Integrating the Physiology, Mechanics and Behavior of Rapid

AMER. ZOOL., 32:382-395 (1992)
Integrating the Physiology, Mechanics and Behavior of
Rapid Running Ghost Crabs: Slow and Steady Doesn't
Always Win the Race1
Department of Integralive Biology, University of California at Berkeley,
Berkeley, California 94720
SYNOPSIS. In 1979 Bliss predicted that, "land crabs are and will undoubtedly continue to be promising objects of scientific research." Studies of
rapid running ghost crabs support her contention and have resulted in
several general findings relating to locomotion and activity. 1) Energy
exchange mechanisms during walking are general and not restricted to
quadrupedal and bipedal morphologies. 2) "Equivalent gaits," such as
trots and gallops, may exist in 4-, 6- and 8-legged animals that differ
greatly in leg and skeletal {i.e., exo- vs. endoskeletal) design. These findings
support the hypothesis that terrestrial locomotion in many species can
be modeled by an inverted pendulum or spring-mass system. 3) An open
circulatory system and chitin-covered gills do not necessarily limit the
rate at which oxygen consumption can be increased or the factorial increase
in oxygen consumption over resting rates. 4) Interspecific and intraspecific
{i.e., ontogenetic) scaling of sub-maximal oxygen consumption and maximal aerobic speed can differ significantly. 5) Locomotion at speeds above
the maximal aerobic speed requiring non-aerobic contributions may be
far more costly than can be predicted from aerobic costs alone. The cost
of transport may attain a minimum at less than maximum speed. 6) The
speed which elicits maximal oxygen consumption during continuous exercise is attained at moderate walking speeds in crabs and probably other
ectotherms. Speeds 15- to 20-fold faster are possible, but cannot be sustained. 7) The low endurance associated with the low maximal oxygen
consumption and maximal aerobic speed of ectotherms moving continuously can be increased or decreased by altering locomotor behavior and
moving intermittently. Ectotherms can locomote at high speeds and travel
for considerable distances or remain active for long periods by including
rest pauses. Alternatively, intense activity with extended exercise periods
or with short pause periods may actually reduce behavioral capacity or
work accomplished relative to continuous activity during which the
behavior is carried out at a lower intensity level without pauses.
Crabs engage in daily or seasonal journeys
In 1979 Bliss outlined the morphological, J° spawn (Cargo, 1958; Saigusa, 1981; Wilphysiological and behavioral "solutions" to be , r and Herrnkind, 1986), to reduce physthe problems of terrestrial life in crabs. In iological stresses such as temperature and
particular, she documented the importance salinity fluctuations and mechanical disturof activity and locomotion in dealing with b a n c e ^ d w a r d s ' 195*> W l l b l r a n d , H e r r n ;
predators, dehydration and reproduction, ^nd, 1986), and to feed (Rangeley and
Thomas, 1987). Crab movements can be
grouped into three general categories (Hill,
1978); 1) long distance migration, often a
to reproduction in the sea, 2) freeof Zoologists, 27-30 December 1990, at San Antonio, ranging movements, such as those involved
in foraging activity, and 3) restricted move382
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ments near the home site, including construction and defense of burrows.
During long distance migrations, mature
female blue crabs may travel as far as 1,000
m per day to reach spawning areas (Cargo,
1958). Christmas crabs, Gecarcoidea natalis,
travel hundreds of meters to mate and
release larvae during their annual terrestrial
migration (Hicks, 1985). Short-distance
journeys away from the burrow or home site
provide crabs with access to food and the
opportunity to investigate the local area
while remaining within safe distance of a
refuge. Sand crabs, Scopimera inflata,
deposit feed as they repeatedly move short
distances (0.5 m) to and from their burrow
(Fielder, 1970). Soldier crabs, Mictyris longicarpus, forage for about 1 to 2 hr during
a single tidal cycle, alternating periods of
walking and feeding. After feeding, armies
of soldier crabs wander over distances in
excess of 400 m at average speeds of 0.15
m sec"1 before returning to their home site
(Cameron, 1966).
In addition to low intensity activity, several species of crab are also capable of rapid
responses to escape from predators, capture
prey, and defend territories. Land crabs can
run from birds, larger crabs and other species that act as predators (Cameron, 1966;
Hughes, 1966; Knopf, 1966; Wolcott, 1978;
Beeveretal., 1979;Trott, 1988). Other crabs
are effective at catching fast moving prey
(Hughes, 1966). Since territoriality is common in ocypodids (e.g., Uca and Ocypode),
intense activity can occur during burrow
defense (Dunham and Gilchrist, 1988).
When an intruder tries to enter another
crab's burrow, the result can be an aggressive interaction that can involve rapid
movements or lead to the use of force.
Among crabs in general, ghost crabs in
the genus Ocypode have been particularly
valuable experimental animals for studies
of locomotion and typify the Krogh Principle, "For many problems there is an animal on which it can be most conveniently
studied." Ghost crabs can search for prey
on open beaches and forage as far as 300 m
a night (Wolcott, 1978). They also possess
the capacity for high intensity activity. A
resident at the mouth of a burrow often
responds to an intruder by "pouncing"
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(Evans et ai, 1976). The ghost crab, Ocypode, is the fastest crustacean observed to date,
moving at speeds in excess of 3 m sec"1 on
hard surfaces (Hafeman and Hubbard, 1969;
Burrows and Hoyle, 1973). As the French
naturalist Bosc noted in 1802, "when they
fear some danger, they save themselves by
walking sideways into their burrow with such
rapidity that this naturalist was a long time
observing them before forming an idea about
the species of animal which was fleeing
before him; it finally took a horse to procure
several specimens of them, again after several futile attempts. One knows well than
an animal so difficult to catch cannot serve
commonly as nourishment; thus in Carolina
no one makes any use of them" (quoted in
Milne and Milne, 1946). Ghost crab locomotion has been examined to test hypotheses in neurobiology, biomechanics, and
exercise physiology.
Because of their locomotor capacity, the
study of eight-legged, sideways movement
has proved to be important in the search
for general principles amidst the spectacular
diversity in locomotor morphology, physiology and behavior. The results of many of
these studies have been reviewed by Herreid
and Full (1988) in The Biology of Land Crabs
(Burggren and McMahon, 1988). In the discussion that follows, we will integrate data
from various areas in an attempt to provide
a more complete picture of crab and animal
locomotion. In doing so, we will highlight
the general principles of locomotion that
have arisen from studies on ghost crabs
(Ocypode quadrata), discuss predictions
from laboratory studies as they pertain to
ghost crab locomotion in every day life and,
finally, suggest areas for future study.
For the most part, laboratory studies on
ghost crabs and most other animals have
elucidated the relationships between morphology, physiology and performance during steady-state, continuous locomotion. We
will summarize these advances, but emphasize the transition from continuous activity
to intermittent and high speed locomotion.
Recent research on ghost crab exercise has
revealed that this transition is an important
factor in assessing the limits of performance. Studies of intermittent locomotion,
in particular, have demonstrated the essen-
similar to a trot, the only difference being
the lack of an aerial phase. The absence of
an aerial phase does not appear sufficient to
exclude a gait from being considered a run
(McMahon, 1985; McMahon et al, 1987).
Since gait changes in ghost crabs can occur
At speeds less than 0.4 m sec"1, 30 g ghost without any obvious change in stepping patcrabs walk (Blickhan and Full, 1987). Walk- tern and a running gait may not require an
ing crabs use an alternating tetrapod gait aerial phase, gaits may be best denned by a
(Barnes, 1975; Clarac, 1981). Legs 2-5 are more complete quantification of locomotor
coordinated so that two sets of walking legs dynamics (i.e., kinetics and kinematics).
alternate, R2 L3 R4 L5 with L2 R3 L4 R5
(R = right side; L = left side). Each set of Galloping
legs functions as an inverted pendulum over
Ghost crabs are capable of high speeds
which the crab vaults. Potential energy of (i.e., 3-4 m sec"1; Hafeman and Hubbard,
the body or center of mass fluctuates out of 1969; Burrows and Hoyle, 1973). As their
phase with forward kinetic energy. Vaulting generic name (Ocypode—swift of foot) sugover stiffened legs conserves mechanical gests, they are among the fastest terrestrial
energy that would otherwise be generated invertebrates. At speeds greater than 0.8by muscles. The maximum energy exchange 0.9 m sec"1, ghost crabs run fast or gallop
in ghost crabs of 55% at 0.2 m sec"1 is sim- (Blickhan and Full, 1987). Fluctuations of
ilar to that found in birds and mammals the body's potential and kinetic energy
(Fig. 1A; Cavagna et al, 1977; Heglund et remain in phase (Fig. 1 A). The stepping patai, 1982). Pendulum-like exchange between tern becomes altered, muscle electrical
kinetic and potential energy appears to be activity is changed and leg five and somea very general mechanism that is not times four are held off the ground and do
restricted to a particular skeletal type (exo- not participate in locomotion (Burrows and
skeleton vs. endoskeleton), number of legs, Hoyle, 1973). Stride frequency becomes
or leg position relative to the body (sprawled independent of speed (Fig. 1B). Faster speeds
vs. upright).
are attained by leaping and taking longer
strides. Aerial phases appear. Strain (i.e.,
deformation under stress) in the exoskeleAt speeds greater than 0.4 m sec ', ghost ton of legs changes significantly at the trotcrabs trot or run slowly (Blickhan and Full, gallop transition as it does in bones of horses,
1987). Energy recovery from pendulum-like dogs and goats (Biewener and Taylor, 1986).
exchange is reduced (Fig. 1A), despite the Although mammals and crabs alter musfact that the stepping pattern is not altered. culo-skeletal function at this transition
In a trot, fluctuations of the body's potential speed, differences in skeletal design are
and kinetic energy shift from being out of apparent since relative peak strain in the
phase, as in the walking gait, to being largely crab exoskeleton increases over that
in phase. The synchronous oscillation of the observed in a walk or trot in contrast to
body's potential and kinetic energy is anal- galloping mammals in which endoskeletal
ogous to a bouncing ball or pogo stick. Stride strain decreases (Fig. 1C; Full etal, 1991).
frequency increases linearly with speed as
Studies on ghost crab locomotion have
seen in trotting quadrupedal mammals (Fig. suggested the possibility that "equivalent
IB; Heglund et al, 1974). Moreover, the gaits" exist in species that differ greatly in
time course and relative magnitude of morphology and physiology. The change in
ground reaction forces are remarkably sim- gait from a trot to a gallop occurs at almost
ilar to those found in trotting quadrupedal the identical speed and stride frequency premammals (Cavagna et al, 1977; Heglund dicted for the trot-gallop transition of a quaetal, 1982; Blickhan and Full, 1987). Ghost drupedal mammal of the same mass (Hegcrabs clearly use a running or bouncing gait lund et al, 1974; Heglund and Taylor, 1988;
tial role of behavior and have even led to a
challenge of Aesop's fable, The Hare and
Tortoise (1947).
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60 -r*—Walk
40 .
Q o
oQ °
Speed (m/sec)
Speed (m/sec)
o° Oc *of
5° "• •
Speed (m/sec)
FIG. 1. Biomechanics of ghost crab locomotion. A. Energy recovery as a function of speed in 27 g crabs
(Blickhan and Full, 1987). A value of 100% would indicate complete transfer between kinetic and gravitational
potential energy, as in a ideal pendulum. Ghost crabs recover the maximum amount of energy (55%) at 0.2 m
sec 1 . B. Stride frequency as a function of speed in 27 g crabs. The transition from a trot to a gallop occurs at
nearly the same speed and frequency as the trot-gallop transition in quadrupeds. C. Peak strain in the exoskeleton
as a function of speed in 14 g crabs. During a gallop, the relative peak strain of the meropodite of the second
"walking" leg increases significantly over that observed in a walk or trot. Note that the walk-trot and trot-gallop
transitions occur at slower speeds in 14 g crabs compared to medium-sized, 27 g, crabs (Full et al., 1991).
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Full, 1989). These studies have led to further research on six-legged locomotors,
insects. Research on the mechanics of cockroaches has shown that 2-, 4-, 6- and
8-legged animals can generate comparable
ground reaction force patterns (Full and Tu,
1990, 1991). Despite the obvious diversity,
all can run or bounce in a similar manner.
A mass on top of a spring appears to be an
appropriate starting point for a model of
terrestrial locomotion (McMahon, 1985;
Blickhan, 1990; McMahon and Cheng,
Aerobic metabolism
Ghost crabs increase oxygen uptake rapidly at the onset of exercise (Full and Herreid, 1983; Full, 1987). The time required
to attain 50% of the steady state oxygen
consumption (i.e., 30-60 sec) is within the
range observed for mammals and insects
(Full, 1987). This suggests that reliance on
chitin-covered gills and an open circulatory
system does not necessarily restrict a rapid
aerobic response, despite the fact that other
exercising crabs show far more sluggish aerobic kinetics (Wood and Randall, 1981a;
Herreid etal, 1983; Full and Herreid, 1984;
Full et al., 1985). Below speeds that elicit
maximal rates of oxygen consumption (i.e.,
less than 0.2 m sec"1), the energy required
by ghost crabs for sustained, constant speed
locomotion is supplied by aerobic ATP production (Fig. 2A). Steady-state oxygen consumption increases linearly with speed in
ghost crabs as is typical for most pedestrians.
Anaerobic metabolism
Accelerated glycolysis in ghost crabs contributes little to energy production during
steady-state, submaximal exercise, even at
speeds that elicit 70-90% of the maximal
oxygen consumption (Full, 1987). As in
other species, rapid glycolysis does occur at
the onset of submaximal exercise (i.e., the
first 5-10 min). Surprisingly, lactate removal
in ghost crabs can actually exceed production during exercise and can result in a
decrease in whole body lactate after 10-15
min. Other crab species show a far greater
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reliance on anaerobic metabolism even during submaximal exercise (Burke, 1979;
Wood and Randall, 19816; Full and Herreid, 1984). Whole body lactate continues
to increase in fiddler crabs throughout a 15
min exercise bout and is associated with a
very slow increase in oxygen uptake (Full
and Herreid, 1984).
At speeds greater than the speed that elicits the maximal rate of oxygen consumption
(i.e., maximum aerobic speed or greater than
0.2 m sec"1 for a medium-sized ghost crab
at 24°C), ghost crabs rely primarily on nonaerobic energy sources (Fig. 2A). Crabs
exercising at the walk-trot transition (i.e.,
0.4 m sec"1) show large increases in muscle
lactate and a significant depletion of arginine phosphate (Full and Prestwich, 1986).
The rate of lactate production and arginine
phosphate depletion increases further during exercise at faster speeds that fall in the
middle of the trotting gait (i.e., 0.6 m sec"1).
The contribution of ATP from aerobic
metabolism may actually decrease at these
high speeds because the maximal rate of
consumption is not attained before fatigue.
Conservative estimates of the total cost of
locomotion at mid-trot speed reveal an 35fold increase above resting rates (Fig. 2A).
By contrast, extrapolation of the aerobic cost
to mid-trot speed shows only a 17-fold
increase. Locomotion at speeds greater than
the maximal aerobic speed can be far more
costly than can be predicted from aerobic
costs. The total energy utilization rate may
increase curvilinearly as speed is increased.
Minimum cost of locomotion
At speeds less than the maximal aerobic
speed, the energetic cost of travelling a given
distance (i.e., the cost of transport) decreases
and approaches a minimum (Fig. 2B). By
the standard comparison of the minimum
cost of transport (i.e., the slope of the steadystate oxygen consumption vs. speed function; Taylor et al., 1970), ghost crabs fall
within the 95% confidence limits for all
pedestrians of the same body mass (Full,
1987). Despite running sideways with eight
armored legs, cost is similar to 2-, 4-, 6-,
8-, 40- and even 100-legged travelers (Full,
1989; Full etal., 1990).
The minimum cost of transport evalua-
0.2 -
0.1 •
Extrapolated Minimum
Cost of Transport
Speed (m/seo)
Speed (m/sec)
FIG. 2. Locomotion energetics of the ghost crab. A. Aerobic, high energy phosphate, and glycolytic contributions
in walking and trotting crabs (27 g; Full and Prestwich, 1986). The total number of ATP equivalents increases
non-linearly at speeds above that which elicit maximal oxygen consumption. B. Total cost of locomotion as a
function of speed for 27 g crabs. The total cost of transport includes estimates of glycolytic and high-energy
phosphate contributions. The total cost of transport is minimal at the maximum aerobic speed. C. Endurance
or time to fatigue as a function of speed for 27 g crabs. Endurance decreases exponentially above the speed
which elicits maximal oxygen consumption, the maximum aerobic speed (Full, 1987).
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tion is typically restricted to aerobically
supported speed ranges (Taylor et al., 1970;
Heglund et al., 1982). This speed range is
narrow for ghost crabs and most other ectotherms relative to endotherms. If total cost
per distance is considered for ghost crabs,
then a minimum appears to be attained in
the middle of the walking gait where exoskeletal strain is low, maximum mechanical
energy exchange occurs, maximum oxygen
consumption is attained, and non-aerobic
sources are not heavily depended upon.
Total cost of transport is minimized at midwalking speed because of the curvilinear
function of total cost and speed, which is
similar to the function observed in swimming fish.
Effect of growth and body mass
The large size range of ghost crabs (i.e.,
2-70 g) provides a unique opportunity to
test whether intraspecific scaling of aerobic
cost follows the trends observed for interspecific variation. Mass-specific resting and
maximal oxygen consumption decrease with
body mass intraspecifically, as observed
interspecifically (Fig. 3A). When crabs grow,
their mass-specific minimum cost of transport (i.e., slope of the mass-specific, steadystate oxygen consumption vs. speed function) decreases and follows the interspecific
relationship which predicts the cost of over
150 pedestrian species (Full, 1989). The
y-intercept of the mass-specific, steady-state
oxygen consumption vs. speed function does
not scale as predicted. At slow walking
speeds, large crabs (71 g) consume as much
oxygen per unit mass as crabs less than one
half their mass (Full, 1987). The higher than
predicted aerobic cost of exercise in large
crabs is significant, not only because of the
consequences of the greater cost, but perhaps more importantly because the elevated
cost affects endurance. As has been shown
in lunged and lungless salamanders, aerobic
cost and maximal oxygen consumption
interact to determine the speed at which
maximal oxygen consumption is attained
(Full et al., 1988). High aerobic costs of
locomotion result in maximal oxygen consumption rates being attained at relatively
low speeds and lead to an increased reliance
on anaerobic metabolism.
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Effect of temperature
Ghost crabs acclimated at 24°C reach
thermal equilibrium with the environment
at ambient temperatures (Tamb) of 15 and
24°C. Steady-state oxygen consumption
decreases significantly from 24 to 15°C (Fig.
3B). The decrease is due to lower resting
rates of oxygen uptake and a lower y-intercept of the steady-state oxygen consumption vs. speed function. The minimum cost
of transport (i.e., the slope of the steadystate, oxygen consumption vs. speed function) does not change. The independence of
the minimum cost of transport with changes
in temperature has been shown in both vertebrates (John-Alder and Bennett, 1981;
Rome, 1982) and arthropods (Herreid et al.,
1981; Full and Tullis, 1990). At Tamb of 30°C
and a low relative humidity, body temperatures of ghost crabs are only 24°C (Weinstein and Full, 1990&), indicating the capacity to maintain body temperature by
evaporative cooling. Steady-state oxygen
consumption at an ambient temperature of
30°C only increases 1.8-fold at faster speeds,
despite the fact that the ghost crab's body
temperature is the same as at an ambient
temperature of 24°C where oxygen consumption increases 6.5-fold. Dehydration,
as well as temperature, may have substantial effects on gas transport. Relatively slow
speeds may require anaerobic metabolism
due to the dehydration.
Maximal oxygen consumption
At speeds eliciting oxygen consumption
rates that are maximal, endurance of the
ghost crab declines and locomotion is considered unsustainable (Fig. 2C). All else
being equal, animals with greater aerobic
capacities will be able to sustain higher
speeds. Ghost crabs can attain maximal rates
of oxygen consumption that are similar to
those measured in other ectotherms, such
as lizards (Bennett, 1982). Using chitin-covered gills and an open circulatory system
does not necessarily restrict the capacity for
oxygen uptake. Ghost crabs can increase
oxygen consumption as much as 12-fold
over resting rates (Full and Herreid, 1983),
Effect of Growth
Effect of Temperature
0 8-i
£ .^
I D\
amb= 3 0 O C
\ 24°C
Speed (m sec" 1 )
\ 30°C
Speed (m sec" 1 )
FIG. 3. Effect of growth and temperature on the locomotion energetics of ghost crabs. A. Steady-state oxygen
consumption as a function of speed for 2, 27, and 71 g crabs (Full, 1987). Maximum aerobic speed (i.e., the
speed which elicits maximal oxygen consumption, MAS) is the highest in 27 g crabs. The mass-specific minimum
cost of transport (slope of line) decreases with an increase in body mass. B. Steady-state oxygen consumption
as a function of speed and ambient temperature for 27 g crabs (Weinstein and Full, 1990b). Maximum aerobic
speed and maximal oxygen consumption are greatest at an ambient temperature of 24"C. C. Endurance time as
a function of speed for 2, 27, and 71 g crabs. Endurance capacity is correlated with maximum aerobic speed.
Crabs of 27 g show the greatest endurance capacity. D. Endurance time as a function of speed and ambient
temperature for 27 g crabs. Endurance capacity was correlated with maximum aerobic speed. Crabs show the
greatest endurance at an ambient temperature of 24°C.
an aerobic factorial scope comparable to that
of exercising lizards and mammals (i.e., 5to 15-fold; Bennett, 1982; Taylor et al,
1980). In contrast to ghost crabs, most other
crustaceans have a more modest capacity to
increase oxygen consumption (i.e., 2- to
6-fold; McMahon, 1981).
endurance declines (Fig. 2C). In ghost crabs
speeds that are two or three times the maximal aerobic speed can only be maintained
for 50 and 36 seconds, respectively (Full
and Prestwich, 1986). Speeds 15 to 20 times
the maximal aerobic speed are possible, but
can only be maintained for a few seconds
(Full and Prestwich, 1986).
Maximal aerobic speed
Maximal aerobic speed (i.e., the speed at
which maximal oxygen consumption is
attained; John-Alder and Bennett, 1981) is
highly correlated with sustainable activity.
When speed is increased and maximal rates
of oxygen consumption are approached,
Effect of growth and body mass
As ghost crabs grow, mass-specific maximal oxygen consumption decreases in parallel with resting oxygen uptake (Full, 1987).
Intraspecific scaling of maximal oxygen
consumption in ghost crabs follows a func-
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tion similar to interspecific scaling in lizards
(Bennett, 1982) and mammals (Taylor et
al., 1980).
Maximal rates of oxygen consumption
alone are an insufficient predictor of sustainable activity (Full et al, 1988). It is the
interaction of the cost of locomotion and
maximal oxygen consumption that determines the maximum aerobic speed. Small
ghost crabs (<2 g) have the highest rates of
mass-specific maximal oxygen uptake, but
also have the greatest mass-specific cost of
locomotion (i.e., submaximal oxygen consumption) relative to larger crabs (Fig. 3A).
As a result, small ghost crabs attain maximal oxygen consumption at relatively low
speeds (i.e., they have a low maximal aerobic speed). Intermediate sized crabs (~27
g) have a mass-specific, maximal oxygen
consumption and cost of locomotion that
are greater than those of the largest crabs,
but less than those of the smallest crabs.
Large ghost crabs (5:71 g) have the lowest
rates of mass-specific, maximal oxygen
uptake and the lowest mass-specific cost of
locomotion. However, the largest crabs do
not have the greatest maximal aerobic speed
as predicted from interspecific scaling.
Because the mass-specific cost of locomotion in the largest crabs (i.e., y-intercept) is
somewhat greater than predicted from
interspecific scaling relationships, the largest crabs attain maximal rates of oxygen
consumption at speeds that are less than the
intermediate sized animals, and have lower
endurance (Fig. 3C). Intermediate sized
crabs actually have the greatest maximal
aerobic speed and the greatest endurance.
Effect of temperature
Locomotor endurance is highly dependent on ambient temperature in ectotherms
(John-Alder and Bennett, 1981; Full and
Tullis, 1990). In ghost crabs, decreases in
maximal oxygen consumption and maximal aerobic speed at 15CC are correlated
with a lower endurance than at 24°C (Fig.
3D). Resting metabolic rates are similar at
an ambient temperature of 24 and 30°C, but
maximal oxygen consumption, maximal
aerobic speed, and consequently, endurance, are significantly reduced when ambient temperature is 30°C (Fig. 3D). Since body
temperature is the same at 24 and 30°C,
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dehydration may have adverse effects on
stamina. The endurance of constant speed
exercise is greatest when ambient temperature is 24°C.
For ghost crabs living on exposed sandy
beaches, the burrow provides safety from
extreme environmental fluctuations, predators, and competitors (Lighter, 1974).
When the ghost crab, Ocypode ceratophthalmus, emerges from its burrow, it makes several short trips within a few meters of the
burrow before venturing over greater distances (Hughes, 1966). In Ocypode kuhlii,
these short forays last an average of 90 sec
(Evans et al., 1976). Several species of ghost
crab actively search for live prey (e.g., small
crustaceans, including juvenile Ocypode, and
mollusks; Hughes, 1966; Wolcott, 1978;
Trott, 1988). Long distance foraging in
Ocypode quadrata generally occurs within
several hundred meters of the burrow (Wolcott, 1978). Even during the longest journeys, ghost crabs appear to make frequent
starts and stops. As do most animals, they
move intermittently. Yet, as we have already
discussed, many proposed limitations of
terrestrial locomotion are based on steadystate, continuous activity. Results from
studies on steady-state exercise have been
used 1) to propose design constraints for
oxygen transport (Weibel and Taylor, 1981),
2) to advance hypotheses concerning the
evolution of endothermy (Bennett and
Ruben, 1979) and 3) to predict natural
locomotory behavior (Bennett et al., 1984;
Hertz et ai, 1988). These and other proposed performance or design constraints
based solely on steady-state locomotion may
require revision when results are obtained
from intermittent exercise. Alternating
periods of high-intensity exercise with pause
periods, during which low-intensity or no
work is done, can alter metabolic responses
and endurance (see review by Sal tin et al.,
Endurance and distance capacity
Ghost crabs fatigue after 41 min of continuous walking at 0.15 m sec 1 , a total distance of 372 m (Weinstein and Full, 1990a,
% Vo o
at a n
average speed of
0.15 m s
68 % (2 min / 2 min)
9 9 % (30 s/30 s)
Vo 2 max I
2 min / 2 min
30 s / 30 s
Maximum Aerobic
Speed (m sec
FIG. 4. Effect of intermittent locomotion on relative workload in ghost crabs. Steady-state oxygen consumption
of continuous locomotion increases linearly with speed (solid line) for 27 g crabs until it attains a maximum
rate (VO2max) at the maximum aerobic speed. Continuous locomotion at 0.15 m sec' requires 84% V02max.
Crabs increase their effective VO2max and maximum aerobic speed (right most dashed line) by exercising
intermittently using 2 min exercise and pause periods. A submaximal workload of 0.15 m sec"1 becomes a
smaller fraction (68%) of the effective maximal rate of oxygen consumption during intermittent exercise. Intermittent exercise at an average speed of 0.15 m sec"' using 30 sec exercise and pause periods decreases the
effective VO2max and maximum aerobic speed (left most dashed line). The workload at these shorter intervals
is equivalent to 99% VO2max.
1992; Table 1). A speed of 0.15 m seer1 is
below the speed at which maximal oxygen
consumption is attained. Crabs exercising
at 0.30 m sec"1, a speed above the maximal
aerobic speed, can only sustain this speed
for 7.5 min, a distance of 135 m. If locomotion is done intermittently by alternating
2 min bouts of exercise at 0.30 m sec"1 with
2 min pauses, then crabs fatigue after 87
min, a total distance of 787 m. Using this
protocol, crabs can exercise at a speed (0.30
m sec"1) above the maximal aerobic speed
repeatedly as long as pauses are included.
Distance capacity (i.e., distance traveled to
fatigue) increases by 5.8-fold compared to
continuous exercise at this speed, and by
2.1 -fold compared to continuous exercise at
the same average speed (0.15 m sec"1). Exercise periods of 3, 4, and 5 min (exercise/
pause duration = 1) decrease distance
capacity relative to continuous exercise at
the same average speed. When shorter pause
periods (0.5 and 1 min) are alternated with
2 min exercise periods, distance capacity
also decreases.
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"Altering" the maximal aerobic speed
Relative to continuous locomotion, distance capacity can be increased or decreased
by moving intermittently (Weinstein and
Full, 1992; Table 1). Particular exercise and
pause periods can increase the effective
maximum aerobic speed of a ghost crab (Fig.
4). Crabs can travel the same distance in a
given time period without fatiguing by
moving rapidly at speeds above that which
elicits maximal oxygen consumption as long
as pauses are included. Intermittent locomotion can decrease the relative work load
at a given speed. A speed that requires 84%
of maximal oxygen consumption during
continuous walking may only demand 68%
of the effective maximal oxygen consumption if a crab walks twice as fast, but rests
half the time (2 min exercise, 2 min pause).
These results suggest that the limitations
associated with low maximal oxygen consumption and maximal aerobic speed of
ectotherms (i.e., relative to endotherms) can
be reduced by simply adopting a different
locomotor behavior. In addition to the
TABLE 1. Distance capacity during intermittent exercise.
Total distance travelled before fatigue (m)
duration (sec)
duration (sec)
Intermittent exercise
Continuous exercise
at same AvS
371.6 ± 42.6
371.6 ±42.6
371.6 ±42.6
371.6 ±42.6
371.6 ±42.6
Continuous exercise
at same AbS
134.7 ±
134.7 ±
134.7 ±
134.7 ±
Distance capacity for intermittent exercise and continuous exercise are given as mean ± SE (Weinstein and
Full, 1992). The absolute speed (AbS) for each intermittent protocol is 0.30 m sec"1 (n = 5). n = 11 for continuous
exercise at the same AbS. Distance capacity for continuous exercise at the same average speed (AvS; 0.15m
sec"') is recalculated from data reported by Full (1987) over the range of speeds from 0.13—0.19 m sec"1.
" Significantly different from the distance capacity at the same AvS (P < 0.05).
Significantly different from the distance capacity at the same AbS (P < 0.05).
advantages in distance capacity, intermit- metabolites in ghost crabs taken at the end
tent behavior allows time for sensing the of exercise and pause intervals suggest that
environment or performing other less stren- 120 sec pause periods are adequate for some
uous behaviors during the pauses.
lactate clearance and phosphagen repletion,
Other combinations of exercise and pause but 30 sec pause periods are insufficient
intervals can decrease distance capacity rel- (Weinstein and Full, 1990a; Table 2). Difative to locomotion at the same average ferences in distance capacity found for interspeed (Weinstein and Full, 1992; Table 1). mittent vs. continuous exercise, even at the
Crabs can fatigue sooner in a given time same average speed, are most likely assoperiod by moving rapidly at speeds above ciated with the kinetics of fatigue-producing
that which elicits maximal oxygen con- agents relative to the rate of recovery prosumption. Intermittent locomotion can cesses. The dynamics of physiological rate
increase the relative work load at a given processes can significantly affect the duraspeed. A speed that requires 84% of maxi- tion of locomotor behavior.
mal oxygen consumption during continuAn apparent disadvantage of intermittent
ous walking may demand 99% of the effec- exercise is the high cost compared to contive maximal oxygen consumption if a crab tinuous exercise. When calculated from the
walks twice as fast, but rests half the time average rate of oxygen consumption during
(30 sec exercise, 30 sec pause; Fig. 4). complete exercise-pause cycles, intermitBehavioral capacity or work done during tent exercise is the same as or more expenintense activity with extended exercise peri- sive than continuous exercise both per time
ods or with short pause periods may be less and per distance (Weinstein and Full, 1992).
than if that behavior were carried out at a The difference in cost is most likely a conlower intensity level without pauses.
sequence of the elevated metabolic rate during the pause periods, compared to the restMetabolic response
ing metabolic rate, and the high energy
Intermittent activity differs from contin- demand of the supramaximal speeds
uous activity in that the former relies pri- employed during the exercise periods (Full
marily on the rate at which systems turn on and Prestwich, 1986; Fig. 2B).
and off during transitions to or from a steadySUMMARY AND CONCLUSIONS
state. At the onset of exercise before oxygen
uptake has attained a steady-state, the conIn 1979 Bliss predicted that, "land crabs
centration of lactic acid can increase due to are and will undoubtedly continue to be
accelerated glycolysis and high-energy promising objects of scientific research."
phosphate and oxygen stores can be Studies of ghost crabs support her contendepleted. During recovery or a pause from tion and have resulted in several general
activity, lactate can be cleared and high- findings relating to locomotion and activity.
energy phosphate and oxygen stores can be By selecting ghost crabs to address general
replenished. Measurements of muscle questions concerning locomotion, an inter-
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TABLE 2. Muscle metabolite concentration.
exercise group
pause group
A. 30 sec exercise period; 30 sec pause period
2.2 ± 0.7
21.5 ± 1.2
Arginine phosphate
•7.1 ± 1.1
*6.7 ± 1.2
•9.9 ± 1.0
*7.7 ± 1.2
*12.7 ± 1.2
*2.6 ± 0.7
t*9.4 ± 1.4
t*8.3 ± 1.7
B. 120 sec exercise period; 120 sec pause period
Arginine phosphate
1.2 ±0.1
21.3 ±0.9
Means ± SE are reported for resting and exercising crabs. Values are expressed in /imol g~' leg. In the experimental protocol, shaded bars represent exercise at 0.3 m sec"' and white bars represent pause periods. Time is
given in minutes. Arrows indicate when muscle samples were taken. Samples are labeled R (rest), IE (intermittent
exercise), or IP (intermittent pause).
* Significantly different from resting levels.
t Intermittent pause levels are significantly different from intermittent exercise levels.
esting picture of the animal itself has
emerged. Biomechanical studies show that
in 30 g crabs the maximum energy exchange
during walking occurs at the very slow speed
of 0.2 m sec-1. This speed may require the
minimum amount of metabolic energy to
travel a given distance when non-aerobic
costs are considered. Maximal oxygen consumption is also attained at 0.2 m sec 1 .
Above this speed, endurance during continuous locomotion is greatly reduced. Laboratory speed measurements of freely moving ghost crabs suggest that they do most
often select the speed of 0.2 m sec"1 (Fig.
High speed locomotion above 0.2 m sec"1
is not only possible, but may occur frequently in one of the fastest terrestrial
arthropods (40% of the time; Fig. 5).
Although high-speed locomotion is costly
and could result in a greater risk of injury
{i.e., as shown by increased exoskeletal
strains), it may not necessarily limit activity
with respect to distance capacity if the activity is done intermittently. Ghost crabs and
other ectotherms may obviate the limitation of a low maximal rate of oxygen consumption behaviorally by selecting a strategy that includes intermittent locomotion.
Distance capacity can be increased by moving intermittently, but only if the exercise
to pause ratios are within well defined limits
set by the dynamics of physiological rate
processes. In other words, the hare in
Aesop's Fable (1947) could have beaten the
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tortoise easily using intermittent activity if
it had only selected a shorter pause duration. The "rabbit of crustaceans" (Cott,
1930), ghost crabs, have shown us that slow
and steady is not the only option.
Future studies on ghost crab locomotion,
as well as on other species, should be directed
toward at least two areas. First, additional
performance criteria must be used to evaluate locomotor capacity. Many studies have
determined the energetics and endurance of
locomotion, but few have examined stability, maneuverability and durability. Likewise, the effect of variation in substrata {e.g.,
sand vs. clay or hard rock; smooth vs. irregular terrain) has not been addressed adequately. Second, detailed field studies on
Speed (m/sec)
FIG. 5. Preferred speed of free locomotion by ghost
crabs obtained on a track. 500 trials were recorded
(Blickhan and Full, 1987). The preferred speed distribution showed a maximum at 0.1-0.3 m sec"', but
speeds above the maximal aerobic speeds were frequent.
locomotion (i.e., speed, frequency and duration of movement) must be conducted. Integration of physiology, mechanics and
behavior requires knowledge of ecologically
relevant capacities and the extent to which
animals use these capacities in nature (Hertz
etai, 1988).
The authors would like to thank Mary
Full for the comparison to Aesop's Fable.
This study was supported by an NSF Graduate Fellowship to RBW and NSF Grant
DCB 89-04586 and PYI 90-58138 to RJF.
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