The tube feet of sea urchins and sea stars contain functionally different mutable collagenous tissues
1 Académie Universitaire Wallonie-Bruxelles, Université de
Mons-Hainaut, Laboratoire de Biologie marine, 6 Avenue du champ de Mars, 7000
Mons, Belgium
2 Académie Universitaire Wallonie-Bruxelles, Université Libre
de Bruxelles, Laboratoire de Biologie Marine, 50 Avenue F.D. Roosevelt, 1050
Brussels, Belgium
Author for correspondence (e-mail:
Patrick.Flammang{at}umh.ac.be)
Accepted 14 April 2005
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Summary |
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Key words: connective tissue, mechanical property, ultrastructure, Asteroidea, Echinoidea
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Introduction |
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MCTs are composed of collagen fibres with varying sizes, conformation and
spatial arrangement, each fibre consisting of numerous spindle-shaped collagen
fibrils (Trotter et al., 2000;
Wilkie et al., 2004
). An
elastomeric network of fibrillin microfibrils surrounds and separates the
collagen fibres (Trotter et al.,
2000
; Wilkie et al.,
2004
). This microfibrillar network maintains the organization of
collagen fibrils as they slide with respect to one another during lengthening
and shortening of the tissue; it may also provide long-range restoring force
(Thurmond and Trotter, 1996
;
Trotter et al., 2000
). Both
collagen fibrils and microfibrils are interconnected by a matrix of
proteoglycans and glycoproteins (Trotter
et al., 2000
; Wilkie et al.,
2004
). Furthermore, MCTs always contain a special type of cell,
the so-called juxtaligamental cells, which are characterized by the presence
in their cytoplasm of numerous electron-dense, membrane-bound granules. Nerve
terminals and axon-like profiles have often been observed in contact with, or
in the vicinity of, these secretory cells
(Wilkie, 1996
).
Juxtaligamental cells are believed to contain molecules that regulate
interactions between the collagen fibrils
(Trotter and Koob, 1995
;
Koob et al., 1999
;
Trotter et al., 2000
). The
temporary nature of these interactions accounts for the capacity of MCTs to
switch reversibly from a stiff to a compliant state
(Tipper et al., 2003
;
Wilkie et al., 2004
).
Tube feet are the external appendages of the echinoderm water-vascular
system and present a remarkable diversity of forms and functions
(Flammang, 1996). Although it
has often been suggested that an MCT is present in echinoderm tube feet
(Florey and Cahill, 1977
;
Motokawa, 1984
;
Byrne, 1994
;
Flammang, 1996
), this has never
been demonstrated experimentally. In sea urchins and sea stars, tube feet are
discending (i.e. they consist of a proximal extensible stem and a distal
disc-shaped extremity) and are involved in attachment to the substratum and
locomotion. In the present study, the material properties of the tube foot
stem of the echinoid Paracentrotus lividus and the asteroid
Marthasterias glacialis were investigated in order to search for
evidence of the presence of an MCT.
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Materials and methods |
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Preparation of specimens and bathing solutions
Two experiments were conducted on both species to establish the tensile
properties of their tube feet under various conditions. In the first, each
individual was dissected under water to prevent tissue desiccation, and the
five ambulacra were separated into five fragments, each representing a fifth
of the test in sea urchins or one arm in sea stars. Each ambulacrum was then
incubated for 1 h at room temperature and under slight agitation in one of the
five following solutions: (1) ASW (artificial seawater made up of 445 mmol
l-1 NaCl, 60 mmol l-1 MgCl2, 10 mmol
l-1 KCl, 2.4 mmol l-1 NaHCO3, 10 mmol
l-1 Hepes and 10 mmol l-1 CaCl2; pH 7.8); (2)
ASW-EGTA (in which CaCl2 was replaced by 2.5 mmol l-1
EGTA); (3) ASW-EGTA-TX (in which 1% Triton-X100 was added to the ASW-EGTA
solution); (4) ASW-TX (ASW solution with 1% Triton-X100); and (5) DW
(deionised water). The mechanical tests were performed in the solutions and,
for each ambulacrum, 10 adoral tube feet from the sea urchins or 10 mid-arm
tube feet from the sea stars were tested. The whole protocol was repeated with
three different individuals of each species. For two individuals of P.
lividus, the ambulacra that had been bathed in ASW-EGTA were returned to
ASW and incubated for an additional 1 h (ASW-EGTA ASW). Mechanical
tests were repeated on 10 adoral tube feet per ambulacrum.
In the second experiment, individuals from both species were anaesthetized
by incubation in ASW containing 0.1% propylene phenoxetol (ASW-PP) for 1 h at
room temperature. This anaesthetic was used to prevent non-specific,
manipulation-induced stiffening of the connective tissue
(Motokawa and Tsuchi, 2003). It
was preferred to the commonly used MgCl2 because the latter
modifies the ionic environment of the tissues and thus affects connective
tissue mechanical properties (Wilkie,
1996
; Santos and Flammang,
2005
). Subsequently, individuals were dissected in the ASW-PP
solution, and the ambulacra were incubated for an additional 1 h either in the
ASW-PP solution or in the same solution containing 1% Triton-X100 (ASW-PP-TX).
As in the first experiment, three individuals per species and 10 tube feet per
ambulacrum were tested.
Measurement of mechanical properties
Mechanical traction tests were performed with a Mecmesin-Versa Test
motorized stand fitted with an electronic force gauge that measures forces up
to 2.5 N (Mecmesin AFG 2.5 N, Horsham, UK), connected to a computer collecting
the data. The precision of the tensile force measurements was 0.0005 N.
Ambulacra were placed upside down, and a small surgical clip was attached to
one tube foot in the portion of the stem just under the disc and then pulled
perpendicular to the specimen (in the direction of the natural extension) at a
constant rate of 25 mm min-1
(Santos and Flammang, 2005),
until failure. Failure never occurred at the clip. Before pulling the tube
foot, the initial length of the stem (distance between the base of the tube
foot and the clip) was measured at the point at which the force started to
increase and reached 0.0015 N. The initial length of the tube foot, together
with the time required to break the tube foot at a constant extension rate,
was subsequently used to calculate the stem final length at failure. From
these data, several material properties were calculated: the true strain, the
true stress, the tangent modulus of elasticity and the breaking energy density
(Fig. 1). True values of strain
and stress were used instead of nominal values because of the high extensions
observed for both species' tube feet
(Shadwick, 1992
).
|
![]() | (1) |
The true stress () was calculated as the product of the extension
ratio and tensile stress [force (F) divided by cross-sectional area
(S)]. It is expressed in N m-2 or Pa (Pascal). The maximum
value of stress (at breaking force) is an indicator of the strength of the
tube foot:
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The connective tissue cross-sectional area was used for the calculations of
the true stress instead of the stem wall cross-sectional area because this
tissue appears clearly as the layer bearing most of the load exerted on a tube
foot. Indeed, Florey (cited in Florey and
Cahill, 1977) reported that the connective tissue resists
extensions with forces bigger by one or two orders of magnitude than those
developed by the muscle when stimulated to maximal contraction. The
ultrastructure of the epidermis and nerve plexus suggests that they are even
weaker.
The modulus of elasticity (E) was calculated as the tangent to the
slope of the stress-strain curve. It is a measure of the tube foot stiffness
and is also expressed in Pa:
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Finally, we calculated the breaking energy density as the integral of force multiplied by extension (i.e. the area under a force-extension curve) divided by the volume of stem connective tissue (calculated as the product of tube foot initial length multiplied by mean connective tissue cross-sectional area). This parameter is an indicator of the energy needed to extend and break the tube foot. It is also referred to as the toughness and is expressed in J m-3.
For both species, the results were analysed in order to look for significant differences in the mechanical properties of the tube feet between different individuals and between the different bathing solutions. Data were analysed by two-way analysis of variance (ANOVA) followed by the multiple comparison test of Tukey. When necessary, logarithmic transformation was used to achieve homoscedasticity. The variability explained by each factor is derived from the sum of squares.
Morphological analyses
The mean values of the cross-sectional areas of each tissue layer of the
tube foot stem from each species were obtained using tube feet dissected from
the animals used for the mechanical tests. For both species, 10 tube feet were
cut off the ambulacra that remained in ASW and were fixed in Bouin's fluid for
24 h. They were subsequently dehydrated in a sequence of graded ethanols,
embedded in paraffin wax using a routine method, and cut transversely into 7
µm-thick sections with a Microm HM 340 E microtome. The sections were
mounted on clean glass slides and stained with Masson's trichrome.
Measurements were made with a Leica Laborlux light microscope equipped with a
graduated eyepiece on sections taken halfway between the base and the disc of
the tube foot. A mean value of the connective tissue cross-sectional area was
calculated from measurements of connective tissue diameter and thickness made
on 10 tube feet. This mean value was used in the calculation of stem
mechanical properties for the particular animal from which the tube feet were
dissected.
For transmission electron microscopy (TEM), tube feet from both species were fixed for 3 h at 4°C in 3% glutaraldehyde in cacodylate buffer (0.1 mol l-1, pH 7.8; adjusted to 1030 mOsm l-1 with NaCl). Then they were rinsed in cacodylate buffer, post-fixed for 1 h in 1% OsO4 in the same buffer, dehydrated in graded ethanols, and embedded in Spurr resin. Transverse ultrathin sections (70-80 nm in thickness) were cut with a Leica UCT ultramicrotome equipped with a diamond knife, collected on copper grids and stained with uranyl acetate and lead citrate. Ultrathin sections were observed with a Zeiss Leo 906E transmission electron microscope, and morphometric measurements were obtained using analySIS® software (Soft Imaging System GmbH, Münster, Germany).
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Results |
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The TEM study revealed several ultrastructural differences in the
connective tissue layer of sea urchin and sea star tube feet. In both species,
this layer was organized into an outer sheath of longitudinally orientated
collagen fibres and an inner sheath of helicoidally orientated fibres (see
also Flammang, 1996). The outer
sheath was almost 20 times thicker than the inner one in the tube feet of
P. lividus, but the two sheaths were similar in thickness in those of
M. glacialis (compare Fig.
2A,B). Within the outer sheath of sea urchin tube feet, the
collagen fibres were densely packed and embedded in an electron-lucent matrix
(Fig. 2C,E). Each fibre
consisted of fibrils with a maximum diameter of 113±32 nm
(N=20) and separated from each other by 20-40 nm. Within the outer
sheath of sea star tube feet, on the other hand, the fibres were more
dispersed, being enclosed and separated by an electron-dense network of
microfibrils (Fig. 2D,F,G).
Each fibre contained fibrils with a maximum diameter of 232±28
nm(N=20) and separated from each other by 10-30 nm.
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Mechanical properties of the stem
In the first experiment, the effect of five solutions on the mechanical
properties of tube feet was tested. Artificial seawater (ASW) was used as a
standard solution. ASW-EGTA was used as a calcium-free medium (EGTA is a
calcium chelator that removes the endogenous calcium from the tissues). The
other three solutions were treatments that disrupted cellular membranes: two
made use of the non-ionic detergent Triton-X100, either in the presence
(ASW-TX) or absence (ASW-EGTA-TX) of calcium, and the third, deionised water
(DW), worked by osmotic shock.
Fig. 3 represents examples of typical J-shaped stress-strain curves obtained for sea urchin and sea star tube feet in three of the five solutions. The tube foot stems of these two echinoderm species seem to have different mechanical properties, echinoid tube feet being apparently stronger, stiffer and tougher than asteroid tube feet.
|
|
In both species, there was no significant difference in tube foot extensibility between samples incubated in ASW-EGTA and ASW (Fig. 4A,F). However, the treatment with ASW-EGTA significantly decreased the tensile strength, stiffness and toughness of the tube feet in comparison with ASW (Fig. 4B-E,G-J). The tube foot plasticization due to the absence of calcium was fully reversed when sea urchin ambulacra were put back and incubated in ASW after their bath in ASW-EGTA (ASW-EGTA >> ASW) (Fig. 5). Sea urchin tube feet showed similar extensibility and initial stiffness in the three cell-disrupting solutions, with values comparable to those obtained in ASW (Fig. 4A,C). By contrast, the cell-disrupting solutions significantly increased tube foot strength and final stiffness in comparison with tissues incubated in ASW, and a fortiori in comparison with tissues incubated in ASW-EGTA (Fig. 4B,D). Tube foot toughness was significantly higher in ASW-EGTA-TX, but not in the other cell-disrupting solutions, than in ASW (Fig. 4E). However, stem initial stiffness and toughness were significantly higher in the cell-disrupting solutions than in ASW-EGTA (Fig. 4C,E). In sea stars, tube foot extensibility, strength, final stiffness and toughness were not significantly affected by the three cell-disrupting solutions in comparison with ASW but were significantly affected in comparison with ASW-EGTA (Fig. 4F,G,I,J). Tube foot initial stiffness was significantly higher in the three cell-disrupting solutions than in ASW and ASW-EGTA (Fig. 4H).
|
|
In the second experiment, tube feet were anaesthetized in ASW with 1% propylene phenoxetol and then tested in the absence (ASW-PP) and the presence (ASW-PP-TX) of a cell-disrupting agent. In this experiment, the anaesthetising agent was used to make sure all the tube feet were in the same relaxed state at the beginning of the mechanical tests.
The two-way analysis of variance of the whole data set for tube foot material properties (Table 2) showed that, in sea urchins, individuals influence only extensibility, explaining 10% of its variability, whereas solutions explain the largest proportion of the overall variability in tube foot mechanical properties (15-60%). No interactions between the two factors were observed. In sea stars, solutions accounted for 41.3 and 13.7% of the variability in tube foot extensibility and final stiffness, respectively, but did not influence the other properties. The variability in the latter was partly explained (10-25%) by the individuals. Once again, no significant interactions were found between the two factors.
As in the first experiment, sea urchin tube feet showed again higher tensile strength, final stiffness and toughness in the cell-disrupting solution (Fig. 6B,D,E). However, in this experiment, the presence of the cell-disrupting agent also increased the extensibility and the initial stiffness of anaesthetized tube feet (Fig. 6A,C). In sea stars, there was no significant difference between tube feet incubated in the two solutions except for stem extensibility and final stiffness, which decreased in the cell-disrupting solution (Fig. 6F-J).
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Discussion |
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There are, however, several differences between the tube feet of sea
urchins and sea stars as far as morphology and mechanics are concerned. In sea
stars, the connective tissue cross-sectional area represents only 10% of
the stem wall cross-sectional area as opposed to
40% in sea urchins.
Another major morphological difference lies in the proportion between the
outer connective tissue sheath, in which the collagen fibres are
longitudinally orientated (Nichols,
1966
; Florey and Cahill,
1977
), and the inner sheath in which the fibres are arranged as a
crossed-fibre helical array (Skyler
McCurley and Kier, 1995
). In Paracentrotus lividus, the
former is
20 times thicker than the latter, while in Marthasterias
glacialis they are of equal importance. Mechanically, on the other hand,
echinoid tube feet are stronger, stiffer and tougher than asteroid tube feet.
All these differences probably reflect variations in the functioning of the
tube feet. In addition to their role as a holdfast, tube feet in both sea
urchins and sea stars are involved in locomotion. Echinoid tube feet function
as traction systems, attaching to the substratum and contracting, hence
pulling the sea urchin, whereas asteroid tube feet act as struts that are used
as levers (Lawrence, 1987
). A
much more important protraction force is presumably needed in the latter case
because the tube feet not only extend to reach the substratum but also lift
and support the weight of the animal during locomotion. This protraction force
is achieved by an increase in hydrostatic pressure within the water-vascular
fluid, and it is the function of the inner connective tissue sheath to resist
the hoop stress (which tends to increase diameter) induced by this pressure
(Skyler McCurley and Kier,
1995
; Vogel,
2003
). It is not surprising, therefore, that this sheath is more
developed in the tube foot stem of M. glacialis than in P.
lividus. As the collagen fibres in this sheath are likely to be disposed
at a high angle to the longitudinal axis of the stem (in the asteroids
Luidia clathrata and Astropecten articulatus this angle is
67° in fully extended tube feet;
Skyler McCurley and Kier,
1995
), it is unlikely that they resist longitudinal stress, this
being the function of the outer sheath of collagen fibres. If this is the
case, our values of stem tensile strength and stiffness are underestimated as
they were calculated using the total cross-sectional area of the whole
connective tissue layer and not the cross-sectional area of the outer sheath
(see Eqns 2,
3). According to the proportion
of both sheaths in the two species, this underestimation is more important for
sea star tube feet, meaning that their actual values of strength and stiffness
would therefore be much closer to those calculated for the sea urchin tube
foot stem. However, estimating the relative proportions of both connective
tissue sheaths is difficult in light microscopy, and processing every tube
foot for TEM is impracticable. As only intraspecific comparisons have been
made in this study, the cross-sectional area of the whole connective tissue
layer has been used for calculations of mechanical properties, and the
comparisons between the different individuals and treatments used remain
valid.
In the tube feet of both species, the outer connective tissue sheath
contained a large amount of cell processes with electron-dense granules, which
are remarkably similar in appearance to the juxtaligamental cells always
present in echinoderm MCTs (Wilkie,
1996). This is initial evidence for the presence of an MCT in sea
urchin and sea star tube feet because there is no known MCT that lacks these
cells, whereas they are absent from the few definitely non-mutable collagenous
structures examined (Wilkie,
2002
; Wilkie et al.,
2003
). There are, nevertheless, differences between sea star and
sea urchin tube feet. In the former, two populations of juxtaligamental-like
cell processes may be distinguished on the basis of the size of their
secretory granules, while in the latter, only one population occurs. The
co-occurrence of two or more populations of granule-containing cells has been
described in many echinoderm MCTs (Wilkie,
1996
).
Although morphology strongly suggests the presence of an MCT in sea urchin
and sea star tube foot stems, only mechanical testing can demonstrate this
presence unequivocally. In our first experiment, the tube foot stems of P.
lividus and M. glacialis were tested in five treatments known to
influence the physiological state and thus the mechanical properties of
different MCTs (see Wilkie,
2002 for a review). Mechanical measurements were performed on tube
feet whose connective tissue was in its natural, standard state (ASW),
depleted of calcium (ASW-EGTA) or exposed to the contents of disrupted cells
in the absence (ASW-EGTA-TX; DW) and presence (ASW-TX) of calcium. As
previously observed in other MCTs, tube feet from both species became
compliant when in a state of calcium depletion, indicating that their
mechanical properties are influenced by calcium concentration
(Wilkie, 1996
;
Wilkie et al., 2004
). Indeed,
previous studies suggested that calcium depletion can inhibit
calcium-dependent macromolecular associations that regulate the viscosity of
the matrix (Motokawa, 1988
;
Wilkie, 1988
). Although this
effect is non-specific (it was also observed in non-mutable collagenous
structures; Wilkie et al.,
2003
), it mimics the soft state of MCTs
(Motokawa and Tsuchi, 2003
).
Cell-disrupting treatments, on the other hand, induce a stiffening response in
the two most studied MCTs, i.e. the sea urchin spine ligament
(Szulgit and Shadwick, 1994
)
and the holothuroid dermis (Trotter and
Koob, 1995
). An identical response was observed in sea urchin tube
feet treated with the three cell-disrupting treatments, their stems being
consistently stronger and stiffer (final stiffness) in these solutions than in
ASW. These solutions, however, had no effect on stem extensibility, initial
stiffness and toughness. On the other hand, all mechanical properties (except
extensibility) were significantly increased when the tube feet were treated
with cell-disrupting solutions in the absence of calcium in comparison with
the treatment in ASW-EGTA. This is different from what occurs in the echinoid
compass-rotular ligament, a non-mutable collagenous tissue in which mean
breaking load was not significantly different in ASW-EGTA and in DW
(Wilkie et al., 2003
).
Cell-disrupting agents had a different action on sea star tube feet. Indeed,
tube foot stems of M. glacialis bathed in these solutions showed
similar extensibility, strength, final stiffness and toughness as those
incubated in ASW. Only the initial stiffness increased significantly after
cell perforation. However, similar to what occurred in P. lividus,
all stem mechanical properties were significantly affected by incubation in
the calcium-free cell-disrupting solutions in comparison with incubation in
ASW-EGTA.
In both species, important animal-animal variability was observed,
accounting for as much as 50% of the variation in the mechanical properties
measured. Such an interindividual variability has been reported in other
mechanical studies of MCTs (e.g. Trotter
and Koob, 1995), but this is the first time it has been
quantified. To avoid this phenomenon, which masks the effect of the different
bathing solutions, some authors have used specimens rested for up to 24 h
(Motokawa and Tsuchi, 2003
) or
anaesthetized specimens (Wilkie et al.,
1999
). In our second experiment, individuals were anaesthetized to
avoid any non-specific stiffening of the connective tissue under nervous
control. The mechanical properties of anaesthetized tube feet were similar to
those obtained in ASW but with a lower interindividual variability. In P.
lividus, the addition of the cell-disrupting solution induced once again
a significant strengthening and stiffening of the tube feet. Moreover, this
time, extensibility, initial stiffness and toughness also increased in this
solution. In M. glacialis, the lysing agent did not cause
strengthening but decreased final stiffness and extensibility.
In both P. lividus and M. glacialis, the results of the
mechanical tests together with the presence of juxtaligamental-like cells in
the connective tissue clearly show that an MCT is present in their tube feet.
However, the tube foot stems of echinoids and asteroids are affected
differently by the cell-disrupting solutions, indicating that their MCTs could
be functionally different. This hypothesis is supported by the observation
that there is a single type of juxtaligamental-like cell in the connective
tissue of echinoid tube feet but two types of cells in asteroid tube feet. The
influence of our bathing solutions on the mechanical properties of the tube
feet of P. lividus matches exactly the influence of similar
treatments on sea urchin spine ligament and holothuroid dermis (see, for
example, Szulgit and Shadwick,
1994; Trotter and Koob,
1995
). These observations suggest that, following cell lysis, a
stiffening factor is released from the juxtaligamental-like cells in the
extracellular matrix. Recently, such a factor, named tensilin, was isolated
from sea cucumber dermis and characterized
(Tipper et al., 2003
). This is
a collagen-fibril binding protein that, when released from the
juxtaligamental-like cells, has the ability to induce dermis stiffening
(Tipper et al., 2003
;
Wilkie et al., 2004
).
As far as the tube foot MCT of M. glacialis is concerned, our
observations in the calcium-free solutions indicate that, following cell
perforation, a stiffening factor is released into the extracellular matrix.
This factor seems to act differently from that of P. lividus, having
a very limited effect in the presence of calcium. Hence, in sea stars, the
standard state of tube foot MCT appears to be mechanically similar to its
stiffened state, as evidenced by the lack of effect of cell-disrupting
solutions on tensile strength, final stiffness and toughness. Yet, solutions
inducing cell lysis have an effect on the tube foot stem extensibility and
initial stiffness, two mechanical properties that are presumably directly
linked to the elastic network of microfibrils
(Vincent, 1990;
Thurmond and Trotter, 1996
;
Vogel, 2003
). Moreover, this
elastic component of the connective tissue seems to be much more developed in
the tube feet of M. glacialis than in those of P. lividus.
Therefore, the asteroid stiffening factor could in some way interact with the
microfibrillar network. Interestingly, the possibility that MCT stiffness may
be altered by changing the interactions between the collagen fibrils and the
microfibrils has already been proposed
(Szulgit and Shadwick, 2000
).
Clearly, more experiments are needed to clarify the functioning of the MCT in
asteroid tube feet.
It is certainly an adaptive advantage for both echinoids and asteroids to
have tube foot stem connective tissue with mutable mechanical properties. In
order to protract the tube foot, ampulla muscles contract to force the
ambulacral fluid into the lumen, inducing a gradual stretching of the stem. To
retract, the retractor muscles of the tube foot contract, expelling the
ambulacral fluid back into the ampulla. When there is a differential
contraction of these muscles, the tube foot bends to the more contracted side
(Flammang, 1996). Therefore, in
the compliant or destiffened state, MCT would deform with low energetic costs,
assisting the ampulla muscles during tube foot elongation as well as retractor
muscles during retraction and bending. In the stiffened state, MCT would also
have a prominent role in the energy-sparing maintenance of position, for
example during strong attachment to the substratum to resist hydrodynamically
generated loads.
List of symbols and abbreviations
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Acknowledgments |
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Footnotes |
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References |
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