Extreme impact and cavitation forces of a biological hammer: strike forces of the peacock mantis shrimp Odontodactylus scyllarus
Department of Integrative Biology, University of California, Berkeley, CA 94720-3140, USA
* Author for correspondence (e-mail: patek{at}berkeley.edu)
Accepted 11 August 2005
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Summary |
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Key words: stomatopoda, crustacea, fracture, biomechanics, force, impact, cavitation, mollusca, shell, evolution, peacock mantis shrimp, Odontodactylus scyllarus
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Introduction |
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Mantis shrimp (Crustacea, Stomatopoda) use their greatly enlarged second
thoracic raptorial appendages to smash or spear prey, construct and excavate
burrows, defend against predators and fight with conspecifics
(Caldwell, 1975). In `spearer'
stomatopods, the dactyl is a sharp, spiny, barbed spear, which stabs into
soft-bodied, evasive prey. `Smasher' stomatopods can stab with the sharp tip
of their dactyl or smash with the bulbous heel of the dactyl
(Fig. 1). In order to generate
extreme accelerations with their raptorial appendages, all mantis shrimp
species are thought to utilize a power amplification mechanism consisting of
elastic springs, latches and lever arms
(Burrows, 1969
;
Burrows and Hoyle, 1972
;
McNeill et al., 1972
;
Patek et al., 2004
). The click
mechanism holds the limb in place during muscle contraction
(Burrows, 1969
;
Burrows and Hoyle, 1972
;
McNeill et al., 1972
), and a
specialized spring stores and releases elastic energy
(Patek et al., 2004
). The
subject of the present study, the `smasher' peacock mantis shrimp
Odontodactylus scyllarus, can deliver strikes lasting only a few
milliseconds, with accelerations of over 105 m s-2 and
speeds of over 20 m s-1 (Fig.
1; Patek et al.,
2004
).
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When cavitation bubbles collapse, considerable energy is released in the
form of heat, luminescence and sound
(Brennen, 1995). The shock
waves and microjets generated during the collapse of the cavitation bubbles
cause stress and fatigue in adjacent surfaces, ultimately leading to failure
and flaking of surface materials (Brennen,
1995
). Remarkably, a 2.7 mmcavitation bubble collapsing near a
wall can generate over 9 MPa of impact pressure over a period of approximately
5 µs (Shima et al., 1983
;
Tomita et al., 1983
). Such
cavitation forces can destroy rapidly rotating boat propellers, aid in
water-based metal cutters, and are even thought to provide the mechanism by
which water picks remove dental plaque
(Brennen, 1995
).
Cavitation has been documented in several biological systems. Most
biological examples of cavitation are caused by low pressure fluid tension in
enclosed spaces, such as tree xylem
(Smith, 1994;
Tyree et al., 1984
;
Tyree and Sperry, 1989
),
octopus suckers (Smith, 1991
;
Smith, 1996
), human
metacarpophalangeal joints (Unsworth et
al., 1971
), fern sporangia
(Ritman and Milburn, 1990
) and
fungal spores (Milburn, 1970
;
Money et al., 1998
). By
contrast, perhaps the most dynamic example of biological cavitation is found
in snapping shrimp, which shoot cavitation bubbles to stun their prey
(Lohse et al., 2001
;
Versluis et al., 2000
). The
snapping claw closes and shoots a water jet at extreme speeds, which causes
negative pressure and associated cavitation behind the water jet
(Lohse et al., 2001
;
Versluis et al., 2000
).
Indeed, the loud popping noises heard in many oceans are generated by the
collapse of cavitation bubbles during snapping shrimp strikes
(Versluis et al., 2000
).
The presence of cavitation is often detected acoustically because the sound
of cavitation bubbles collapsing contains greater energy at higher frequencies
than similar events without cavitation
(Brennen, 1995;
Lush and Angell, 1984
;
Martin et al., 1981
). Thus,
the acoustic signature of cavitation is the presence of a broadband signal
extending, with substantial energy, into the ultrasonic range (above 20 kHz),
as compared to events without cavitation that lack power in the ultrasonic
acoustic range. This phenomenon has been examined extensively in the
engineering literature, including controlled studies in which cavitation is
present and absent, as well as correlative studies linking cavitation damage
with the acoustic power of the signal in the ultrasonic range
(Brennen, 1995
;
Ceccio and Brennen, 1991
;
Lush and Angell, 1984
;
Martin et al., 1981
).
Cavitation has also been detected via acoustic analyses, especially
in the ultrasonic range, in studies of tree xylem cavitation
(Ikeda and Ohtsu, 1992
;
Perks et al., 2004
;
Tyree et al., 1984
) and fern
sporangia (Ritman and Milburn,
1990
).
The presence and dynamics of cavitation can also be detected visually.
Extreme high-speed video is necessary to capture the microsecond timescales of
cavitation bubble formation, luminescence and collapse. Cavitation bubbles in
snapping shrimp were visualized using high-speed video, coupled with the use
of a photodector to detect the emission of luminescence
(Lohse et al., 2001). The
simple presence/absence of cavitation vapor bubbles has been examined in
x-rays of joints after knuckle-cracking in humans
(Unsworth et al., 1971
) and
light microscope images of fungal spores
(Money et al., 1998
).
Despite our rich understanding of crushing forces and their influences on shell evolution, as well as a substantial body of work on the physics of cavitation, little is known about the impact forces generated by biological hammers and biological cavitation. The mantis shrimp's unusual mechanism for breaking shells suggests fundamental questions about the amplitude of the limb impact forces and relative contribution of cavitation forces. Here, through the use of force transducers, acoustic analyses and high-speed video, we report the limb impact and cavitation forces generated by the peacock mantis shrimp Odontodactylus scyllarus. The goals of this study were to (1) visualize limb impact and cavitation while measuring forces, specifically to identify the presence and relative contribution of cavitation to force generation; (2) measure the timing and acoustic signature of impact and cavitation; and (3) measure amplitude of forces across a range of striking surface geometries in order to assess the effects of striking surface on the amplitude of cavitation and impact forces. This study provides the first in-depth examination of a biological hammer and reveals a potent combination of power amplification, extreme impact forces and cavitation dynamics.
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Materials and methods |
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Synchronous high-speed video and force sensor analysis of force peaks
Cavitation processes were visualized through the use of high-speed video.
Digital video images were collected at 100 000 frames s-1 (0.3
mm pixel-1, 10 µs shutter speed, Ultima APX high speed camera
and Multi Channel Data Link, Photron, San Diego, CA, USA) and were
synchronized with a one-axis force sensor (force range 444.8 N, upper
frequency limit 75 kHz, Model 200B02, PCB Piezotronics, Depew, NY, USA)
sampled at 100,000 samples s-1. The kinematics of the recorded
movements were analyzed using a custom computer program (Matlab v7.0.1, The
Mathworks, Natick, MA, USA). The distance moved by the limb across each frame
was calibrated, using a structure within the image sequence with known
dimensions.
Acoustic analyses of impact and cavitation
In addition to image analysis, we measured the acoustic signatures of limb
impact and cavitation. We simultaneously measured strike forces and sound when
mantis shrimp struck curved and flat force-sensor surfaces. Sounds generated
during strikes on curved and flat surfaces were measured using a hydrophone
(1170 kHz TC4013 hydrophone, 1 Hz1 MHzVP2000 voltage
preamplifier; Reson Inc., Goleta, CA, USA). Acoustic data were collected at
500 000 samples s-1, using a data acquisition board
(PCI-DAS4020/12, Measurement Computing, Middleboro, MA, USA) and custom
computer data acquisition programs (Matlab v7.0.1). The onset of the first
peak was detected automatically with a threshold of 0.05 V above the average
value of a 100-sample window. The second peak onset was set at 0.05 V above
the average value of a 40-sample window following the first peak. The second
peak duration was set to the same duration as the first peak.
The power spectral density of each acoustic peak was calculated using a multitaper method (discrete-time Fourier transform, nonparametric pmtm periodogram, Matlab v7.0.1). The short duration of the Fourier transforms resulted in a loss of low frequency resolution below approximately 2 kHz. The maximum amplitude of the acoustic data was scaled to 1 V prior to comparing the power spectral density across events. For the flat surface tests, acoustic data were collected for five individuals (35 strikes per individual). For the curved surface tests, acoustic data were collected from six individuals (421 strikes per individual).
One-axis analysis of impact and cavitation forces
We used a one-axis force sensor to measure the relative contributions of
limb impact force and cavitation force (force range 444.8 N, upper frequency
limit 75 kHz, Model 200B02, PCB Piezotronics, NY, USA). The stainless steel
force sensor had a 12.7 mm diameter load surface and a stiffness of 1.9 kN
µm-1. Data were collected at 500,000 samples s-1
using a data acquisition board (NIDAQ 6062E, National Instruments, Austin, TX,
USA). Peak forces (amplitude of force trace) and force impulse (integrated
area under a force curve; Caldwell et al.,
2004; Ozkaya and Nordin,
1999
) were analyzed using custom-designed computer analysis tools
(Matlab v7.0.1). The onset of the first peak was set as an increase of 0.05 V
above the average value of a 100-sample window. The second peak onset was set
at 0.08 V above a 40-sample average window after the first peak. The ends of
the first and second peaks were set to the same value as the onset voltage for
each peak.
Video recordings (60 frames s-1, Sony DCR-VX2100, Sony Corp., New York, NY, USA) were simultaneously collected in order to establish whether the force sensor was struck by one or both raptorial appendages. Both peaks were analyzed if only one raptorial appendage struck the force sensor. If two raptorial appendages struck the force sensor in close succession, four force peaks were logged, leading to potential ambiguity as to the source of each of the four peaks. In these cases, only the first peak was included in the analysis. Some individuals exceeded the capacity of the load cell, thus any force data that exceeded the linear range of the load cell (>445 N) wereremoved. After the overloaded data had been removed, the final dataset reported here included four individuals with 6, 12, 22 and 25 strikes per individual.
Three-axis force analyses of strikes on curved and flat surfaces
We measured the effects of surface geometry on force generation through the
use of curved and flat surfaces. For the curved sensor, we measured the radius
of curvature of a range of snails typically consumed by these mantis shrimp
and machined a curved cap for the force sensor with the average measured
radius of curvature (9.7 mm curvature; 28.5 mmsolid, 300-series stainless
steel from strike surface to sensor surface). The flat sensor was 24.1
mmx24.1 mm, with 18.1 mm solid, 300-series stainless steel from strike
surface to sensor surface.
Strike forces on curved and flat surfaces were compared using a waterproof, three-axis, piezoelectronic force sensor designed for measuring impact forces (force range 1334 N in each axis, 90 kHz upper frequency limit, <4.1% cross-talk between axes; W20M25/010G10, PCB Piezotronics). The z-axis was designated as a horizontal force `into' the sensor. The y-axis was defined as a vertical force, and the x-axis represented lateral forces.
The stainless steel sensor provided a reasonable, although not perfect,
approximation of mollusk shell material properties. For comparison, mollusk
shells have tensile strength ranging from 30167 MPa, Young's modulus of
elasticity (stiffness) 3070 GPa, and Vicker's hardness ranging from 110
to 250 kg mm-2 (Vincent,
1990). 300-series stainless steel typically has a tensile strength
(to yield) of 200300 MPa, modulus of elasticity of 193 GPa, and
Vicker's hardness of 139169 kg mm-2 (product data sheets;
Harvey, 1985
).
The peak amplitude of forces in the three axes was measured using a custom, automated computer program and forces from each axis were summed using standard vector calculations (Matlab v7.0.1). The onset threshold of the first force peak was set as 0.02 V above the average value of a 100-sample window; the onset of the second force peak was set as 0.05 V over a 40-sample average window following the first peak.
The thick and heavy steel caps on the three-axis force sensor generated long reverberations, which prevented unambiguous quantitative measurements of impulse at less than 1 ms after the initial impact. Thus, although we could measure the amplitude and the relative timing of the multiple peaks, it was not possible to report conclusive impulse data after the initial force peak. Some animals exceeded the capacity of this force sensor and these data were removed from the analyses. With these data removed, our final dataset included, for the flat sensor tests, ten individuals (520 strikes per individual) and for the curved sensor tests, six individuals (423 strikes per individual). Video recordings (60 frames s-1; Sony DCR-VX2100, Sony Corp.) were simultaneously collected in order to establish whether the force sensor was struck by one or both raptorial appendages.
Statistical analyses
Values are means ± S.D. One-way analysis of variance
(ANOVA) was used to assess individual variation in the temporal aspects of
force generation. The scaling of force with carapace length and dactyl heel
width was evaluated with a linear regression. Statistical software was used
for these calculations (JMP 5.0.1, SAS Institute, Inc., Cary, NC, USA).
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Results |
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One axis analysis of impact and cavitation forces
We used a one-axis force sensor to measure the relative contribution of
limb impact force and cavitation force, both in terms of peak force and
impulse (Fig. 6). We found that
the cavitation forces were an average of 50% of the limb impact forces, and
reached a maximum of 280% of the limb impact force within a given strike
(Table 3). The ratio of the
second peak to the first peak force was not significantly different across
individuals in the peak force, but the ratio of the second impulse to the
first impulse did vary significantly across individuals (one-way ANOVA; peak
force: P=0.8486; impulse: P=0.0004). The average time
between the first and second peak was 410±60 µs
(Table 2), with significant
differences across individuals (one-way ANOVA, P<0.0001). The
duration of the first peak averaged 49±18 µs and the second peak
averaged 66±28 µs.
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Three-axis force analyses of strikes on curved and flat surfaces
The three-axis force sensor showed that cavitation forces were typically
half the amplitude of the limb impact forces, although in some strikes, the
cavitation forces reached 140% of the limb impact forces
(Table 4). The average time
between impact and cavitation was 390±54 µs for the curved surface
and 480±71 µs for the flat surface
(Table 2). The ratio of the
second peak force to the first peak force was not consistently significantly
different across individuals (one-way ANOVA; curved cap, P=0.7264;
flat cap, P=0.0009). Time between the first and second force peak was
significantly different across individuals (one-way ANOVA; curved cap,
P <0.0001; flat cap, P=0.0015).
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Limb impact generated an average 472 N peak force summed across the three axes on the curved surface and 693 N on the flat surface, with maximum recorded forces reaching 983 N and 1501 N, respectively (Table 4). For the curved surface, animals generated peak forces of 11181917 times their body weight. With the flat surface, individuals generated peak forces of 14202624 times their body weight.
The majority of the force was delivered through the z-axis with similar force profiles for both flat and curved sensors (flat: z, 77±7%; y, 12±5%; x, 11±6%; curved: z, 79±7%; y, 12±5%; x, 9±7%; all values mean ± S.D.).
A narrow size range of animals was sampled for this study, but some size/force correlations were identified that were consistent across both log-transformed and raw data. Carapace length (range: 26.735.8 mm) was not correlated with force amplitude in the raw curved cap data; however, log-transformed data mean force was correlated with carapace length (r2=0.8332, P=0.0305, scaling exponent=1.78). Also in the curved cap data, the width of the leading surface of the dactyl heel (range: 3.75.6 mm) was significantly correlated with summed force across three axes [linear regression, maximum force: r2=0.8897, P=0.0039 (raw data) and r2=0.8902, P=0.0047, scaling exponent=2.14 (logged data); mean force: r2=0.8636, P=0.0073 (raw data) and r2=0.8274, P=0.0119, scaling exponent=1.39 (logged data)]. In the flat cap surface data, carapace length was not correlated with force (P>0.6) and, again, the dactyl heel width was significantly correlated with the summed force across three axes [linear regression, maximum force: r2=0.4827, P=0.0258 (raw data) and r2=0.5618, P=0.0126, scaling exponent=1.95 (logged data); mean force: r2=0.4772, P=0.0270 (raw data) and r2=0.5615, P=0.0126, scaling exponent=1.64 (logged data)].
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Discussion |
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In contrast to crushing and peeling mechanisms, the mantis shrimp's hammer generates forces ranging from hundreds to over a thousand Newtons, delivered over microsecond timescales (Tables 3, 4). A strike with a single appendage generates two force peaks, approximately 0.5 ms apart, with the first force peak caused by limb impact and the second peak generated by cavitation bubble collapse (Figs 2, 3, 4). A strike with both appendages, therefore, generates four force peaks in extremely rapid succession (Fig. 6), at time scales on the order of 1000 times shorter than typical, cyclically applied, crushing forces.
While the absolute values of these peak forces are well within the range of
crushing forces, mantis shrimp generate forces that are thousands of times
their body weight, exceeding, by far, previous estimates of maximum force
production (on the order of hundreds of times body weight)
(Alexander, 1985;
Taylor, 2000
). Thus, the
hammering mechanism allows mantis shrimp to generate peak forces that far
surpass the peak forces generated by shell-crushers of similar body size.
However, these high force peaks are delivered over very short time periods,
typically 49 µs and 66 µs, for the impact and cavitation forces,
respectively. As a result, the impulses of the strikes are typically on the
order of a fraction of a µNs.
Inelastic impacts on hard substrates cause a rapid change in acceleration
over a very short time period and thereby generate high peak forces and low
impulses. The material properties of a substrate can influence the recorded
peak forces, through the time course of this change in acceleration and
associated absorption of energy. Thus, the peak forces produced by mantis
shrimp in this study should be interpreted in the context of the steel
surfaces that they struck; a more energetically absorptive surface would yield
lower peak amplitudes. However, the presence of cavitation appeared not to be
influenced by the material properties of the striking surface; cavitation was
consistently observed in naturalistic strikes of force sensors and snail
shells (e.g. Figs 1,
3) and even when animals struck
rubber corks (R.L.C. and S.N.P., personal observation). It is worth noting
that the particular strategy employed by mantis shrimp, that of using
sequential applications of brief high magnitude forces, is well known to
engineers as an effective mechanism for fracturing composite materials,
specifically via rapid jets and ballistic impacts
(Meyers, 1994).
Perhaps even more surprising than the high peak forces is the observation
that mantis shrimp couple these impact forces with the implosive force of
cavitation bubble collapse. While on average the cavitation forces were half
those of the impact forces, in many cases the cavitation force actually
exceeded those of the limb's impact (Tables
3,
4). In both the thin-surface,
one-axis force sensor and the thick, solid steel, three-axis force sensors,
cavitation forces played a substantial role in force generation, suggesting
that this phenomenon is robust across surface geometries, surface thickness
and mass (Tables 2,
3,
4). The combination of impact
fractures and the surface stresses caused by cavitation may be effective for
damaging the composite, ceramic layers of a mollusk shell
(Vincent, 1990). In future
studies, it would be informative to mount strain gauge force transducers to
actual shells and to examine the relative damage imposed by limb impact and
cavitation forces, especially in relation to the material properties of a
shell. Indeed, to our knowledge, experimental tests of shell fracture
mechanics in response to hammering with an appendage have not been previously
studied.
Acoustic analyses of mantis shrimp strikes also yielded information about
the presence of cavitation. The majority of the acoustic power was contained
in the collapse of the cavitation bubble, with the acoustic power of the
cavitation bubble collapse averaging 1.21.6 times the acoustic power of
the limb impact (Table 1). The
spectral distribution of the two sound peaks differed primarily in the
ultrasonic range (Fig. 5),
thereby supporting the hypothesis that the second acoustic peak was generated
by cavitation bubble collapse, which is characterized by a broadband acoustic
signature with substantial energy into the ultrasonic range
(Brennen, 1995;
Lush and Angell, 1984
;
Martin et al., 1981
).
Ultrasonic acoustic measurements of mantis shrimp strikes may be helpful in
future studies for establishing the presence and absence of cavitation under
different depth conditions or when smashing particular substrates,
specifically through identification of two acoustic peaks and the presence of
a broadband ultrasonic signature in the second peak.
The role of cavitation and control of cavitation by biological systems
remains an interesting and wide-open area of biological research, and perhaps
it is time to consider the evolutionary history of cavitation, even if only as
an epiphenomenon. Cavitation phenomena are sensitive to ambient pressure and
impurities in the water, such that cavitation bubbles form more readily at low
pressures and in aerated and impure water (such as saltwater). Thus, it would
be interesting to incorporate depth as a factor in evolutionary analyses of
biological cavitation structures, because organisms at depths of greater than
100 m are far less likely to induce cavitation
(Smith, 1996).
The subject of this study, O. scyllarus, is a shallow water
species and is typically found to a depth of 330 m
(Ahyong, 2001;
Manning, 1967
). However, the
genus Odontodactylus includes some of the deepest living smasher
stomatopods. While most odontodactylids are found living shallower than 50 m,
O. hawaiiensis occurs to depths of greater than 100 m
(Manning, 1967
;
Retamal, 2002
) and O.
brevirostris has been reported to depths of over 400 m, although
generally this species is found in the 1540 m range
(Manning, 1967
). Most other
Gonodactyloidea smashers are found at less than 40 m, although several occur
to 80100 m and Echinosquilla guerini is found to 200 m
(Ahyong, 2001
). Some of the
deepest small gonodactylids seem to have changed their predatory behavior and
concentrate on small prey taken in the water column or prey that does not
require heavy smashing (R.L.C., personal observation). There are, of course,
multiple explanations for these depth distribution patterns. For example,
mineralization is more difficult in colder deep water, such that mollusks and
crustaceans are not as well-mineralized
(Vermeij, 1987
) and powerful
hammers may be neither necessary nor possible.
The inherent challenges in the design of a failure-resistant, biological
hammer may explain why, outside of stomatopods, relatively few species hammer
shells (Currey, 1967;
Vermeij, 1987
). It is
intriguing that mantis shrimp do not fracture their own exoskeleton during
these strikes. Mantis shrimp raptorial appendages show wear over time and they
molt regularly to grow a new exoskeleton. Nonetheless, in between molts,
smasher mantis shrimp generate tens of thousands of blows
(Caldwell et al., 1989
;
Full et al., 1989
) with a
destructive combination of high impacts and implosive cavitation events. In
addition to shell hammering, many stomatopods also strike rocks, coral and
coralline algae for den construction. This raises fundamental questions as to
the mechanical and material properties of the dactyl heel, about which we know
little.
Currey et al. (1982)
examined the raptorial appendages of an alcohol-preserved
Gonodactylus specimen and found that the outer layer of the dactyl
heel is highly calcified and covers a layer of fibrous cuticle, within which
soft tissue is located. Microhardness tests yielded higher values along the
outermost cuticular layer, as compared to the inner fibrous layer.
Interestingly, microhardness correlated positively with the ratio of
phosphorus to calcium in the heel's surface. Currey et al.
(1982
) also noted that the
outermost layer was highly brittle, but that cracks did not propagate into the
fibrous layer. Further studies of material and mechanical properties of the
mantis shrimp's limb may hold clues for engineered materials that are
resistant to both cavitation and impact forces.
It is not presently known how and whether shells respond differently to
crushing forces, impact forces and cavitation forces. Mantis shrimp evolved a
ballistic raptorial appendage during the Carboniferous
(Schöllmann, 2004, F.
Schram, personal communication), and a true smashing appendage at least by the
Eocene, in what appears to be an odotondactylid (C. Hof, personal
communication). It is possible that this unusual method of breaking snails has
played an important, but currently unexamined, role in the evolution of shell
form in stomatopod prey populations. Mantis shrimp provide a remarkable
example of biological cavitation coupled with high impact forces which, in
combination, appear to be tremendously effective in fracturing shells.
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Acknowledgments |
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Footnotes |
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References |
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Ahyong, S. T. (2001). Revision of the Australia Stomatopod Crustacea. Sydney: Australian Museum.
Alexander, R. M. (1985). The maximum forces exerted by animals. J. Exp. Biol. 115,231 -238.[Abstract]
Beal, B. F. (1983). Predation of juveniles by the hard clam Mercenaria mercenaria (Linne) by the snapping shrimp Alpheus heterochaelis Say and Alpheus normanni Kingsley. J. Shellfish Res. 3,1 -9.
Brennen, C. E. (1995). Cavitation and Bubble Dynamics. New York: Oxford University Press.
Burrows, M. (1969). The mechanics and neural control of the prey capture strike in the mantid shrimps Squilla and Hemisquilla. Z. Vergl. Physiol. 62,361 -381.[CrossRef]
Burrows, M. and Hoyle, G. (1972). Neuromuscular physiology of the strike mechanism of the mantis shrimp, Hemisquilla.J. Exp. Zool. 179,379 -394.[CrossRef]
Butler, R. W. and Kirbyson, J. W. (1979). Oyster predation by the black oystercatcher in British Columbia. Condor 81,433 -435.
Caldwell, G. E., Robertson, D. G. E. and Whittlesey, S. N. (2004). Forces and their measurement. In Research Methods in Biomechanics (ed. D. G. E. Robertson). Champaign, IL: Human Kinetics.
Caldwell, R. L. (1975). Ecology and evolution of agonistic behavior in stomatopods. Naturwissenschaften 62,214 -222.[CrossRef]
Caldwell, R. L., Roderick, G. K. and Shuster, S. M. (1989). Studies of predation by Gonodactylus bredini. In Biology of Stomatopods, Vol. 3 (ed. E. A. Ferrero), pp. 117-131. Modena: Mucchi.
Ceccio, S. L. and Brennen, C. E. (1991). Observations of the dynamics and acoustics of travelling bubble cavitation. J. Fluid Mech. 233,633 -660.
Coombs, W. P., Jr (1979). Osteology and myology of the hindlimb in the Ankylosauria (Reptilia, Ornithischia). J. Paleontol. 53,666 -684.[Abstract]
Currey, J. D. (1967). The failure of exoskeletons and endoskeletons. J. Morphol. 123, 1-16.[CrossRef][Medline]
Currey, J. D., Nash, A. and Bonfield, W. (1982). Calcified cuticle in the stomatopod smashing limb. J. Mater. Sci. 17,1939 -1944.[CrossRef]
Full, R. J., Caldwell, R. L. and Chow, S. W. (1989). Smashing energetics: prey selection and feeding efficiency of the stomatopod, Gonodactylus bredini.Ethology 81,134 -147.
Grubich, J. R. (2000). Crushing motor patterns in drum (Teleostei: Sciaenidae): functional novelties associated with molluscivory. J. Exp. Biol. 203,3161 -3176.[Abstract]
Harvey, P. D. (1985). Engineering Properties Of Steel. Metals Park, Ohio: American Society for Metals.
Herrel, A., O'Reilly, J. C. and Richmond, A. M. (2002). Evolution of bite performance in turtles. J. Evol. Biol. 15,1083 -1094.[CrossRef]
Ikeda, T. and Ohtsu, M. (1992). Detection of xylem cavitation in field-grown pine trees using the acoustic-emission technique. Ecol. Res. 7,391 -395.
Kaiser, M. J., Hughes, R. N. and Reid, D. G. (1990). Chelal morphometry, prey-size selection and aggressive competition in green and red forms of Carcinus maenas (L.). J. Exp. Mar. Biol. Ecol. 140,121 -134.[CrossRef]
Korff, W. L. and Wainwright, P. C. (2004). Motor pattern control for increasing crushing force in the striped burrfish (Chilomycterus schoepfi). Zoology 107,335 -346.[CrossRef]
Lohse, D., Schmitz, B. and Versluis, M. (2001). Snapping shrimp make flashing bubbles. Nature 413,477 -478.[CrossRef][Medline]
Lush, P. A. and Angell, B. (1984). Correlation of cavitation erosion and sound pressure level. J. Fluid. Eng. 106,347 -351.
Manning, R. B. (1967). Review of the genus Odontodactylus (Crustacea: Stomatopoda). Proc. US Natn. Mus. 123,1 -35.
Martin, C. S., Medlarz, H., Wiggert, D. C. and Brennen, C. (1981). Cavitation inception in spool valves. Trans. ASME 103,564 -576.
McNeill, P., Burrows, M. and Hoyle, G. (1972). Fine structures of muscles controlling the strike of the mantis shrimp, Hemisquilla. J. Exp. Zool. 179,395 -416.[CrossRef]
Meyers, M. A. (1994). Dynamic Behavior of Materials. New York: John Wiley and Sons.
Milburn, J. A. (1970). Cavitation and osmotic potentials of Sordaria ascospores. New Phytol. 69,133 -141.
Money, N. P., Caesar-TonThat, T.-C., Frederick, B. and Henson, J. M. (1998). Melanin synthesis is associated with changes in hyphopodial turgor, permeability, and wall rigidity in Gaeumannomyces graminis var. graminis. Fungal Genet. Biol. 24,240 -251.[CrossRef][Medline]
Moody, K. E. and Steneck, R. S. (1993). Mechanisms of predation among large decapod crustaceans of the Gulf of Maine coast: functional vs. phylogenetic patterns. J. Exp. Mar. Biol. Ecol. 168,111 -124.[CrossRef]
Ozkaya, N. and Nordin, M. (1999). Fundamentals of Biomechanics: Equilibrium, Motion and Deformation. New York: Springer.
Patek, S. N., Korff, W. L. and Caldwell, R. L. (2004). Deadly strike mechanism of a mantis shrimp. Nature 428,819 -820.[CrossRef][Medline]
Perks, M. P., Irvine, J. and Grace, J. (2004). Xylem acoustic signals from mature Pinus sylvestris during an extended drought. Ann. For. Sci. 61, 1-8.[CrossRef]
Preston, S. J., Revie, I. C., Orr, J. F. and Roberts, D. (1996). A comparison of the strengths of gastropod shells with forces generated by potential crab predators. J. Zool. 238,181 -193.
Retamal, M. A. (2002). Odontodactylus hawaiiensis Manning, 1967 (Stomatopoda, Gonodactylidae) in Chilean waters. Gayana 66,73 -75.
Ritman, K. T. and Milburn, J. A. (1990). The acoustic detection of cavitation in fern sporangia. J. Exp. Bot. 41,1157 -1160.
Schöllmann, L. (2004). Archaeostomatopodea (Malacostraca, Hoplocarida) from the Namurian B (Upper Marsdenian, Carboniferous) of Hagen-Vorhalle (NRW, Germany) and a redescription of some species of the family Tyrannophontidae. Geologie und Paläontologie in Westfalen 62,111 -141.
Shima, A., Takayama, K. and Tomita, Y. (1983). Mechanism of impact pressure generation from spark-generated bubble collapse near a wall. AAIA J. 21,55 -59.
Smith, A. M. (1991). Negative pressure generated by octopus suckers: a study of the tensile strength of water in nature. J. Exp. Biol. 157,257 -271.
Smith, A. M. (1994). Xylem transport and the
negative pressures sustainable by water. Ann. Bot.
74,647
-651.
Smith, A. M. (1996). Cephalopod sucker design
and the physical limits to negative pressure. J. Exp.
Biol. 199,949
-958.
Snyder, N. F. R. and Snyder, H. A. (1969). A comparative study of mollusc predation by limpkins, everglade kites, and boat-tailed grackles. Living Bird 8, 177-223.
Taylor, G. M. (2000). Maximum force production: why are crabs so strong? Proc. R. Soc. Lond. B 267,1475 -1480.[CrossRef][Medline]
Tomita, Y. and Shima, A. (1990). High-speed photographic observations of laser-induced cavitation bubbles in water. Acustica 71,161 -171.
Tomita, Y., Shima, A. and Takahashi, K. (1983). The collapse of a gas bubble attached to a solid wall by a shock wave and the induced impact pressure. J. Fluid. Eng. 105,341 -349.
Tyree, M. T. and Sperry, J. S. (1989). Vulnerability of xylem to cavitation and embolism. Annu. Rev. Plant Physiol. Plant Mol. Biol. 40,19 -38.[CrossRef]
Tyree, M. T., Dixon, M. A., Tyree, E. L. and Johnson, R. (1984). Ultrasonic acoustic emissions from the sapwood of cedar and hemlock. Plant Physiol. 75,988 -992.
Unsworth, A., Dowson, D. and Wright, V. (1971). `Cracking joints': A bioengineering study of cavitation in the metacarpophalangeal joint. Ann. Rheum. Dis. 30,348 -358.[Medline]
Vermeij, G. J. (1987). Evolution and Escalation: An Ecological History of Life. Princeton: Princeton University Press.
Vermeij, G. J. and Currey, J. D. (1980). Geographical variation in the strength of thaidid snail shells. Biol. Bull. 158,383 -389.
Versluis, M., Schmitz, B., von der Heydt, A. and Lohse, D.
(2000). How snapping shrimp snap: through cavitating bubbles.
Science 289,2114
-2117.
Vincent, J. (1990). Structural Biomaterials. Princeton: Princeton University Press.
Voight, J. R. (2000). A deep-sea octupus (Graneledone cf. boreopacifica) as a shell-crushing hydrothermal vent predator. J. Zool. 252,335 -341.[CrossRef]
Walker, J. D. (1975). Karate strikes. Am. J. Phys. 43,845 -849.
Wilk, S. R., McNair, R. E. and Feld, M. S. (1983). The physics of karate. Am. J. Phys. 51,783 -790.
Young, F. R. (1999). Cavitation. London: Imperial College Press.
Zipser, E. and Vermeij, G. J. (1978). Crushing behavior of tropical and temperate crabs. J. Exp. Mar. Biol. Ecol. 31,155 -172.[CrossRef]
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