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First published online March 31, 2007
Journal of Experimental Biology 210, 1446-1454 (2007)
Published by The Company of Biologists 2007
doi: 10.1242/jeb.02757
Just drop it and run: the effect of limb autotomy on running distance and locomotion energetics of field crickets (Gryllus bimaculatus)
1 School of Veterinary and Biomedical Sciences, Murdoch University, Murdoch,
WA 6150, Australia
2 Department of Zoology and Entomology, University of Pretoria, Pretoria,
0002, South Africa
* Author for correspondence (e-mail: T.Fleming{at}murdoch.edu.au)
Accepted 16 February 2007
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Summary |
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Key words: cost of transport, energy, insect, locomotion, metabolic rate, Orthoptera, running
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). In
the cricket Acheta domestica, hindlimb autotomy similarly results in
a significant reduction in escape speed and jumping ability, and therefore
makes the animals more susceptible to predation by both lizards and mice
(Bateman and Fleming, 2006a).
An immediate cost in terms of reduced locomotion due to autotomy of an
appendage has similarly been demonstrated for a number of other invertebrates;
for example, reduced walking or running speed post-autotomy for harvestmen
(Opiliones) (Guffey, 1999),
spiders (Araneae) (Amaya et al.,
2001; Apontes and Brown,
2005), and stick insects (Phasmatodea)
(Carlberg, 1984), or a
significant reduction in swimming speed after caudal lamellae autotomy in
Odonata larvae (Burnside and Robinson,
1995; Gyssels and Stoks,
2005; McPeek et al.,
1996; Robinson et al.,
1991; Stoks,
1999). Crab swimming speed is also reduced by removal of a
swimming leg (Juanes and Smith,
1995; Smith,
1995), and in starfish, arm loss significantly affects locomotory
ability (Bingham et al., 2000;
Slater and Lawrence,
1980).
Indirect assessment of the affects of autotomy upon energetic costs
incurred through locomotion may be made by scrutiny of the mechanisms of
locomotion. For example, in the swimming bivalve Limaria fragilis
(Mytiloida), mantle tentacles contribute to swimming by a rowing motion
(Donovan et al., 1994).
Autotomy of the longest tentacles in these molluscs reduces clap distance by
13%, which the animals compensate for by clapping faster to maintain swimming
speed (Donovan et al., 1994).
This increased clap speed would therefore increase their metabolic expenditure
in order to maintain swimming distance. As far as we are aware, however, the
direct metabolic costs of locomotory impairment due to autotomy have not been
measured for any invertebrate species.
Two important variables used to compare locomotor performance, both inter-
and intraspecifically, are endurance capacity and metabolic energy costs
(Full, 1987). The aim of the
present study was to determine how autotomy of a hindleg affected the
locomotory endurance for field crickets, Gryllus bimaculatus, and
whether there was a measurable change in metabolic rate or cost of transport
for these animals.
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Materials and methods |
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In this study, we examined two aspects of locomotory fitness in intact and autotomised crickets: endurance and respirometry.
Endurance
Our first measure of fitness was the distance run by an animal until it
stopped and would move no further in response to stimulus (termed
`endurance'). For the study of endurance post-autotomy, a total of 60 crickets
(30 male, 30 female) aged 7–14 days post adult eclosion were taken from
a mixed-sex colony. They were moved to individual holding jars and held for 24
h prior to commencing experiments (we found that animals tested immediately
after removal from large mixed-sex colonies demonstrated a significant
increase in locomotion speed after 24 h of holding individually). On the
experimental day, individuals were weighed (to 0.01 g) and measured for
pronotum width (mm, using digital callipers). Animals were then placed into a
circular arena of 1 m circumference and 
5 cm width. Crickets were timed
upon introducing them to the arena. They were induced to run around the
circumference of the arena by tapping a stick twice on the arena floor
immediately behind the cricket whenever it stopped moving. Trials were stopped
when two successive double-taps did not induce the cricket to move. The number
of circuits (equivalent to distance in m), the number of taps (reflecting the
number of stops the animal made), and the total time (s, measured with a
stopwatch) were recorded and speed (m s–1) subsequently
calculated.
Animals were assigned to either autotomy or control (intact) treatments
(N=15 for each treatment group for each sex) such that the speed and
mass of individuals in each group were matched closely. Individuals in the
autotomy group were induced to autotomise their right hindlimb (R3)
by grasping the leg with tweezers so that the animal had to autotomise its
limb in order to escape. From previous data
(Bateman and Fleming, 2005), we
know that a hindleg weighs about 4.52±0.73% (N=66) of the
animals' body mass. Every individual was then re-run 24 h later. The change in
distance run, speed and number of stops m–1 run were
expressed as Day 2 values divided by Day 1 values for each individual. These
three measurements (dependent variables) were each analysed for the effects of
autotomy treatment and sex (independent factors), with body mass and pronotum
width as covariates by analysis of covariance (ANCOVA).
Respirometry
Our second measure of locomotory fitness was the metabolic cost of
transport incurred during escape running. The system employed in the present
study therefore used a `running tube' as a respirometry chamber, along which
crickets ran back and forth at their own, and variable, speed; such a setup
has been used successfully by other authors
(Berrigan and Lighton, 1994;
Duncan, 1999;
Duncan and Lighton, 1997;
Lighton and Duncan, 1995;
Lighton and Feener, 1989;
Lighton et al., 1993;
Lipp et al., 2005). The
running tube was made of a 1 m length of 40 mm diameter glass tubing, with a
wax base that served two functions. The wax base occupied approximately one
third of the internal volume; the final gas volume of the tube was therefore
800 ml. The wax base also allowed the crickets a flat surface upon which they
could get purchase during running.
Measurements of CO2 emission were carried out using a flow-through respirometry system (Sable Systems TR-2 from Sable Systems, Las Vegas, NV, USA). We present data for CO2 emission rather than O2 consumption because we were measuring CO2 emission into a large volume (of our running tube) and stability and resolution of the LiCor analyser are superior to those of the best current O2 analysers. The incurrent air stream was scrubbed of H2O and CO2 with silica gel and soda lime, respectively; air exiting the chamber was similarly scrubbed of H2O before entering a CO2 analyser (LiCor 6262, Lincoln, NE, USA). The gas analyser was then connected to a Sable Systems sub-sampler pump and mass flower controller. A flow rate of approximately 270 ml min–1 was maintained throughout the experiments, and temperature was relatively stable at about 21°C. Every 0.1 s, mass flow and CO2 values (µmol mol–1) were recorded on a PC (Datacan V, Sable Systems).
Measurements were made on 18 individual male crickets aged between 14 and
21 days post adult eclosion [we maintained constant ages since mass-specific
metabolic rate has been shown to vary considerably with age in Acheta
domestica (Hack, 1997)].
We only analysed males since females may be expected to show greater
variability in metabolic rate due to different stages of egg production and
are less able to increase metabolic activity during intense terrestrial
exercise (Kolluru et al.,
2004). Half of the crickets used had been induced to autotomise
their right hindlimb 5 days prior to the experiment by grasping the leg with
tweezers such that the animal had to autotomise its limb in order to escape.
Measurements of autotomised and intact individuals were alternated during the
experiment.
The experimental procedure was carried out as follows. A baseline CO2 reading was recorded and then individuals were weighed (to 0.0001 g) and pronotum width measured (to 0.01 mm) before they were placed in the metabolic chamber. They were given at least 10 min to adjust to the chamber, during which time a small dark cloth was placed over the tube immediately above the cricket. This effectively confined the cricket to a length of about 10 cm. Although we could not observe any movements during this time, the cricket did not emerge from under the cloth and so was confined to this small area during this time. Readings from this time were used to estimate the resting metabolic rate of stationary crickets. After this, the animal was induced to move the length of the respiratory chamber by touching its back or hindlegs with a piece of card attached to a magnet controlled by a second magnet outside the chamber. The cricket was induced to move back and forth along the length of the chamber for at least 5–10 min (some animals struggled to keep moving for longer periods). The distance travelled (in m) and time spent moving (monitored with a stopwatch) were recorded in order to calculate average running speed (m s–1).
The rates of mass-specific CO2 production (ml
s–1 kg–1) were calculated for the initial
rest phase (R
CO2) and the
activity bout (ACO2).
Resting metabolic rate indicates the energetic costs of inactive subsistence,
and were analysed for the effect of autotomy treatment (independent factor) by
ANCOVA with body mass and pronotum width as covariates.
Crickets did not always reach a steady state of CO2 production,
often running faster and stronger at the commencement of exercise [similar to
results for spiders on a treadmill
(Schmitz, 2005)]. Therefore,
ACO2 was calculated as the
average of all data points between the start of the plateau (there was a steep
increase in CO2 upon commencement of activity, which then levelled
out after about 3 min as the air within the running tube was replaced) to the
end of the exercise period (whereupon CO2 levels dropped
immediately). Active metabolic rate data were analysed for the effect of
autotomy treatment (independent factor) by ANCOVA, with body mass, pronotum
width, mass-specific resting metabolic rate, and walking speed as covariates.
The Cost of Transport (COT; calculated as
ACO2 divided by walking
speed) was analysed similarly. The slopes of
ACO2 versus speed
(the minimum cost of transport or MCOT) were compared for intact and
autotomised animals by t-test
(Zar, 1999).
All data are given as the mean ± 1 s.d. The critical level for
statistical analyses was set at P<0.05 and statistical analyses
were carried out using Statistica version 6.0
(StatSoft, 2001).
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CO2) was not
significantly different between autotomised and intact animals
(Fig. 2;
F1,14=0.45, P=0.514, the covariates body mass,
P=0.162, and pronotum width, P=0.677, did not contribute
significantly to RCO2).
However, when the animals were active, despite being slower, on average,
autotomised animals had significantly higher metabolic rates
(ACO2) compared with intact
control animals (Fig. 2,
Table 1;
F1,12=6.79, P=0.023). Metabolic rate was
significantly correlated with running speed, whilst body mass, pronotum width
and resting metabolic rate
(RCO2) did not
significantly affect ACO2
(Table 1).
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The slopes of ACO2
versus speed (MCOT) were significantly different for autotomised and
control animals (calculated from Fig.
2; t14=3.80, P<0.001). The cost of
transport (ACO2 divided by
speed; COT) was significantly affected by autotomy treatment, with COT values
higher for autotomised animals, independently of walking speed
(Table 2;
F1,12=8.13, P=0.015).
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There appears to be very little information on the locomotory endurance of
arthropods. Most studies of locomotory energetics require that animals run
only as far as required to achieve a stable metabolic state. None of the
studies of Orthoptera we accessed discusses the endurance of the animal under
examination. Blowflies ran >90% of the time (1.5 h) that they were in a
recording chamber (Berrigan and Lighton,
1994). The same flies would walk continuously for 6–16 h
(
=9.6 h), covering 465–814 m,
during which time they would lose 50% of their body mass. Full examined
endurance in ghost crabs (Full,
1987), and found that endurance time decreased as exercise speed
increased, with small (=2 g) animals
showing the least stamina compared with larger
(=27 g and
=71 g) animals. Our crickets
demonstrated significant reduction in running endurance post-autotomy.
Autotomised crickets moved an average of only 14.5±8.5 m (range
3.75–35 m), compared with 26.6±19.6 m (range 1–82 m) when
intact.
Amongst arthropods, the energetic cost of pedestrian locomotion has been
extensively studied in ants, cockroaches and beetles; a few studies have also
been carried out on wasps, flies, spiders, mites and crabs (see
Table 3 for details). As far as
we are aware, only Full et al. have examined the energetic costs of locomotion
in Orthoptera (Full et al.,
1990). Some authors have assessed `maximal metabolic rate' in a
closed circuit system (e.g. shaking a sealed container containing the crickets
with a uniform motion for a period of time, forcing the cricket to exercise
vigorously) (Kolluru et al.,
2004); there is, however, no quantification of activity level
under this particular experimental setup. Hack examined the energetics of
different male mating strategies in the house cricket Acheta
domestica, comparing walking with calling behaviour
(Hack, 1998); however, this
study examined the costs `per step or single cycle of movement of a single
leg' when the animals were held in a small (47 ml) respiratory chamber; these
data therefore do not allow for a comparison between walking speed and
metabolic expenditure.
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Oxygen consumption in the Australian field cricket Teleogryllus
commodus (0.95±0.07 g) was examined while running on a miniature
treadmill (Full et al., 1990),
and MCOT=8.03 ml O2g–1 km–1
oxygen consumption was recorded (equivalent to 0.161 J kg–1
km–1, using the authors' conversion of 1 ml
O2=20.1 J). Our G. bimaculatus (0.70±0.09 g) did
not achieve a steady state of locomotion, with a brief burst of high-speed
running followed by slower movement. Nevertheless, the cost of locomotion in
our animals was remarkably similar to that for T. commodus, at
0.178± 0.018 J kg–1 km–1 for intact
and 0.230±0.034 J kg–1 km–1 for
autotomised G. bimaculatus.
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). However the slopes of the lines drawn (MCOT values) have
been demonstrated to be markedly resilient to variation in temperature (e.g.
Full and Tullis, 1990a;
Lighton and Feener, 1989;
Weier et al., 1995). In
Fig. 3 the MCOT values for each
study are plotted against against body mass. MCOT scales inversely with body
mass, and is therefore higher for small animals
(Lighton and Feener,
1989).
The data for T. commodus and G. bimaculatus reveal that
these crickets have similar MCOT to other species of similar mass and do not
appear to be exceptional in regard to their normal energetics, sitting very
close to the regression line for these data
(Fig. 3). However when they
have autotomised a hindleg, G. bimaculatus demonstrate significantly
higher MCOT values than intact animals. In this study we only examined the
affect of autotomy of a single leg. An estimated 29% of males and 38% of
females in a field population of Gryllus bimaculatus were missing
limbs, with 18% of males and 13% of females missing more than one leg
(Bateman and Fleming, 2005). We
would anticipate further increases in the energetic cost of locomotion with
additional leg loss, since the effects upon the biomechanics of walking become
more pronounced with additional leg loss
(Hughes, 1957).
Autotomised crickets are not able to walk as fast as intact animals, and
have increased metabolic rates; their COT and MCOT values are significantly
higher than for intact crickets. Such a result suggests that loss of a leg
interferes with the walking biomechanics in these animals, since removal of a
leg results in the remaining legs having to function under altered conditions
(Hughes, 1957). The mechanisms
used by a species to move significantly affect the efficiency of such
locomotion (Full et al.,
1990).
Crickets are likely to use the alternating tripod gait when moving fast
(Delcomyn, 1981). This gait
`ensures that at least three legs are in contact with the walking surface
at all times, and that the insect's centre of gravity is always within the
base of support formed by the stationary legs'
[(Delcomyn, 1981), p. 105].
This gait is altered upon autotomy of a leg. Furthermore, `the proportion
of time that a leg spends off the ground during each step increases as the
speed of the animal increases'
[(Delcomyn, 1981), p. 110],
suggesting that the costs of autotomy would be most evident during faster
paces, as we found.
The effects of limb amputation on locomotion (reviewed by
Delcomyn, 1981) have been
examined in cockroaches (Delcomyn,
1971; Hughes,
1957), beetles (Wilson,
1966) and stick insects
(Graham, 1977). Loss of even a
single limb in cockroaches results in a significant alteration to the posture
of the remaining limbs (Hughes,
1957). Loss of a hindlimb results in shortened stride of the
remaining hindlimb, which is held closer into the body and is apparently
`dragged' (so that it exerted little propulsive thrust), the middle legs are
held closer to the body, and the front and middle legs on the amputated side
are retracted farther back than normal
(Hughes, 1957). The loss of
propulsion and balance experienced upon loss of a leg, coupled with increased
proportion of body mass supported and altered coordination, is therefore
likely to account for the greater costs of locomotion experienced by
autotomised animals.
A number of authors have suggested that various spiders and harvestmen may
have `spare legs', with individuals appearing to suffer minimal costs from the
loss of a limb or two (Brueseke et al.,
2001; Brueseke et al., 1999;
Johnson and Jakob, 1999) (but
see Amaya et al., 2001;
Apontes and Brown, 2005). This
hypothesis might predict that the animal has excellent walking biomechanics,
such that the loss of a single leg impedes natural movements only minimally.
It might, therefore, be expected that such spiders have a low MCOT. Consistent
with this, a tarantula, the wolf spider Pardosa lugubris (Lycosidae)
and Myrmecotypus rettenmeyeri (Clubionidae), show MCOT values that
are small for their respective body masses
(Fig. 3)
(Herreid et al., 1981b;
Lighton and Gillespie, 1989;
Schmitz, 2005). On the other
hand, data for Marpissa muscosa (Salticidae) indicates that these
jumping spiders have a very high MCOT (in
Fig. 3) and pay a heavy
metabolic cost for faster locomotion
(Schmitz, 2005). This may be
due to unique locomotion mechanics in these spiders, which jump rather than
walk. Given the `spare leg' hypothesis for some arachnids, it would be very
informative to compare the MCOT values for more spider species, and examine
the effects of autotomy upon these costs.
Despite the benefits of losing a leg in order to escape a predator, there
are nevertheless many costs of leg autotomy incurred by crickets. In this
study, we found that autotomy of a single hindlimb significantly reduced
endurance and also increased the metabolic costs of locomotion for these
animals. Both compromised endurance and energetics would contribute to an
increased likelihood of failing to survive a subsequent predatory encounter.
Furthermore, the energetic costs of locomotion may also contribute to
alterations in specific mating behaviours, which we have demonstrated are
affected by limb autotomy (e.g. Bateman and
Fleming, 2005; Bateman and
Fleming, 2006b; Bateman and
Fleming, 2006c).
One particularly important consideration for autotomised crickets may be a
trade-off between the metabolic costs of calling (e.g.
Hack, 1998;
Hoback and Wagner, 1997) and
locomotion in order to secure a mate. For intact crickets, locomotion may
incur expenses comparable to those of calling. For example, in the house
cricket, Acheta domestica, high pulse rate chirping is equally as
energetically expensive as walking (low pulse rate chirping is an order of
magnitude less energetically expensive than walking, although less effective
at attracting mates) (Hack,
1998). However, if the costs of locomotion are increased (e.g. by
autotomy of a leg or two), then calling may become significantly more
advantageous. Crickets may therefore have to make energetic trade-offs that
impact on lifetime reproductive success in response to autotomy of a limb.
These trade-offs due to energetic costs of calling and locomotion may reflect
the reduced ability of autotomised males to compete with intact males for
mates (Bateman and Fleming,
2005).
A second trade-off may be balancing the amount of time spent walking to
find a mate versus remaining stationary. Many cricket males sing from
burrows to reduce predation risk and to allow sequestering of females
(Simmons, 1986a;
Simmons, 1986b). However,
small male Scapsipedus meridianus that are unable to obtain a burrow
sing less and move more to avoid predation than males who have a burrow from
which to sing (Bateman, 2000);
these crickets would therefore accrue multiple negative impacts due to forced
locomotion (if they experience similar higher costs of locomotion as G.
bimaculatus post limb autotomy). Also, females responding to male call
may put less effort into their phonotaxis if they are missing a limb and
therefore incurring an increase in metabolic cost of transport compared with
intact females. A reduction in locomotory behaviour would presumably be to the
detriment of reproductive activity.
Thirdly, both males and females may incur increased energetic costs of
movement when foraging if they have autotomised a limb. In male Gryllus
campestris, acoustic signalling is condition-dependent, with well-fed
crickets being able to sing more (Holzer
et al., 2003). For female gryllid crickets, egg production is also
affected by nutritional status: female black-horned tree crickets
(Oecanthus nigricornis) that receive large nuptial gifts lay more
eggs (Brown et al., 1996).
Overall, therefore, due to the increased costs of locomotion after they have autotomised a limb, crickets may have to shun potentially dangerous situations, avoid metabolically costly activities, and may have reduced feeding and therefore fecundity. But at least they are still alive.
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