilament
areas. In an attempt to correct for this variability, we measured the
cross-sectional areas of each cell, its myofilaments, and its mitochondrial
core for every circular fibre visible in the photomicrograph. We presented the
data using box plots to provide a better overview of the variability in the
muscle fibres. We measured approximately 40 SMR and 40 CMP fibres from each of
5 animals.
We also used ImageJ software to estimate the aggregate cross sectional area of the sarcoplasmic reticulum (SR) in each of the muscle cells we measured above. It is important to emphasize that the SR data we report are not estimates of the volume fraction of SR, but are indicative of the relative proportion of SR in each muscle fibre type.
Statistics
The SMR and CMP morphometric and mechanical data were distributed normally.
We used a one-way ANOVA with Tukey's honestly significant difference (HSD)
post hoc test for all comparisons.
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIXReferences |
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The radial muscle fibres occupied a mean of 18.2±2.7% (N=17) of the total cross-sectional area of the muscle preparations. Regression analysis indicated no relationship between the proportion of radial muscles and dorsal mantle length (P=0.94, data not shown) for our sample population.
Mechanical properties of muscle fibres
Using regression analysis (data not shown) we were unable to detect
relationships between dorsal mantle length (DML) of the squid and any of the
following variables: maximum unloaded shortening velocity
(Vmax), peak isometric stress (P0),
twitch:tetanus (Tw:Tt) ratio, the stimulus frequency that elicited maximum
force, or the time course of the contraction. Therefore, we did not segregate
data by body size.
The mean P0 of the SMR preparations was significantly higher than that of the CMP preparations (P<0.001; Fig. 5, Fig. 6A). P0 range was 190–250 mN mm–2 physiological cross section (pcs) and 272–378 mN mm–2 pcs for CMP and SMR preparations, respectively. The stimulation frequency that elicited P0 was significantly higher in SMR (441±37 Hz) preparations than in CMP (400±15 Hz) preparations (P=0.026), but the relevance of this difference is uncertain given that both SMR and CMP preparations were stimulated within 10% of P0 at a stimulation frequency of about 150 Hz. The Tw:Tt ratio was significantly lower in SMR preparations than in CMP preparations (P=0.046; Fig. 5, Fig. 6B).
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All the slack tests resulted in close relationships between step length and force recovery time (see Fig. 7A for two examples). The mean Vmax of SMR fibre preparations was significantly lower than CMP preparations (P=0.0006; Fig. 7B). Vmax range was 3.5–6.8 L0 s–1 and 1.6–3.7 L0 s–1 for the CMP and SMR preparations, respectively.
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The passive tension at L0 was substantially higher in all of the SMR preparations than in the CMP preparations (Fig. 8).
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIXReferences |
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) and
the fast twitch fibres of frogs (Curtin
and Edman, 1994). Both the uncorrected
(Fig. 6A) and corrected
P0 for the SMR fibres are much higher than values reported
for their hypothetical analogues (Mommsen
et al., 1981): the aerobic red muscles of fishes (e.g.
Swank et al., 1997;
Young and Rome, 2001). This is
not surprising given that the thick filaments of the SMR fibres of D.
pealeii are more than two times longer than the thick filaments of the
red muscles of fishes [e.g. carp (Sosnicki
et al., 1991)].
The twitch:tetanus (Tw:Tt) ratio for the CMP fibres of D. pealeii
was identical to that of the CMP fibres of A. subulata
(Milligan et al., 1997) but
the Tw:Tt ratio of the SMR fibres was significantly lower. This implies that
the pattern of activation of the two muscle types may be different in
vivo. Circumstantial evidence suggests that the SMR fibres are innervated
by the non-giant motor system (Prosser and
Young, 1937; Young,
1938; Brown et al.,
1991). The CMP fibres of the market squid Loligo
opalescens are innervated by both the giant and non-giant systems
(Otis and Gilly, 1990),
although it remains unclear if each CMP muscle cell receives dual innervation
or if populations of CMP fibres are innervated by one system or the other.
There was an approximately twofold difference in shortening velocity
between the SMR and CMP fibres. Although shortening velocity varies with the
load on the muscles and we have no information on the loads experienced in the
mantle, it is likely that the CMP fibres shorten more rapidly than the SMR
fibres in vivo. The Vmax we found for the CMP
fibres is comparable to that of another loliginid squid, Alloteuthis
subulata (Milligan et al.,
1997), assuming that the Q10 of squid muscle is about
2.0.
Despite the significantly greater area of sarcoplasmic reticulum (SR)
visible in the cross sections of the CMP muscle fibres we found no differences
in the time course of muscle contraction during brief tetanus
(Table 1) or in the minimum
current required to elicit maximal contraction between the two preparation
types. Although the volume fraction of SR present in a muscle cell correlates
with fibre type in vertebrates (Eisenberg,
1983) and relaxation rate, a thorough analysis of E–C
coupling is required before a complete comparison of SMR and CMP fibres can be
made. Fast Na+ channels have been found putatively in the CMP
fibres of L. opalescens (Gilly et
al., 1996) and in A. subulata
(Rogers et al., 1997), but it
is unknown if they are present in the SMR fibres as well.
It is noteworthy that none of the temporal aspects (TL,
TP, T50) that we measured differed
between the two fibre types. Studies of D. pealeii, L. opalescens and
the brief squid Lolliguncula brevis indicate that the period of the
jet changes little as swimming speed increases
(O'Dor, 1988;
Anderson and DeMont, 2000;
Bartol, 2001b). As a squid jets
faster, the refilling times become shorter, presumably as radial muscle
activity increases to speed refilling
(Gosline et al., 1983), and
the amplitude of mantle contraction may increase
(Anderson and DeMont, 2000),
but the time course of mantle contraction does not change dramatically. Thus,
the similarity in the temporal aspects of isometric contraction that we noted
appears consistent with mantle kinematics.
Passive tension and effect of the tunic
We were unable to remove the outer tunic from the SMR preparations and it
is possible that this thin (ca. 25 µm) layer of collagen fibres affected
passive tension in the preparations, Vmax, and the
temporal aspects of isometric contraction. The passive tension at
L0 was substantially higher in all of the SMR preparations
compared with the CMP preparations (Fig.
8). Examination of the SMR preparations with polarized light
microscopy revealed that the long axes of the collagen fibres in the outer
tunic were approximately 60° to the long axes of the circular muscle
fibres (data not shown). Because there is no discernable difference in the
distribution of intramuscular connective tissue fibres across the mantle wall
(Thompson and Kier, 2001), we
attribute the difference in passive tension to the presence of the tunic.
Although the tunic may have contributed to passive tension, there are several
reasons why it is unlikely to have affected Vmax or the
temporal aspects of isometric contraction. First, for three of the SMR
preparations we conducted slack step tests at preparation lengths that were
shorter than L0. At these shorter lengths, passive tension
was zero and the mean Vmax of the three SMR fibres was
little different from the Vmax at L0.
Second, we had numerous preparations that contained the tunic as well as both
SMR and CMP fibres. In these mixed fibre preparations (which were excluded
from all of the other analyses), Vmax varied inversely
with the percentage of SMR fibres in the preparation (Pearson's
R=–0.6, P=0.01, N=20), despite the presence
of the tunic. Therefore, it is unlikely that elastic recoil of the tunic
fibres affected Vmax. Third, there were no significant differences
in the temporal aspects of isometric contractions between the mixed SMR/CMP
preparations and either the `pure' SMR or CMP preparations (data not
shown).
Do ultrastructural differences explain mechanical differences?
In striated muscles including, presumably, obliquely striated circular
muscles, thick filament length is proportional to the peak isometric stress
(P0) of the fibre (e.g.
Josephson, 1975;
Kier and Curtin, 2002). Thus,
the longer thick filaments of the SMR fibres should increase the
P0 produced relative to the CMP fibres. Consistent with
this hypothesis, we found that the P0 of SMR fibres was,
indeed, significantly greater than that of the CMP fibres. Because maximum
unloaded shortening velocity (Vmax) is inversely
proportional to thick filament length (e.g.
Josephson, 1975;
Kier and Curtin, 2002), the
longer thick filaments of SMR fibres should be correlated with slower
Vmax. Consistent with this hypothesis, we found that
Vmax was significantly slower in the SMR fibres.
But do the differences in thick filament length alone explain the differences in the contractile properties of the SMR and CMP circular muscle fibres of D. pealeii? The thick filaments of the SMR fibres are about 1.75 times longer than those of CMP fibres (Figs 2, 3). Thus, if other aspects of the two fibre types are the same, and if the relationship between thick filament length and isometric stress is linear, the P0 of SMR fibres should be 1.75 times greater than the P0 of CMP fibres. The P0 of the SMR fibres was approximately 1.5 times greater (Fig. 6A), but if we correct for differences in the size of the core of mitochondria, the P0 is about two times greater. By similar reasoning, the Vmax of the SMR fibres should be 1.75 times slower than the CMP fibres, and it is approximately two times slower (Fig. 7B).
We cannot exclude the possibility that different isoforms of the
myofilament lattice proteins are expressed in SMR and CMP fibres. The
obliquely striated muscles of squid have received scant attention relative to
other striated muscles and little is known about the isoforms of contractile
proteins present in the mantle. Matulef and colleagues
(Matulef et al., 1998) found
evidence for two isoforms (`A' and `B') of myosin heavy chain in the funnel
retractor muscle of D. pealeii that may be splice variants of a
single gene. The putative splice variants differ in the amino acid sequence of
the ATP binding region (Matulef et al.,
1998); thus, the splice variants may affect Vmax. There
is no evidence that both variants are expressed in the mantle, though RT-PCR
analysis of the arms and tentacles of D. pealeii indicated that one
isoform (`A') composes more than 95% and 90% of the total myosin heavy chain
in the arms and tentacles, respectively
(Kier and Schachat, 2008).
Limited information about a few other myofilament lattice proteins involved in
shortening is available. Konno (Konno,
1978) purified myosin, tropomyosin and three troponins from the
mantle of an ommastrephid squid (Todarodes pacificus). Unfortunately,
the methods used by Konno were inappropriate to determine if isoforms of any
of the isolated proteins were present. Ojima et al. determined the amino acid
sequence of troponin C in T. pacificus, but did not find isoforms
(Ojima et al., 2001).
Additional work is still needed to determine the full extent of specialization
between CMP and SMR fibres. We are currently studying potential myosin heavy
chain isoforms in the mantle. Nevertheless, our results are consistent with
the prediction that structural differences play a primary role in determining
the differences in the mechanical properties of the two types of circular
muscle fibres.
Functional significance of circular muscle specialization
The differences in mechanical properties of the two types of circular
muscle fibres may have a number of significant effects on mantle kinematics
and jet locomotion.
Muscle `gears'
The SMR and CMP fibres follow parallel trajectories through the mantle. In
this way, there does not appear to be an `architectural gear ratio'
(sensu Brainerd and Azizi,
2005) between the SMR and CMP fibres as there is between the red
and white muscle fibres of fishes
(Alexander, 1968;
Rome and Sosnicki, 1991;
Wakeling and Johnston, 1999)
and the various layers of hypaxial muscle in Siren lacertina
(Brainerd and Azizi, 2005).
Nevertheless, the twofold difference in P0 and
Vmax between the SMR and CMP fibres suggests that the
mantle does have at least two muscle `gears'. Simultaneous mantle kinematics
and electromyographic (EMG) recordings in the brief squid Lolliguncula
brevis are consistent with the idea that the two fibre types are
differentially recruited as swimming speed increases. Bartol
(Bartol, 2001a) observed no CMP
electrical activity at <1 DML s–1, both SMR activity and
sporadic CMP activity at 1–3 DML s–1, and continual CMP
activity at >3 DML s–1. Thus, the aerobic SMR and
anaerobic CMP (Bone et al.,
1981; Mommsen et al.,
1981) fibres may represent low and high `gears', respectively.
Strain and strain rate predictions from a simple mantle model
Consideration of the geometry of the mantle shows that circular muscle
fibre strain and strain rate vary as a function of location in the mantle
wall; strain and strain rate increase from the outer (i.e. the side covered by
the skin) to the inner (i.e. the side in contact with the mantle cavity)
surface. This transmural gradient arises because (1) the mantle is circular in
cross section, (2) the mantle wall is constant in volume
(Ward, 1972), and (3) the
length of the mantle either does not increase when the circular muscles
contract (Ward, 1972) or
increases by less than 5% (Packard and
Trueman, 1974). As the circular muscle fibres contract, therefore,
the mantle not only decreases in diameter but the mantle wall thickness
increases (Fig. 9). Transmural
variation in strain and strain rate has several interesting implications for
mantle muscle function. Do SMR and CMP fibres near the outer surface of the
mantle operate on a different portion of the length–tension curve than
those near the inner edge? Within the CMP fibres, does power output vary
across the mantle wall? Although our data do not permit direct answers to
these questions, modeling of the dimensional changes of the mantle during
jetting allows prediction of mantle muscle strain rate and strain and thus
provides insight.
|
To explore the relationship between the transmural gradient of strain and
strain rate and the contractile properties of the CMP and SMR circular muscle
fibres, we constructed a simple model based on a transverse slice of the
mantle. The dimensions of the model slice were based on measurements of mantle
diameter and mantle wall thickness at 
DML from an adult D.
pealeii (DML, 150 mm) anesthetised in a 1:1 solution of 7.5%
MgCl2:seawater (Messenger et al., 1983). The anesthetic relaxed the
circular muscles, resulting in mantle dimensions similar to those observed
just prior to the start of the exhalant phase (i.e. the portion of the jet in
which water is forced out of the funnel by contraction of the circular
muscles) of the jet (see Thompson and
Kier, 2001).
We selected three jetting speeds for comparison: slow (
0.5 DML
s–1), intermediate (2 DML s–1), and
fast (an escape jet at 12 DML s–1). We do not have
coordinated mantle kinematics and EMG data for D. pealeii, but in
L. brevis the SMR fibres alone are active at slow swimming speeds
<1 DML s–1, while the CMP fibres are active sporadically
at intermediate speeds (1–3 DML s–1) and constantly at
high speeds [>3 DML s–1
(Bartol, 2001a)]. We presume
that the speeds we selected, then, represent situations in which power for the
jet is provided by the SMR fibres alone (slow), both the SMR and CMP fibres
(intermediate), and the CMP fibres alone (fast). We measured the amplitude of
mantle contraction and the period of the exhalant phase of the jet during
slow, intermediate and escape jets from the high-speed (250 frames
s–1) video sequences of another specimen of D.
pealeii (DML, 152 mm). During the exhalant phase of the jet, the diameter
of the mantle decreased 5% over 0.3 s, 12% over 0.25 s and 25% over 0.15 s,
for the slow, intermediate and escape jets, respectively (J. T. Thompson, P.
S. Krueger and I. K. Bartol, in preparation). Hyperinflation
(Gosline et al., 1983) of the
mantle was not apparent in the jets we evaluated.
We combined the morphological and kinematics data to calculate the mantle
wall thickness at the end of a jet (see Appendix and
Fig. 9). We then calculated
circumferential strain and strain rate
(
in mantle circumference lengths
s–1) at the outer and the inner edges of the mantle wall. The
results of the calculations are listed in
Table 2 and the initial
conditions and values used for the calculations are provided in
Table 3. The model predicts
that the circular muscle fibres near the inner surface of the mantle wall
experience 1.3- and 1.4-fold higher strain and strain rates during slow
jetting and escape jetting, respectively, than fibres near the outer surface.
The model also shows that the greater the thickness of the mantle wall
relative to the radius of the mantle, the greater the difference in transmural
strain and strain rate for the inner versus the outer surface (see
Appendix).
|
|
The model also predicts that both the SMR and CMP circular muscle fibres
experience high strains at intermediate and higher jetting speeds
(Table 2). The cross-striated
muscle fibres of the vertebrates appear to experience relatively low strains,
especially during locomotion (Burkholder
and Lieber, 2001). For example, the red muscles of carp experience
maximum strain of 0.14 during sustainable swimming speeds, and the strain of
white muscles during escape responses is 0.18
(van Leeuwen et al., 1990;
Rome and Sosnicki, 1991).
Moreover, these strains are nearly centered on the fibre length
(L0) that produces the highest force
(Rome and Sosnicki, 1991). One
problem with our model, and with studies of obliquely striated muscles in
general, is that we cannot yet relate mantle circumference to
L0 and, thus, cannot determine where on the
length–tension curve the different muscle fibres operate. This issue is
currently under investigation.
Milligan et al. (Milligan et al.,
1997) calculated power output from the force–velocity
relationship of the CMP fibres of the loliginid squid Alloteuthis
subulata. They noted that peak power output occurred at
V/Vmax of about 0.38 and that the fibres produced
high power over a fairly broad range of lengths, particularly compared to the
cross striated fibres of a variety of vertebrates
(Lännergren et al., 1982;
Curtin and Woledge, 1988;
Rome and Sosnicki, 1990;
McLister et al., 1995). We
estimated V/Vmax by using the strain rates
() calculated from the model as a
proxy for the in vivo shortening velocity (V) of the
circular fibres and the mean Vmax data from
Fig. 7B. If peak in
vitro power at a V/Vmax of 0.38 occurs also
in the SMR and CMP fibres of D. pealeii, the model predicts that SMR
fibre power output peaks near the likely recruitment speed of the CMP fibres
(Table 2). The model also
predicts that the CMP fibres generate virtually no power for slow jetting
while the SMR fibres are too slow to generate power for escape jets. The
transmural variation in strain and strain rate suggests that different regions
of the mantle produce different amounts of work during locomotion (see
Higham et al., 2008).
Note that our model does not consider the hyperinflation of the mantle that
often occurs during escape jets (Gosline
et al., 1983; Thompson and
Kier, 2001). Because hyperinflation of the mantle increases muscle
fibre length before contraction, strain is likely to be even greater during
escape jets.
Why do the SMR fibres have long thick filaments?
The muscular mantle wall of an adult D. pealeii can be over 5 mm
thick, yet the combined cross-sectional area of the two SMR fibre layers
represents only 4–6% of the total cross section of the mantle wall.
Therefore, the loads experienced by the SMR fibres during hovering and slow
jetting must be high, particularly because the CMP fibres are likely quiescent
during these behaviours (Bartol,
2001a). Longer thick filaments
(Josephson, 1975;
Kier and Curtin, 2002) provide
a means to increase the stress generated by the SMR fibres.
During hovering and slow swimming, squids undulate or flap their fins to
generate thrust while also using the pulsed jet. The fins of squids, including
D. pealeii, originate on cartilages embedded within and supported by
the mantle musculature, and the mantle muscle and connective tissue fibres
must resist the loads generated by the fins
(Kier, 1989). Because the SMR
fibres alone appear to be electrically active during hovering and slow jetting
(Bartol, 2001a), the SMR fibres
must not only provide power for jetting but also, in combination with mantle
connective tissues, maintain mantle wall stiffness to support the fins. As
highlighted by Mommsen and colleagues
(Mommsen et al., 1981), the
location of the two layers of the SMR fibres on the inner and outer surfaces
of the mantle is ideal for pressurizing the entire mantle. Perhaps the longer
thick filaments and corresponding higher P0 of the SMR
fibres are as important for maintaining mantle wall stiffness for fin support
as for generating jet thrust at low swimming speeds. In this context, it is
interesting that the timing of an ontogenetic increase in the thick filament
length of the SMR fibres in the loliginid squid Sepioteuthis
lessoniana coincides with a dramatic ontogenetic increase in the relative
size of the fins (Thompson and Kier,
2006) (J. T. Thompson, unpublished observations).
Muscle specialization in squids
The use of mitochondria-rich fibres for slow swimming may be common in
cephalopod muscle fibres. Small bundles of them are found in the transverse
muscles of the fins of the Caribbean reef squid Sepioteuthis
sepioidea and the European cuttlefish Sepia officinalis
(Kier, 1989). Simultaneous
recordings of electromyography and fin kinematics in S. officinalis
suggested that the mitochondria-rich transverse fibres were used for
continuous, low-amplitude fin movements while the mitochondria-poor fibres
were recruited during higher amplitude fin beating
(Kier et al., 1989).
Different circular muscle fibre types may not, however, be found in the
mantles of all squids. A single type of circular muscle fibre with a small
core of mitochondria, resembling the CMP fibres, is present in the mantles of
many of the gelatinous-bodied mesopelagic and bathypelagic species (J. T.
Thompson, in preparation). The majority of these animals rely primarily on
fins for locomotion (Vecchione and Roper,
1991; Vecchione et al.,
2002) and thus the factors that favored the evolution of CMP and
SMR circular muscle fibres may not apply for these animals.
Mapping the distribution of the two circular muscle fibre types onto recent
coleoid cephalopod phylogenies (Young and
Vecchione, 1996; Carlini et
al., 2000; Akasaki et al.,
2006) suggests that the SMR/CMP distinction arose independently in
several families of squids (J. T. Thompson, in preparation). Thus, study of
the SMR and CMP circular muscle fibres of the mantle may provide an excellent
opportunity to examine not only muscle mechanics but also the evolution of
specialization in an obliquely striated muscle.
|
APPENDIX |
|---|
|
TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIXReferences |
|---|
)]:
 | (A1) |
) and that the
volume of the mantle tissue is constant. 
out) at the outer
edge of the mantle wall:
 | (A2) |
 | (A3) |
in) at the inner
edge of the mantle wall:
 | (A4) |
in
increasing as ri:ti decreases. In
other words, the greater the relative thickness of the mantle wall, the
greater the transmural difference in strain and strain rate. )
has a minimal effect on the differences in transmural strain and strain rate.
We calculated the volume (v) of the mantle tissue as:
 | (A5) |
)
is proportional to the square of the thickness of the mantle wall
(t), Eqn A5 can be
rewritten as:
 | (A6) |
) gives:
 | (A7) |
LIST OF ABBREVIATIONS
|
Acknowledgments |
|---|
|
References |
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|
TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONAPPENDIXReferences |
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