FATIGUE AND FRACTURE AT THE MUSCLE SCAR OF
FOUR INTERTIDAL LIMPET SPECIES: C limstule, C.
pelte, C digitalis, and d. mitre
DANIEL BAGDAD
HOPKINS MARINE STATION
1988
ABSTRACT
This study examined and compared the forces required to
fracture limpet shells. Shells of recently-killed Calliselle
pelte, Collisella limatule, Colliselle digitelis, and Acmses
mitre were frectured in an apparatus mimicking the crushing
behavior of crabs. In addition, shells of C limatule and C. pelte
were tested for fatigue fracture by repeatedlg loading the
shells. All species save A. mitre showed increased force
needed for frecture es shell thickness increased. No
significent differences existed in force es a function of shell
thickness among the species nor within each species for forces
applied at the length and width of the scar and margin.
However, shell size at the width of the scar was significantlg
smaller than at the other orientations for each species,
suggesting that crabs could attack more shells at the scar
width than at other places. Also, shells of C limstule had
significantlg smaller widths at the scar then the other species,
suggesting that perhaps more C limatule shells are found
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fractured et the muscle scar because these smaller scar-width
shells are within the grasping range of more crabs. Fatigue
fracture proved significant (causing fracture below 200 cycles)
at force loads above 602 of the predicted breaking force. Above
70-752 of predicted strengths, fracture required less than 50
cycles, indicating that within short time spans crabs could
fracture shells without ever exerting a maximum force.
Scanning electron microscope observations revealed that the
crossed-lamellar lagers along the horseshoe-shaped scar lager
form almost continuous sheets that allow cracks to frecture
the upper portion of the shell cleanly at the muscle scer.
IHTRODUCTION
A previous studg on intertidal limpets (Chapin, 1966)
focused on the predatorg of the shore creb, Fachygrepsus
crassiges. Several limpets, particularly Colliselle limatule,
left in an aquarium with a crab were found after several dags
to have been crushed neer the muscle scar. This form of attack
left the rim of the shell intact, the top was cleanly severed
from the rest of the shell. Tests done with needle-nosed pliers
showed that for Colliselle limatule substantially less force
was required to fracture the shell at the scar than at other
points. In this studg l examine the apparent structural
weckness of the muscle scar lager both by comparing the
forces required to break shells of one species et different
locations and by compering the forces necessarg to crush shells
of different species at the same point on the shell. To see if
high and low-spired limpets differed in fracture strength
focused on species that varied in relative height (figure 1).
Another reason for focusing in particular on the muscle scar
lager was that most limpet shells varg in thickness along the
shell (figure 24), with a thickened margin and apez and a
relatively thin muscle scar lager. One objective of my studg
wes to determine if this thinning-out of the shell neer the scer
allowed the shell to fracture more easilg at the scar,
especially in comparison to the thickened margin.
The horseshoe-sheped muscle scer (figure 28) on the
inner surfece of limpet shells results from the attachment of
the foot adductor muscles. Although Chapin (1966) found C.
limatule shells to break more easilg along the length than
width of the scar, was interested to discover if some feature
of the actual shell structure along the horeshoe-shaped scar
accounted for the frecture characteristics. In particuler,
HacClintock (1967) describes the myostracal (muscle scer
lager of the shell as differing from the typical
crossed-lamellar structure of limpet shells (figure 34). At the
scer the muscle attechment interferes with the usuel
shell-laging process of the mantle. The resulting structure is
usuallg prismatic, and Curreg (1974) describes this structure
as stronger than crossed-lamellar (tensile strength »60PN/m-
for prisms). The prisms of the myostracum form the inner
surface of the shell (figure 3B). Figure 4 shows the effects of
a crushing force applied by a crab cheliped, with the result
being tension along the inner surece and compression along the
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outer surface. The high tensile strength of the prisms would
allow this material to resist frecture at higher stresses than
the lower strength of the adjacent shell structures. In light of
this picture, 1 was interested in investigating which structural
festures of the muscle scar lager, if ang, account for the
fracture mechanics.
Another interesting aspect of limpet shell fracture at
the muscle scer involves fatigue fracture. Boulding (1966) and
Currey (1984) have examined fatigue fracture in bivalves and
shovn that crabs often load a shell repeatedig up to around 200
times (sometimes over several hours or dags). As long as the
crab exerts a force/area of at least 60-702 of the predicted
breaking strength, the shell is likely to fracture after a number
of cycles at this submaximal stress. In this fashion crabs can
successfully attack large shells that theg cannot crush in one
attempt. As no study thus far has examined fatigue fracture in
intertidel limpets, also investigated the effectiveness of the
this predatorg technique.
MATERIALS AND METHODS
A. TEST OF MUSCLE SCAR AND SHELL MARGIN STRENGTH
Callisella pelts, Colliselle limstule, Colliselle sigitslis,
and Acmses mitre (figure 5) were collected at various
locations at the Hopkins Marine Station (Pacific Grove, CA) and
placed in an aquerium with running sea water. The limpets
were dissected out of the shell and the shells placed in dishes
with sea water. Messurements were taken of: length and width
of the shell at both the scar and the margin; height from
aperture to apex; and the thickness of the shell at the front,
back, right side, and left side at the level of both scar and
margin. To fracture the shells constructed two
nutcrecker-like devices (figure 6). Each crushing device
consisted of two blocks of wood connected by a hinge, such that
the blocks could close like upper and lower jaws. Two small
metal plates (see figure 6) on the same side of each block acted
as teeth to contact the shell and transmit the force. When
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loaded in the apparatus the apex of the limpet shell pointed
toward the blocks. The base of the shell rested on an adjacent
block of wood (see figure 6) that served as a substrate to
prevent slippage. The force was applied by attaching a spring
scale to the hook protruding from the end of the upper block.
The force was incressed slowlg until the shell fractured, and
this maximum force was recorded. The magnitude of the actual
force transmitted to the shell was calculated by accounting for
the mass of the wood blocks and the spring scale. By adjusting
the orientation and point of contect between shell and crushing
device, one could load shells from each species at one of four
locations (figure 7):
1) Force applied along the length of the margin, here termed
Longitudinal Margin.
2) Force applied along the width of the margin, here termed
Lateral Margin.
3) Force applied along the length of the muscle scar, hère
termed Longitudinal Scar.
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4) Force applied along the length of the muscle scar, here
termed Lateral Scar.
The same device was used to test if shells missing the
portion of the shell above the scar (such that onlg the rim is
left intact) would be easier to break than completelg intact
shells. For this test l used Colliselle pelte shells and applied
the forces at the front and lateral margin.
B. FATIGUE-LOADING EXPERIMENTS
Colliselle limatula and Colliselle pelte shells were
loaded repeatedlg for five seconds at a time for up to e
maximum of 200 cycles. The loads applied were some fraction
of the predicted breaking force ranging from around 10-902.
Values for the predicted breaking force were determined from
the results of part A for the two limpet species in question.
The values were teken from the linear regression lines for
force vs. thickness (figure 10). The tests were conducted using
the same crushing devices previouslg described, with a known
mass attached to the spring scale. During each fatigue
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sequence examined the shell under a dissecting microscope
after every 25-30 cycles to trace the development of
fatigue/stress cracks. A scanning electron microscope was
used to examine fatigue cracks and fracture surfaces along the
muscle scar lager.
C. FIMITE ELEMENT ANALVSIS
constructed models of four limpet species (Calliselle
pelte, Colliselle limatule, Colliselle digitalis, Acmees mitre)
on a Macintosh"" computer using e finite element analgsis
progrem (HSC/pal"“, MacNeal-Schwendler Corporation). The
models consisted of interconnected quadrilateral and triangular
plates. The nodal points (XYZ coordinates) for each limpet were
determined by first projecting a slide with a grating (see
figure 8) onto the shell. The pattern of lines on the shell was
then photographed and the resulting picture projected onto a
screen. The result was a topographic map of the shell surface,
from which ! derived XY coordinetes (2 coordinates were
measured on the shell). Also, specified realistic material
properties for the shells, including ectuel thicknesses for each
plate. used material properties for enother limpet species,
Estelle mevicans (Currey, 1980): Voung's Modulus-6.0 x 103
N/m2, Shear Modulus-2.7 x 10° N/m2, Vielding Strength-3.3 x
107 M/m2, Poisson's Ratio-O.1, Calcium Carbonate Mass
Densitu-2.93). For each species ! epplied forces equal to
75-602 of the predicted breaking force (ascertained from the
force vs. thickness results of part A).
RESULTS
A. COMPARISON AMONG SPECIES OF FORCE VS. THICKNESS
VALUES AT EACH GRASPING ORIENTATION
Figure 94 shows the combined force vs. thickness values
of the four species tested (C. Felte, C. limstule, C digitelis. 4
mitre) for forces applied along the length of the muscle scar.
Figure 98 plots individual linear regressions and reveals that C
limatule, C. pelte, end C digitelis eoch showed e significent
increase in force required to frecture the shell as thickness et
the scor increosed (r.z.65, pc.001, r z.26, pc.05, r =.33, p..02,
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respectivelg). A. mitre did not show a significant force vs.
thickness relationship. Comparisons of mean force/thickness
values between pairs of the three species showing significant
positive force/thickness slopes (for longitudinal/scer loading)
revealed that C oigitalis shells were easier to crush than
those of C. limstule, but only by a factor of 1.3. A similar set
of force vs. scer thickness calculations for loading ecross the
width of the scar and length/width of the margin produced
compareble trends, with only 4. mitra displaging no significant
increase in force required for frecture es thickness at the scar
increased. For the comparison of forces required to fracture
the shell when loaded longitudinallg and laterallg at the
margin, plotted force against relative thickness (scar
thickness/margin thickness), since the force required to
frecture the shell at the margin depends on the margin
thickness as well as the thickness at the scar. In all three
cases (lateral scer, longitudinal/lateral margin) no significant
differences appeared among the species tested.
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B. FORCE VS. THICKNESS WITHIN EACH SPECIES
Comparisons emong force/thickness means within esch
species at the four grasping orientations showed no significant
differences, with the sole exception of C limatule shells
which break more easily at the margins than the scars
(longitudinal margin vs. longitudinal scar, p4.001; lateral
margin vs. leteral scer, p«.05). Therefore the grephs of force
vs. thickness for each species (figure 10) show the overall
trend for all four grasping orientations treated as one set of
date. Again, onlg A. mitre produced no overall significant
trend in force vs. thickness.
Figure 11 shows the results of the forces required to
fracture the rims of C pelte shells (missing the top of the
shell above the scar) compered to intact shells. Shells missing
the apical portion (above the scar) did not fracture at a
significentlg lower force than intect shells, and thus onlg the
overall trend (with force vs. thickness for all shells grouped
together) is plotted. This graph shows again that more force is
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necessary to fracture thicker shells.
C. COMPARISONS OF SHELL DIMENSIONS WITHIN AND AMONG
SPECIES
Measurements at the length and width of the scar and
margin revealed (figure 12) that for each species the shell
width at the scar was significantlg smaller than the distence
which must be spanned by a cheliped in the other three
orientations (p«.001 in all three cases). Also, the comparison
of sizes emong species (figure 13), using shells with similar
lengths (margin length- 18-2 1mm) revealed that C. limatule
has the smallest average width at the scar(pe.00 1), with 4
mitre substantially wider at the scar than the others.
D. FATIGUE-LOADING EXPERIMENTS
The results of repeated force loading along the length of
the scar for C limatule and C. pelte show the effectiveness of
this type of force loading (Figure 14). As long as the static
force exceeded 603 of the predicted breeking force the
strength of the shell was reduced. The values for predicted
breaking force (obtained from linear regression values of force
vs. thickness for C limatule and C pelte respectivelg)
appeared fairly accurate, as those shells loaded in excess of
200 cucles at low percentage loads and then tested for
breaking strength by fracturing the shell generallg broke near
predicted force values. The fatigue plots also illustrate that at
eround 70-752 (and ebove) of the predicted breaking force,
fracture resulted(almost alwags) after fewer than 50 cycles.
Light(dissecting) microscope observations of fatigued shells
demonstrated the development end extension of fatigue
cracking. Figure 154 shows the typical pattern of 1-2 stress
cracks (white lines on the shell) beginning at the front of the
shell; over time these cracks spread around the inner surface,
generallg traveling along the muscle scar lager (figures 158 &a;
16). Crecks at the margin and scer (seen on the shell's
underside) almost always spread out around the shell(in
elliptical rings), while closer to the apex the cracks moyed
radially (figure 15C). Often, especiallg at the front and back of
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the shell, scar-level rings would merge and travel radiallg
toward the margin (figure 150). In this manner when the shell
ultimately fractured the top would "pop-off" and the margin
rim left behind would split in two.
E. OBSERVATIONS OF FRACTURE PATTERNS AT THE MUSCLE SCAR
1. Visual-- In longitudinal scar loading most shells
would develop a small crack at the very front of the shell at
the level of the scer under sub-breaking loads (seen
perticulerly in C. limatule during fetigue-loading). Once the
force epplied reached the critical level, the entire top would
break off cleanly at the scar. In mang cases the fracture at the
front of the shell anterior to the actual myostracum was
jagged and irregular, while the fracture at the scar itself was
smooth. Margin-loaded shells tend to break first at the scar
level. In mang instances the entire top would fracture cleanig
before the margin shattered.
2. SEM-- Closer inspections of scer fracture surfaces
under the scanning electron microscope revealed a smooth
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creck surface resulting from cleavage of the crossed-lameller
structure between the primarg lamellae (along the grain). As
seen in figure 17, the parallel crossed-lamellar sheets ran
along the shell at the level of the muscle scar with each sheet
parallel normal to the outer surface of the shell (figure 170).
Figure 178 illustrates the smooth fracture surface along the
side of the scar, showing that the crack passed between
lamellae.
F. FINITE ELEMENT ANALYSIS STRESS DIAGRAMS
The stress diagrems for C. oigitalis in figure 19 show
the relative compressive (colored plates) and tensile (white
plates with numbers) stresses resulting from forces applied at
each grasping orientation. The shells with forces applied along
the length and width of the scar show tensile stresses
concentrated where the force was applied, with low
compressive stresses elsewhere. In contrast, the shells with
forces applied at the margin length and width show high tensile
stresses ot the point of opplication 9s well os high
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compressive stresses at the level of the scar (see color
scheme, figure 18). Also of note is that forces applied at the
lateral scar and margin produced greater tensile and
compressive stresses at the front of the shell and at the scar
(compared to forces applied longitudinallg along the scar and
margin).
also compered stresses between e high profile (4.
mitra) end low profile (C. limatula) limpet shell of equel
length and found that at each grasping orientation C limatule
reached greater stress concentrations then A mitra For
instance, application of 802 of the predicted breaking force to
C limatule along the length of the scar resulted in a stress
equal to 7-103 of gielding strength at the scar and margin,
while a comparable load for A. mitre (803 predicted bresking
force) produced a stress equal to only 1-32 of gielding strength
(figure 20).
DISCUSSION
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The majority of shells frectured elong the length or
width of the muscle scer broke cleanlg, completelg severing
the top of the shell from the shell's rim (figure 21). The
effectiveness of this form of attack indicates that a crab such
as Pechugrepsus crassipes cen preg upon limpets without
having to remove the shell from the rock substrate. In mang
cases, particulerly those involving Calliselle limetule, forces
applied at the level of the muscle scar caused portions of the
shell margin just below the point of contact between the
simulated claw and the shell to shatter into framents. For an
actual crab attacking a limpet such as C limatule, this
fragmentation of the shell's margin might enable the crab to
reach under the shell directlg and grab the limpet's exposed
foot. Crushing attacks by crabs at the muscle scar might also
be useful for two other reasons. First, observed mang
instences where limpet shells were curved at the base to
match the substrate, making an attack at the margin more
difficult since the ends were at different heights (see also
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Morris, Abbott, and Haderlie, 1980). Despite the curve of the
margin, the rest of the shell was not changed, such that a crab
could still gresp the shell at the level of the scar. Second,
also found mang limpets with shell margins either embedded in
the rock or wedged against rocks, algae, or even barnacles. In
each of the cases a crab might experience difficulty in crushing
or prying at the margins, but in all likelihood the crab could
still squeeze a shell higher up et the scar level.
FORCE TO BREAK VERSUS SHELL THICKNESS AT THE PUSCLE
SCAR
With the exception of Acmaee mitre shells, found that
the force required to fracture limpet shells at the muscle scar
increased as the thickness at the scar increased. However,
did not discover significant differences in force/thickness
means among the three species showing significant trends in
force vs. thickness (C limatule, C. pelte, C. digitelis) This
result wes true for forces epplied at both the length and width
of the shell at the muscle scer and mergin, with the only
exception being that Calliselle digitelis shells were about 1.3
times easier to fracture at the length of the scar than
Collisella limatule shells. This outcome indicates that the
force required to fracture shells of most limpet species
depends more on the material properties of the calcium
carbonate shell than on the particular shell shape. Thus in
general tall, high-spired Acmaes mitre and low, flat Calliselle
limetule shells of similar muscle scar thicknesses will
fracture at similar crushing forces.
Within each species, shells of similer scar thicknesses
fractured along both the length and width of the muscle scar
and margin did not break at significentlg different force
ranges. Taking into account that the thickness of the shell
margin might influence the force at which margin-loaded sheil
broke by comparing force to relative thickness(scar
thickness/margin thickness) similerlg produced no significant
differences. Again the only exceptions appeared in Colliselle
limatule, where the shell broke more easily along the length of
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the margin than along the length of the scar by a fector of 1.8.
Still, it appears that a crab has no general advantage in
crushing a shell at ang one location on the shell. Thus despite
the apparent thinning of the shell at the muscle scar region,
some other factor is necessarg to make attacks at the scar
vulnerable to crabs.
In considering the dimensions of a limpet shell at both
the muscle scer and the margin, it is cleer that the grasping
orientation where a crab would have to open a cheliped least is
at the width of the scer. The width of the scar was found to be
significantlg less than the other three shell dimensions for
each of the four species, suggesting that even relativelg small
crabs could still crush large limpets by gresping them at the
Width of the scar. For example, a crab that could open a
cheliped to a maximum of 7.1 mm at the tip would still be able
grasp a 20mm long Calliselle limatule shell along the width of
the scar. Moreover, a crab with a 20mm maximum opening that
would just barelg fit the cheliped along the margin length could
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instead obtein a better grasp (apply the force with the teeth of
the claw) at the scar width. Furthermore, by gripping the shell
at the width of the scar this 2Omm long cheliped would most
likely exert a greater total force (similar to a person squeezing
an object between the fingers and palm compared to just
between two fingers). A possible conclusion is that crabs in
general can expand their food resources by crushing limpets
along the muscle scar, especiallg along the width.
The comparison of scar widths in figure 13 shows that
for shells similar in length (18-21mm) from the four species
measured Colliselle limatule has the smallest everage width
at the scar. This finding suggests that given equal numbers of
shells from these species a crab would be able to grasp and
crush more C limatule shells than ang other type. This result
might help explain why more C. limatule shells are found on
the beach having been fractured at the scar (Chapin, 1966).
Another reason that C. limatule (the "file limpet") shells might
be easier to grosp than, for instence, A. mitre shells is that
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the ribs on the back of C limatule shells offer a surfece for
crab cheliped teeth to grip, while 4. mitre shells are often
smooth and slipperg. Finallg, although the force/thickness
values were similar for each species, at a given shell length .
limatule shells have the smallest average thickness at the
scar, implying that not only could more crabs fit their chelae
around C limatule shells, but also a smaller force is necesserg
to frecture the shells.
FATIGUE FRACTURE AT THE SCAR
Fatigue fracture of limpet shells mag be important in
two manners. First, by repeatedlg loading a shell to a force
below that required to immediately fracture the shell a crab
avoids using maximum exertion, thus conserving energy in case
of a sudden emergency (such as appearance of a predator).
Also, through fatigue-loading, a small crab incapable of
exerting sufficient force to frecture the shell in one squeeze
can eventually crush a lerge limpet. The results of the fatigue
experiments show, however, that a crab must exert at least
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60-653 of the breaking force to frecture the shell within 200
cycles. This result is similar to values given by Boulding
(1986) and Curreg (1984) for fatigue in bivalves. Significantig,
if a crab can exert at least 70-752 of the predicted breaking
force, the number of cycles required for fracture decreases
typically to 50 or fewer, as shown in figure 14. As Boulding
(1986) demonstrates, mang crabs fatigue shells over periods of
hours or even dags. In this manner, a Fechygrepsus crassiges
or other crab could eventually fracture a shell (using a few¬
force pulses at a time) without remaining exposed to predators
or other adverse conditions for extended periods of time.
Although a crab will most likelg not apply the same level of
force at the same exact location each time, the total number of
cycles required will still be well below 200.
The observations of fatigue crack development show that
most cracks originate at the front of the shell just below the
muscle scer end subsequently travel around the shell along the
scor. Regions of high tensile stress were marked by white
24
lines, indicating cracks just beneath the surfece. Eventuslig
these cracks would emerge at the inner surface of the shell
along the scar, often merging and traveling down to fracture
the margin. Fatigue loading thus concentrated the stresses
along the scar, ultimatelg producing surface cracks that would
join and sever the top of the shell at the muscle scar.
SCAMMING ELECTRON MICROSCOPE OBSERVATIONS
A possible explenation to the mechanism by which shells
loaded at the margin frectured first at the muscle scar lies in
the muscle scer microstructure. Anagises of the frectured
crossed-lamellar structure at the muscle scar reveal that the
lamellee are oriented with the surface of each sheet lying
normal to the shell's outer surface. In this manner a crack mag
travel along the scer (between the primarg lamellae), leaving
behind a smooth fracture surface. This situation is analogous
to splitting plywood along the grain(Curreg, 1974,1980), in the
direction requiring the leest energg. Although a crock cen
spread between crossed-lamellar sheets for a short distance,
in most cases the lamellae change direction after a short
distence(figure 22), forcing the creck front to fork. Thus in
tupical crossed-lamellar structure a crack is halted unless the
force applied increases. However, in practicallg all the muscle
scar fracture surfaces l observed, the lamellae remained
oriented such that the crack could travel completelg around the
horseshoe-shaped scar without crossing lamellae. Even where
the fracture surface was slightly more ragged, a short distance
later the crack surface was once again smooth, having cut
across the grein briefly to where it could continue between the
sheets. Therefore, it appears that the mechanism for
pop-topping' at the muscle scar involves the crossed-lamellar
sheets and not the actual prismatic myostracum. This outcome
might be anticipated since the myostracum forms only the
inner surface of the shell. Although prisms ere stronger than
crossed-lemellar sheets (Curreg, 1988), the high tensile stress
at the inner surface of the shell is probablg sufficient to
frecture the prisms. However, it is not until the crack reaches
26
the crossed-lameller sheets that the actuel muscle scar
cleavage occurs.
FINITE ELENENT AMALYSIS GRAPHS
Comperison of the relative stresses ceused by forces
applied along the length and width of the scar and margin for
the Colliselle digitelis(figure 19) computer model reveal that
forces transmitted along the length and width of the margin
produced high compressive stresses at the level of the scar
around the front half of the shell. Although the forces applied
along the length and width of the scar produce (as expected)
higher tensile stresses at the point of application, the shells
with equivalent forces applied at the length and width of the
margin show high compressive stress at the muscle scar.
While the shell will tend to fracture at a lower stress in
tension than compression, a high compressive stress mag still
lead to fracture, especially at the scar where the shell
thickness is much smaller then at the margin. Forces applied
at the margin cause both high tensile stress at the margin and
27
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high compressive stress at the scer, resulting in frecture at
forces equal to or less than those required for frecture directig
at the scar. Further evidence showing the scar lager to be a
structurally weak region came in the Calliselle pelte rim
fracture tests (figure 11), where shells missing the top
portion(above the scar lager) fractured at the same range of
forces as intect shells fractured at the margin.
Finally, the finite element analysis graphs also
demonstrate that equal length C limatule end A mitre shells
develop verg different stress concentrations. Comperison of
figure 20 A and B (and C and D) show that at each grasping
orientation the stresses in C limatule are much greater than
those for A. mitra. Again, the most likelg explanation involves
the thinner scar lager in Calliselle limatule at equal shell
lengths. With less shell material to contain the stress, stress
levels cleerly rise in C limatule shells and cause frecture
much more quicklg.
SUMMARY
1) Shells of Colliselle pelte, Colliselle limatule, Colliselle
digitalis, and Acmaes mitre all break cleanly along the muscle
scar when crushed in a crab-like manner.
2) Colliselle pelte, C. limatule, and C. digitslis shells require
more force to break as scar lager thickness increased. A. mitre
shells show no clear trend in force vs. thickness.
3) Aside from C. digitalis being 1.3 times easier to breck along
the length of the scar then C. limatule, there were no other
significant differences in force/thickness among the species
tested.
4) Generallg no significant differences appeared for (force to
break)/(scar thickness) within each species among the four
grasping orientations. The one exception was E limatule
shells which are 1.8 times easier to fracture at the
longitudinal margin vs. longitudinal scar.
5) The width of the shell at the scar proved to be significantig
less then the other three dimensions for eoch species,
suggesting that crabs could grasp morefand larger) shells at
29
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the width of the scar
6) The width of C limstule shells at the scar was significantig
less than the other species, suggesting that more crabs are
eble to crush this species' shells at the scer since more crabs
cen actually grasp these shells et the scar width.
7) Above 602 of the predicted breaking force fatigue loading
fractured shells of C pelte and C. limatule in under 200 cycles.
Above 70-752 less than 50 cycles were necessarg, suggesting
that crabs can crush limpet shells without ever exerting 1002
of the force required to break an unfatigued shell. Also,
smaller crabs incapable of exerting 100% breaking force loads
for large shells can still crush the limpet shell
8) Fatigue cracks originate at the front of the shell and usuallt
travel along the muscle scar, eventuallg severing the top of the
shell.
9) SEH observations revealed crossed-lameller sheets at the
muscle scar oriented such that cracks mag travel between the
sheetstenergetically favorable direction) and eventuallg cause
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the 'pop-top' effect at the muscle scar.
10) Finite element analysis computer models indicate that
forces applied along the length and width of the margin produce
high compressive stresses et the much thinner muscle scer,
often ceusing frecture at the scer first. Also, the relativelg
flat C limatule shells showed higher overall tensile and
compressive stresses than the tall A. mitre shells, probebly
due to the thinner scar lager in equal-length C limatule and 4.
mitre shells.
LITERATURE CITED
Boulding, E. G.(1984). Crab-resistant features of shells of burrowing
bivalves: decreasing vulnerebilitg by increesing handling time. J. Exp.
Mar. Bio. Ecol. 76. pp 201-223
Boulding, E. G., M. Labarbere (1986). Fetigue damege: Repested loading
enables crabs to open lerger bivalves. Biol. Bull. pp 538-547
Buikleg, P. Todd( 1968). Shell damage and repair in five members of the
Genus Acmaee. The Veliger. Vol. 1 1(Supplement). pp 64-66
Chapin, D.(1968). Some observations of predation on Acmaea species bu
the creb Pachggrapsus crassipes. The Veliger. Vol. 11(Supplement).
pp 67-68
Curreg, J. D., J. D. Taglor (1974). The mechanical behavior of some
molluscen hard tissues. J. Zool. Lond. 173. pp 395-406
Curreg, J. D.(1977). Mechanical properties of mother-of-pearl in tension.
Proc. R. Soc. 196B. pp 443-463
Curreg, J. D.(1980). Mechanical properties of mollusc shell. Sump. Soc.
Exp. Biol. 34. pp 75-97
Currey, J. D., K. Brear.(1984). Fatigue fracture of mother-of-pearl and its
significence for predetorg techniques. J. Zool. Lond. 204. pp 541-543
Curreg, J. D.(1968). Shell form and strength. The Mollusca(wilbur, K. and
K. Sinkiss, eds.), Vol. 11. pp 183-208. Academic Press, Inc. Hey York.
Gordon, J. E.(1978). "Structures, or Whg Things Don’t Fall Dovin.“ Penquin
Books, Middlesex(England) and New Vork.
Lowell, R. B.(1986). Crab predation on limpets: predator behavior and
defensive features of the shell morphology of the preg. Biol. Bull.
171. pp 577-596
MecClintock, C.(1967). Shell stucture of patelloid and bellerophantoid
gastropods(Hollusca). Peabody Mus. Nat. Hist. Yale. Univ. Bull 22.
Nachleal-Schwendler (1986). "Stress And Vibration Analusis.“ The
Nacheal-Schwendler Corporation. Los Angeles, CA.
Watabe, N.(1988). Shell structure. The Mollusca(wilbur, K. and K.
Sinkiss, eds.), Vol 11. pp 69-87. Academic Press, Inc. New York.
FIGURE LEGENDS
Figure 1. Comparison of relative shell heights for the four species tested.
The shells are divided into low( C limatule), middle( C. pelte, C. digitelis)
and high(A mitra) relative heights.
Figure 2. A. Diagram indiceting varieble sheil thickness in limpet shells.
The cross-section shows that the margins and apex are thickened relative
to the muscle scar. B. Diagram of the underside of a limpet shell.
IIlustrating the horseshoe-shape of the muscle scar.
Figure 3. A. (From MacClintock, 1967). Diegram showing the orientation
of sheil lagers in e limpet shell. The leger labelled "m" is the
myostracum(muscle scar lager). B. Cross-section of the shell at the level
of the muscle scar, showing that the myostrecum originates on the inner
surface of the shell where the "scar“ appears. A crab-like force would
produce tension at the inner surface(the myostracum). P-Prisms.
CL-Crossed-lameller.
Figure 4. Bending caused by crab-like forces at the muscle scer. The
calcium carbonate shell would tend to frecture first along the inner
surface since the shell is wesker in tension than compression.
Figure 5. Photograph of limpets used in studg, showing relative height
ditferences. From left to right: C limatule, C. digitelis, A. mitre, C pelte
Figure 6. Limpet shell crusher used to frecture shells. A. Side view.
showing a loaded shell situated between two metal plates. The plates are
sttached to the large wood blocks. B: Front view. The wood block at the
left provides a substrete for the shell, preventing the sheil from slipping
to the lett. Theright side of the device is wedged against some bject to
prevent sliding to the right. C. Side view, showing two aluminum breces
attsched to the upper block. The breces prevent the upper block from
sliding over the shell(to the left or right).
Figure 7. Diegrems showing how forces were applied to shells. Diagrams
show external surface of shell from the top. A. "Front scar“ refers to a
force epplied longitudinally et the scar. B. Front margin" refers to a
force epplied longitudinallg et the mergin. C. "Lateral scar“ refers to a
force epplied laterallg et the scar. D. "Leteral mergin" refers to a force
applied laterallg et the margin.
Figure 8. Technique used to generate XVZ coordinates for the finite
element model. A. Greting(perallel bleck lines) used to project lines onto
the shells. B. Diegrem of projector set-up. The lines are projected(in e
dark room) onto the shell and the contour pattern photographed. C. Top
view of B. D. Topogrephic map obtained when contour lines from each
side of the shell are pleced next to each other. The coordinate axes pass
through the apex(at the origin). E. Final limpet modeltA mitre shown)
obteined from topographic map. The dark circles are nodal(XYz) points.
Figure 9. Graph showing the force required to fracture a shell versus the
shell thickness et the anterior end of the shell(at the level of the muscle
scar) for all four species. A. Values for all four species shown together.
B. Linear regressions for each species. The mean force/thickness values
were not significentlg different among the four species. E gigitalis:
U=135,68 434,3, r2-33, p402, n-17. C limatule. y-231 48 433.3, r4-64,
06001,n=22. A. mitre. y-95.98 480.45, r2-.13, p».05, n-11. E. pelte:
=153.0, r2=.26, p6.05, n=18.
Figure 10. Regression lines for the force required to frecture a shelltin
Newtons) plotted against the shell thickness. The force values for esch
gresping orientation(for shells frectured longitudinallg and lateralig along
the muscle scar and margin) did not differ significentlg from each öther
and are combined for each species into one date set. Breaking forces
incressed with sheil thickness in all cases except for 4 mitre. A. L.
Jimstula u- 211.98 + 14.5. r2-.49, p..001. (n=63) B. C digitelis.
U=151.38 + 21.9. r2-.30, p4.001. (n-51) C. A. mitre. g- 45.68 + 75.5. r
-.06, p».05 (n=59) D. C. pelta. y-152.98 + 41.7. ré=.28,p..001 (n-451
Figure 11. Lineer regression showing the force necessarg to fracture 2.
gelte shells both intect and without the top of the shell(such that onlg the
rim remains). Data for forces applied to each tupe of shell longitudinallg
and leterelly ere combined since the force required was essentiallg the
same in each case. g= 200x + 15. r#=.55, p..005 (n=15)
Figure 12. Graphs showing sheil length and width at the scar and margin
for A. C digitalis, B. C limatula, C. A. mitra, and D. C. pelta. In each
instance the width at the scer is significentlg smaller than the other
three orientations(p«.00 1 for all four graphs).
Figure 13. Comparison of shell length(A) and shell width(B) at the level of
the scar among the four species. Shells from each species were
approximatelg equal in length( 18-2 1mm). Both graphs indicate that #
limatule hes the smallest dimensions at the scar(among similar length
shells), with the difference being greatest at the width of the scar.
Figure 14. Fatigue loading in C limatule(A) and C. gelte(B), Shells were
odded for 5 seconds for up to a maximum of 200 cycles. When the applied
force was greater than 603 of the predicted breaking force(see figure 104
&D), fracture resulted in fewer than 200 cycles. Around 752 fewer than
50 cgcles could result in fracture.
Figure 15. Cracking patterns from fatigue-loading(longitudinallu along the
scar) in limpet shells. A. Fatigue crecks originating near the front end of
the shell, at the level of the muscle scar. B. Typical spreading of cracks
along the muscle scar. C. Later stage, showing radial cracks near the
apex. D. Stage just prior to fracture, showing crecks merging and moving
rädially toward the margin. Crecks are shown on the underside of the
shells.
Figure 15. Scanning electron micrograph of fatigue cracks. Several cracks
are shown running along the muscle scar lager(the outline of the
mgostracum is visible near the top left of the picture). Magnification
=3508.
Figure 17. Fracture along the muscle scar. A. SEM photograph of the shell
structure at the muscle scer. Surface shown is the beginning of the
muostrecum, viewed(et e slight angle) from the front and towerd the reer
of the shell. The cross-lamellar sheets originate just below the upper
(ectuelly lower on the shell) lager of prisms. B. SEM photogreph of the
fracture surface along the scar. The surface is smooth since the crack
treveled between the lamellee. C. Diegrem showing orientation of
crossed-lameller sheets at the muscle scer. The primarg lamellee run
normel to the external shell surfece, such that a crab-like force can ceuse
crecks between the sheets. Once between the lemellee the creck cen
spreed eround the shell.
Figure 18. Color scheme for the finite element analgsis stress diegrems
Velues listed ere for compressive stress in terms of the percentage of
maximum gield strength. Tensile stresses appear on the graph as white
plates with values included in the legend.
Figure 19. Stress diagrams for C digitalis compering forces applied at
the margin and scer. Forces applied et the margin produced high
compressive stresses along the scar, possibly explaining whg in these
cases the shell fractured first along the scar. A. "Front scar“ refers to a
force applied longitudinallg along the scar. B. "Front margin" refers to a
force epplied longitudinallg along the mergin. In C & D "Lateral" refers to
a force applied laterallg along the scar(C) and margin(D). Tensile
stresses(Z of gielding strength): A. 1=3.6, 2=3.3, 3=3.1, 4=3.3, 5=3.1 B.
=9.3,2=4.7, 3=6.9 C. 1=1.3, 2=6.3 D. 1=14.9, 2=11.5, 3=0.3
Figure 20. Stress diegrams compering stresses in equal length E himetule
end 4 mitre computer models. For forces applied longitudinalig along the
scar(A B) and the margin(C,D) C Jimatula shows much greater
compressive stress along both the scar and mergin. This most likeig
occurs because C limetule is much thinner than A. mitre all along the
shell. Tensile stresses(Z of gielding strength): A. 1-1.7 B. 1=2.5, 2=2.3
3=2.6,4=2.3, 5=2.2 C. 1=2.0, 2=3.0, 3=8.2 D. 1=1.9, 2=1.8, 3=1.8, 4=2.1
Fiqure 21. Limpets fractured et the muscle scer. A. Examples of shelle
crushed with the nutcracker-like device. B. Diegrem of frecture surfece.
C
Figure et the right is the top of the shell turned over to show thet frecture
occured olong the scer.
Figure 22. (Used from Curreg, 1988). A. Diegrem indicating that in
typical crossed-lemeller structure the lemellee change direction
periodicallg, forcing the crack front to divide. B. SEM photo illustrating
port 4.
O
0

L
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E


8
(HLDNHTXHAV)'LH HAILVIHA
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Figure 3
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Figure 7
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Figure 9
3n Cmera
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+
Sel cator ies


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—



DMITRAI
FORCE VS THICKNESS
FRONT SCAR
—
500
400
300
+ 0
200
f 4
4 1
kos a 40.
100 -
8E

+
0 +—
0.1 0.3 0.5 0.7 0.9
1.1 1,3 1,5 1.7
SCAR THICKNESS(mm)
+ UMATULA
MITRA
A PETA
C DIOTALIS
FORCE VS THICKNESS
FRONT SCAR
340 -
320
300
280
260
240
220 -
200

1B0 -
150

140 -
120 -

100 -
B0 -

50
40 +
1.5 1.7
0.7 0.9
1.1 1.3
0.1 0.3 0.5
SCAR THICKNESS(mm)
MITRA
A PELTA
D DIOTALIS
+ LIMATULA
Figure
2.
320 -
300-
280 -
260 -
240 -
220
200 -
180 -
150 -
140 -
120
100 -
80 -
60 4
40 +
20 +
0.1
400
350 -
300
250
200 -
150 -
100 -
50
0.2


+ *
FORCE VS THICKNESS
COLLSELLA UMATUL




0.5
0.9
0.3
SCAR OR MARGIN THICKNESS(mm)
+ ALL 4 ONENTATONS
FORCE VS THICKNESS
COLLISEA DIG LALIS

1

t1

0.6
0.8
0.4
1.2
SCAR OR MAROIN THICKNESS(mm)
+ ALL 4 ORENTATONS
Figure 10
F.
FORCE VS THICKNESS
ACMAEA MTRA
260
250 -
240 -
230 -
220-
210
200
190
180 -
170
160
150
140 -
130

120 -
110 -
100 -
+

90 -
+ 4
B0 -
+
70 -
60
50
40
0.6
0.2
0.4
0.8
SCAR OR MARGIN THICKNESS(mm)
+ ALL 4 OMENTATIONS
FORCE VS THICKNESS
COLLISELLA PETA
550 -
500
450
400
350

300
250 -
200
150 -
jo pp

+ + + 4
50
0 +
0.5
0.7
0.9
1.5 1.7
0.3
SCAR OR MARGIN THICKNESS(mm)
ALL 4 ORENTATIONS
Z
Z

L
O
L
DD

888188
aaaaa-
D
—tt-

—
8888
(N)yvaa ol soao
—
20 -
19
COMPARISON OF GRASPING ORIENTATIONS
COLUSEUA GORAES
A

A

SCAR WIOTH
MOT
SCAR LENOT
LENOTH
PONNLOE GRASPING
N=12
COMPARISON OF GRASPING ORIENTATIONS
COLUSELLA UMATULA
22
20
16
14
A
A
A

SCAR WIDTH
MDTH
SCAR LENGTH
LENGTH
ORASPINO
COMPARISON OF GRASPING ORIENTATIONS
AMAAMTR
A
A


SCAR RIOTH
LENOTA
SCAR LENOT
MOT
POINTOE, GRASPING
J N-16
COMPARISON OF GRASPING ORIENTATIONS
COLLISELLA PEIA
26 +
24
22
2
18-
16
14
12
10 -
A
V

oL
SCAR LENOT
SCAR WIDTH
MDT
LENOTH
POINT  GRASPINC
N=13
19
15
14
13-
20
19 -
18
17 -
16
15
14-
13-
12
11 -
10

UMATULA

LMATUL
COMPARISON OF SCAR LENGTHS.
ALL 4 SPECIES(18-21m LENOTH)
LA
L
PELIA
DIOTAUS
SPECIES NPE
N=5
COMPARISON OF SCAR WIDTHS
ALL 4 SPECIES(1B-21mm LENGTH)


PELIA
DIOTTALIS
SPECIES NPE
N=5

MITRA

L
MITRA
Figure 13
FATIGUE LOADING
COLSELA UTUL
200 —
190 -
180 -
170 -
160 -
150
140
130
120 -
110 -
100
90 -
80 -
70 -
60 -
50 -
40
30 -
20


10 +
—
50 63 55 71 72 75 79 81 B2 85 92 100
LOAD AS X OF PREDICTED BREAKING FORCE
FATIGUE LOADING
COLLSELLA PELTA
180
170
160
150 -
140
130
120
8. 110 -
100
90
80 -
70
60 -
50 -
40 -
30 -
20 -
10 +
65
50
75
5
LOAD AS X OF PREDICTED BREAKINO FORI
100
Fig
Figure 16
- - --.
Crossed-
anelar
sheeks
Figure 17
EE

FORCE
TAESS
Colo
Veron

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SREEN


Buoe

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Figure 18
COLoR Snen
6 of Haximom Vteld Streogt
O-OS
O5 -00
0-200
0-300
381-0
HO -5.00
5O -600
GO-7
O -8.0
80 -0

0500
50 20.00
22000
30 0
5900
o
550 0
ool-8900
85ooo
DDIGITALISI
DDIGITALISI
FRON
SCAR
FRONT
MARGIN
Figure 10
DDIGITALISI
DDIGITALISI
LATERAL
SCAR
LATERAE
MABGIN
—
—
DLIMHI
DMITRAI
FRONT
SCAG
RONT
S8
-

B
Figure 20
DLIMRI
DMITRAI
FRONT
MARGIN
FBoN
MAAGIN

D
ANT.
AN
Codecside
Post.
057.
g. 5. Diagram showing how the front edge of a crack traveling in the easy direction in
ed-lamellar structure is broken up when the orientation of the structure changes.
6

5
Tf
A



















d
H







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rig. 6. Fracture in crossed-lamellar structure. The crack traveled first between the sheets.
trom right to left, but atter the change in orientation of the sheets it had to break across them
Width of field -350 um.
8
(Caped fron Corgey
188)
Figore 22