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First published online November 30, 2007
Journal of Experimental Biology 210, 4272-4278 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.007054
Mechanical properties of the rigid and hydrostatic skeletons of molting blue crabs, Callinectes sapidus Rathbun
1 Department of Biology, University of North Carolina at Chapel Hill, Chapel
Hill, NC 27599, USA
2 Embrex, Inc., Box 13989, RTP, NC 27709-3989, USA
* Author for correspondence at present address: Department of Integrative Biology, University of California, Berkeley, CA 94720, USA (e-mail: jrataylor{at}berkeley.edu)
Accepted 24 September 2007
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Summary |
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Key words: crab, molting, Callinectes sapidus, cuticle, mechanical properties, tensile strength, Young's modulus, flexural stiffness, hydrostatic skeleton
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Introduction |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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; Scott and Hepburn,
1976; Lipcius and Herrnkind,
1982; Steger and Caldwell,
1983; Adams and Caldwell,
1990; Cromarty et al.,
1991; Katz and Gosline,
1992; Queathem and Full,
1995). In crabs, and probably other arthropods as well, mobility
is maintained during molting by switching to a hydrostatic skeletal support
system (Taylor and Kier, 2003;
Taylor and Kier, 2006). Rigid
and hydrostatic skeletons differ greatly in their structure and mechanisms of
support. Thus, alternation between the two skeletal types requires significant
structural and functional changes in the cuticle.
Rigid skeletal support systems are common in vertebrates, arthropods,
echinoderms and other phyla. Antagonistic muscles insert on stiff skeletal
elements that move relative to one another at joints and can function as
levers that may amplify either the force or the displacement of muscle
contraction. The forces of muscle contraction are thus transmitted through the
stiff elements as compressional, torsional and bending stresses
(Wainwright, 1982) that must
be resisted by the rigid elements in order to avoid failure. In crabs, the
body is typically held above the substratum by multiple jointed legs. The
merus (the fourth, and often longest, segment) of the walking leg is extended
laterally and horizontal with the body, while the last leg segments extend
vertically to the substrate (Hahn and
LaBarbara, 1993). This body posture places bending and torsional
stresses on the merus, and compressional stresses on the last limb segments,
so that limb failure typically occurs by local buckling
(Currey, 1967;
Hahn and LaBarbara, 1993).
Rigid skeletons thus function primarily by resisting compressional, bending
and torsional stresses.
Hydrostatic skeletons are common in soft-bodied invertebrates including
polyps, such as sea anemones, and many types of worm. Classical hydrostatic
skeletons have no rigid elements, are typically cylindrical in shape, and
consist of a flexible, muscular body wall surrounding a liquid-filled cavity
(Chapman, 1958;
Trueman, 1975;
Gutmann, 1981;
Wainwright, 1970;
Wainwright, 1982;
Wainwright et al., 1976). The
body wall typically includes antagonistic longitudinal and circumferential
muscle layers and is reinforced with connective tissue fibers. The forces of
muscle contraction are transmitted through the essentially incompressible
fluid, resulting in an increase in the internal hydrostatic pressure and
tension in the body wall. To prevent changes in body shape, the body wall must
resist this tension (Wainwright,
1970). The structure and mechanical properties of the body wall
therefore control shape changes of the animal by resisting tensile forces
(Harris and Crofton, 1957;
Clark and Cowey, 1958).
The crustacean skeleton alternates between these two dramatically different
forms of skeletal support each time molting occurs. During molting, the animal
first secretes a new cuticle beneath the old exoskeleton. Then ecdysis begins,
during which the animal draws in water through the mouth, breaks the carapace,
withdraws from the old exoskeleton (exuviation), and continues to absorb water
until the new, soft cuticle is inflated to a larger size. It then takes
several days before the new cuticle hardens (see
Herrick, 1895;
Drach, 1939;
Richards, 1951;
Passano, 1960;
Aiken, 1980;
Skinner, 1985). Thus,
immediately after exuviation, crabs are soft, inflated with water, and the
cuticle is in tension, resembling other animals with hydrostatic skeletons.
The muscular arrangement, however, remains unchanged.
Concurrent with this dramatic change in the mechanical function of the
cuticle during the molt cycle are the remarkable changes that occur in its
structure (Roer and Dillaman,
1993). The cuticle changes from a rigid and tough material that
requires significant force to bend and break, to a flimsy membrane that
deforms as easily as plastic wrap. The cuticle is composed of four layers:
epicuticle, exocuticle, endocuticle and membranous layer, in order from
outermost to innermost. These layers are composed of a chitin–protein
matrix and calcium carbonate (Roer and
Dillaman, 1984). Before ecdysis occurs, the new epicuticle and
exocuticle layers are secreted by the underlying hypodermis. These layers
begin hardening, by cross-linking, once exuviation is complete
(Drach, 1939;
Dennell, 1947;
Travis, 1963). Thus, for
several hours following exuviation, the cuticle is highly flexible and soft.
This period is referred to as the soft-shell stage in blue crabs. Within just
a few hours of ecdysis, the innermost and thickest layer of the cuticle, the
endocuticle, is secreted and begins calcification
(Travis, 1957;
Travis, 1963;
Travis, 1965). At
approximately 12 h after ecdysis, tanning and mineralization begins and the
cuticle attains the texture of paper. In blue crabs, this is referred to as
the paper-shell stage. The calcification process continues until the entire
cuticle is secreted. The deposition of calcium carbonate, protein and chitin
continues for up to 30 days postmolt
(Dendinger and Alterman, 1983).
Crabs are then referred to as being in the hard-shell stage until the next
molt. This elaborate process of regeneration and hardening of the cuticle
during each molt provides the structural changes that both require and
facilitate the switch between rigid and hydrostatic support mechanisms.
The changes in structure and function of the cuticle imply correlated
changes in the mechanical properties of the cuticle. As the cuticle
transitions from rigid to soft and flexible during molting, it must also
change from primarily resisting compressive, torsional and bending forces to
primarily resisting tensile forces. Though the mechanical properties of some
crustacean cuticles have been measured previously
(Hepburn et al., 1975;
Joffe et al., 1975a;
Joffe et al., 1975b;
Hepburn and Chandler, 1976;
Currey et al., 1982;
Dendinger and Alterman, 1983;
Palmer et al., 1999;
Dutil et al., 2000), few
studies have measured the mechanical properties throughout the molt cycle
(Dendinger and Alterman, 1983;
Dutil et al., 2000). Both of
these studies found significant changes in tensile strength and elastic
modulus of the cuticle immediately following molting. In this study, we
document the changes in the mechanical properties of the cuticle associated
with its change from a rigid to a hydrostatic skeleton. We measured the
flexural stiffness, Young's modulus of elasticity (in tension) and tensile
strength of the cuticle of the blue crab, Callinectes sapidus, at a
series of postmolt cuticle stages. We discuss these mechanical properties in
the context of the role of the cuticle in skeletal support and movement at
each stage.
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Materials and methods |
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). Male and
female `peeler' crabs (within 2–3 days of molt) ranging from 70 to 85 mm
premolt carapace width were obtained from O'Neals Sea Harvest (Wanchese, NC,
USA). Crabs were transported to the University of North Carolina at Chapel
Hill where they were maintained in individual artificial seawater aquaria (280
mm x 172 mm x 203 mm) at a temperature of 19°C and a salinity
of 15–20 p.p.t. (Instant Ocean Artifical Seawater, Aquarium Systems
Inc., Mentor, OH, USA). Water changes were performed consistently for all
crabs every 2 days. Animals were checked every 2 h for the onset of
exuviation. The time postmolt was calculated from the time exuviation was
complete. Cuticle samples were taken from individual crabs at three different
times postmolt: 1 h (soft-shell stage), 12 h (paper-shell stage) and 7 days
(hard-shell stage). The animals were not fed before or during experiments.
Cuticle samples
Both chelipeds were autotomized from crabs at the three specified postmolt
stages. Limb autotomy is a natural, non-lethal defense mechanism that can be
quickly and easily induced by either applying pressure or making a small
puncture with a needle near the merus-basis joint. One cheliped was used for
tensile testing and the other was used for bending tests. If the chelipeds
differed in size, the larger one was used for tension tests (the larger size
facilitated the preparation of the samples for tensile testing) and the
smaller one for bending tests; otherwise, they were selected at random.
Rectangular samples of cuticle were cut, using a razor blade or scissors, from
the flat, dorsal surface of the merus segment. For bending tests, samples were
cut longitudinally, while samples for tensile tests were cut in the hoop
direction (i.e. circumferentially). This allowed the largest piece of material
to be cut and the loading during the tests to be performed in an orientation
that was appropriate for loading in the animal. It is possible that the
cuticle is anisotropic and thus our results may differ from mechanical
properties measured in other directions. Cuticle samples removed for bending
tests were approximately 5–9 mm wide and 15–25 mm long and those
for tensile tests were approximately 5 mm wide and 10 mm long. The hypodermis
was carefully removed from all samples with the edge of a razor blade under a
microscope. For bending tests, cuticle samples were tested immediately.
Because we had limited access to the tensile testing instrumentation, cuticle
samples for tensile tests were immediately placed in vials of seawater and
stored in a refrigerator until testing could be performed. Samples were stored
in this manner to avoid the effects of chemical fixatives on the mechanical
properties. Samples were kept for no longer than 3 weeks before testing. Prior
to and during all tests, specimens were kept moistened with seawater since
hydration state affects the mechanical properties
(Hepburn et al., 1975;
Joffe et al., 1975b).
Bending tests
Soft and paper cuticle apparatus
A 3-point bending apparatus was constructed that employed two no. 7 size
stainless steel insect pins (0.70 mm diameter) as supports while force was
applied to the center of the sample with a force transducer
(Fig. 1). The insect pins were
attached to the side of a solid brass bar (100 mm x 19 mm x 19 mm)
so that they extended vertically, 10.19 mm apart. Cuticle samples were placed
against the insect pins with the epicuticle surface facing away from the force
transducer. This ensemble was then placed in a square plastic box (11 cm
x 11 cm x 3 cm) filled with seawater on the stage of a dissecting
microscope. Two force transducers that incorporated silicon strain gauge
elements were used (AE-801 Sensor Element, SensorOne Technologies Corp.,
Sausalito, CA, USA). A no. 0 stainless steel insect pin (0.35 mm diameter) was
epoxied to the silicon beam of the sensor element and bent at a 90° angle
so that the head pressed against the cuticle sample. The sensitivity of the
force transducer used for the soft cuticle samples was increased by
lengthening the moment arm with a 90 mm long, 0.35 mm diameter stainless steel
wire attached to the insect pin. The force transducer was mounted on a 3-axis
micromanipulator placed adjacent to the microscope. The micromanipulator was
used to advance incrementally the pin attached to the force transducer in the
center of the sample. The displacement of the cuticle sample and any
displacement of the force transducer were measured with an ocular micrometer.
At each displacement, the force and distance of displacement were recorded.
The total displacement was less than 10% of the sample length.
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The force transducers were calibrated before and after each series of experiments with objects of known weight. The ability of the 3-point bending apparatus to predict the Young's modulus of samples was confirmed using plastic shim stock (Artus Corp., Englewood, CA, USA) of known modulus and a range of thicknesses: 0.01, 0.02, 0.025, 0.04 and 0.05 mm.
Hard cuticle apparatus
A tensometer (Hounsfield Tensometer, Tensometer Limited, Croydon, UK) was
adapted for 3-point bending tests (Fig.
2). The moveable grip was modified by adding two horizontal bars,
19.8 mm apart. A third horizontal bar was attached to the beam of a force
transducer (Fort 250, Precision Instruments, Sarasota, FL, USA) clamped to the
stationary grip. The cuticle sample was inserted vertically between the two
horizontal bars with the epicuticle facing away from the transducer. The three
horizontal bars were machined so that the sample rested against a sharp
90° ridge on each. The moveable grip was advanced incrementally and the
distance between the two grips (displacement) was measured using an ocular
micrometer attached to a free-standing surgical microscope. The force
transducer was connected to the same equipment and analyzed using the same
software as described for the soft and paper cuticle above. Additionally,
calibrations of the force transducer and verification of the 3-point bending
apparatus were made in the same manner as for the apparatus used for the soft
and paper cuticle but with a range of heavier calibration weights and with
plastic shim stock of the following thicknesses: 0.25, 0.31, 0.4, 0.5, 0.6 and
0.75 mm.
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Analysis
Bending
Flexural stiffness, EI, was calculated using the equation for
3-point bending:
 | (1) |
).
Tension
The force and displacement data obtained for each tension test were
converted to stress and strain for analysis. Stress, 
, was calculated
as engineering stress:
 | (2) |
Strain, 
, was calculated as engineering strain:
 | (3) |
L is the change in length of the sample and
L0 is the initial sample length. The use of engineering
strain rather than true strain should not cause significant error since the
measured strains are all relatively low (less than 12%).
A stress–strain plot was created for each cuticle sample, from which
the Young's modulus of elasticity (stiffness), the tensile breaking strength
and the work to failure were obtained. The Young's modulus of the material in
tension is the ratio of stress to strain (i.e. the slope of the plot). For
non-Hookean materials (those that do not show a linear relationship between
stress and strain), the stiffness can be estimated with a tangent modulus,
measured as the slope of the linear portion of the stress–strain plot
between 10 and 50% of the strain at failure
(Hepburn and Joffe, 1974). The
tensile strength of a material is the stress at failure. The work to failure
was estimated by calculating the area under the stress–strain curve up
to the point of failure. The material properties were averaged among samples
of each postmolt stage (soft, paper and hard) and compared across stages using
JMP IN 5.1 statistical software. Data for the modulus and strength were
determined to have a normal distribution by the Shapiro–Wilcoxon test,
so an ANCOVA was used to test for differences among the cuticle samples with
storage time as a covariate. The estimated work to failure was compared among
stages using non-parametric statistics
(Zar, 1999).
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Results |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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2=13.8, P<0.001; Q=2.39,
P<0.05; N=12, 10 and 10, respectively). The measured
flexural stiffness of soft and paper cuticle samples were not statistically
different.
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2=12.7, P<0.01; Q=2.39,
P<0.05; N=15, 18 and 12, respectively).
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Discussion |
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TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
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For the first 12 h following ecdysis, the soft cuticle has a remarkably low
flexural stiffness (2x10–9 to
7x10–9 N m2). When handled, soft cuticle
folds easily under its own weight and obviously cannot resist significant
bending forces. This presents a fundamental problem for functioning as a
typical rigid exoskeleton because movement and muscular antagonism require
that the cuticle resists the bending forces associated with muscle
contraction. The claw muscles of decapod crustaceans are capable of producing
large stresses, as high as 400–2000 kN m–2 during
intermolt (Josephson, 1993).
During molting, intrinsic or extrinsic factors may reduce the force production
of some muscles in order to prevent damage to muscle fibers or cuticle. The
claw muscles undergo significant atrophy prior to molting
(Skinner, 1966;
Mykles and Skinner, 1981;
Mykles and Skinner, 1982;
Mykles and Skinner, 1990) but
they are still capable of producing force following ecdysis, and thus remain
functional (West et al., 1995;
West, 1997). This is important
since the exuviation process itself requires repeated, forceful movements in
order to pull the appendages out of the old exoskeleton
(Travis, 1954;
Lipcius and Herrnkind, 1982;
Phlippen et al., 2000).
Deformation in the cuticle can be seen during this active process (J.R.A.T.,
unpublished observation) and the increased internal hydrostatic pressure
resulting from postmolt inflation (deFur et
al., 1985; Taylor and Kier,
2003) is necessary to provide resistance to muscle contraction.
Indeed, hydrostatic skeletal support is used by the blue crab during the first
12 h following ecdysis (Taylor and Kier,
2003).
As the cuticle hardens during the first week after ecdysis, the flexural
stiffness increases by four orders of magnitude
(1.8x10–5 N m2). This large increase in
flexural stiffness correlates with the progression of the mineralization
process (Vigh and Dendinger,
1982; Dendinger and Alterman,
1983). By 7 days following ecdysis the hard cuticle is capable of
resisting significant bending, torsional and compressional forces. At this
time, the cuticle, rather than the fluid, transmits the forces of muscle
contraction and the animal once again functions using a rigid skeletal support
system (Taylor and Kier,
2003).
The tensile properties of the cuticle also change significantly as crabs
switch between rigid and hydrostatic skeletons. The tensile stiffness, or
Young's modulus, of the soft cuticle within an hour of exuviation is only 132
MPa, but increases significantly to 379 MPa 12 h later during the paper stage
and stabilizes at 361 MPa a week later during the hard stage. We are not aware
of measurements of tensile stiffness for newly molted animals, but the tensile
stiffness we observed for the hard cuticle of the chelipeds is similar to that
reported for the carapace of the crab Scylla serrata (481 MPa)
(Hepburn et al., 1975) and the
carapace of the prawn Panaeus mondon (461–549 MPa)
(Joffe et al., 1975b). A
similar pattern of a rapid increase in flexural stiffness during the first 12
h following ecdysis has also been observed in locust cuticle
(Hepburn and Joffe, 1974).
This difference in tensile stiffness between the soft cuticle and the paper
and hard cuticles reflects the function of the cuticle during the molting
process. During ecdysis, the animal inflates with water and the soft new
cuticle is stretched to accommodate the requisite size increase that occurs at
each molt. Once ecdysis is complete further stretching may be resisted as the
stiffness of the cuticle increases. The increase in Young's modulus observed
in the paper stage cuticle is probably associated with calcification and
cross-linking of cuticle proteins
(Dillaman et al., 2005).
Calcium carbonate deposition continues throughout the paper stage, adding
stiffness to the cuticle, but levels off after 48 h
(Vigh and Dendinger,
1982).
It is striking that the tensile strengths of the soft and paper cuticle are
the same as that of the much more robust hard cuticle, ranging from 10 to 15
MPa. The significantly greater cross-linking and mineralization of the hard
cuticle do not afford it any greater tensile strength than the soft cuticle.
Indeed, the soft and paper cuticles absorb significantly more energy before
breaking than the hard cuticle, with work to failure values of 0.71, 0.81 and
0.17 MPa, respectively. These values of tensile strength are slightly less
than those found in the hard cuticle of the merus of the crab Scylla
serrata (30 MPa) (Hepburn et al.,
1975) and the carapace of the prawn Penaeus mondon
(18–28 MPa) (Joffe et al.,
1975b). They are similar to previous measurements of the carapace
of blue crabs (5.6–15 MPa), despite the fact that they were taken from
the carapace rather than the chelipeds and were frozen before testing
(Dendinger and Alterman,
1983).
In general, the soft- and paper-shell stage cuticles are incapable of
resisting compressional and bending forces but function well in resisting
tensile forces. For comparison, the tensile strengths of soft and paper
cuticles are greater than concrete brick (5.0 MPa) and are the same order of
magnitude as abductin (10 MPa) (Vogel,
2003). The tensile stiffness of soft cuticle approximates that of
mussel byssal thread (100 MPa) (Vogel,
2003).
The typical stresses in the cheliped due to the hydrostatic pressure experienced by soft-shell and paper-shell animals in this study were estimated to be 0.86 MPa and 0.16 MPa, respectively. These estimates indicate that soft-shell crabs operate with a safety factor of approximately 10, while paper-shell crabs operate with a larger safety factor of approximately 100. Thus, the risk of tensile failure of the soft cuticle during movement in hydrostatically supported crabs is low.
The changes in the mechanical properties of the cuticle, as it transitions
from rigid to soft during the molt cycle, may affect the locomotor ability of
animals. For instance, skeletal stiffness is known to affect the jumping
ability of the African desert locust
(Scott and Hepburn, 1976;
Katz and Gosline, 1992), which
can vary as much as twofold during the molt cycle
(Queathem and Full, 1995).
Likewise, changes in the cuticle associated with the shift to hydrostatic
skeletal support are likely to affect locomotion in crabs. This could
potentially have significant effects on the ability of an animal to escape
predators and find shelter during this critical period
(Woodbury, 1986).
Molt-induced changes in the structure and mechanical properties of the
cuticle may vary among arthropods, in part due to differences in the cuticle
that correlate with habitat. For example, as crabs evolved adaptations to life
on land, the cuticle became thicker and more heavily calcified. In addition,
crustacean cuticle differs from insect cuticle, which is tanned but not
calcified, although the material properties of some insects and crustaceans
are reported to be similar (Joffe et al.,
1975b). A more extensive study of the mechanical properties in
other groups of arthropods and other molting phyla may provide new insights
into the mechanics of the molting process and reveal additional important
characteristics relevant to the evolution of ecdysozoans.
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Acknowledgments |
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