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First published online May 1, 2009
Journal of Experimental Biology 212, 1455-1462 (2009)
Published by The Company of Biologists 2009
doi: 10.1242/jeb.025783
Kinematics of horizontal and vertical caterpillar crawling
Department of Biology, Tufts University, Medford, MA 02155, USA
* Author for correspondence (e-mail: linnea.van_griethuijsen{at}tufts.edu)
Accepted 3 March 2009
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Summary |
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 TOP Summary INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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Key words: kinematics, Manduca sexta, soft-bodied, caterpillar, vertical locomotion, climbing, crawling
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INTRODUCTION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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45 deg. (Hunt et al.,
1996
). Many strategies for climbing are used; most involve
attachment to substrates by an interlocking grip using claws, by strong bonds
between the animal and its substrate using adhesives or suction or by using a
friction grip, which combines the previously mentioned strategies
(Cartmill, 1985). Vertical
climbing brings an extra challenge in the form of pitch back or torque,
pulling the upper body away from the substrate and pushing the lower part
against the substrate. The magnitudes of these forces depend on the distance
of the center of mass (COM) from the substrate and the mass itself (see
Fig. 1A). To minimize torque a
climbing animal should keep its COM close to the substrate.
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). Other animals
such as snakes keep their COM close to a vertical substrate by circling and
folding their body around it (Astley and
Jayne, 2007).
In addition to the system used for gripping, size is an important factor in
climbing. Larger animals must find strong structures to support themselves.
The heaviest arboreal animals known are orangutans, which can weigh up to 90
kg (Kay, 1974). Climbing also
brings the risk of falling, which is more damaging for larger animals whose
bones are relatively weaker with a smaller safety factor
(Biewener, 1982). Another
aspect is the cost of climbing, which scales differently than that of
horizontal locomotion. Smaller animals moving horizontally use more energy per
unit mass than larger animals, yet the additional costs of climbing are
constant per unit mass. The additional costs of climbing are therefore
proportionally smaller in smaller animals
(Taylor et al., 1972). From an
energetics standpoint the locomotion of small animals should be less affected
by orientation. This has been seen in desert ants (Cataglyphis
fortis) and wood ants (Formica pratensis) whose walking
kinematics were, after correcting for speed, only little affected by slope
(Seidl and Wehner, 2008). The
same is true for gecko species, Gekko gecko and Eublepharis
macularius (both weighing about 50 g), although the climbing performance
of the ground-dwelling species (E. macularius) was limited in speed
(Zaaf et al., 2001). However,
the stride length and swing duration of the hindlimb in heavier iguana lizards
(Dipsosaurus dorsalis about 60 g) were found to change when moving
from horizontal to a 30 deg. slope (Jayne
and Irschick, 1999).
All of these examples involve animals with stiff, articulated skeletons
with easily quantifiable kinematics. Soft-bodied animals such as caterpillars
are also excellent climbers whose motions during climbing closely resemble
those in other orientations. Manduca sexta (Linnaeus 1763) initiates
crawling with the tip of its abdomen, the terminal prolegs (TP) and continues
with an anterior grade wave of steps with its remaining four pairs of prolegs
(see Fig. 1B–D). The
three pairs of thoracic legs also undergo an anterior grade wave of steps;
however, these movements are less consistent than those of the prolegs
(Johnston and Levine, 1996).
In addition, the prolegs have a strong gripping system and they contribute
more to locomotion than the thoracic legs. During crawling, muscles are
activated to `unhook' the prolegs. The prolegs are then lifted (not shortened)
and carried forward by waves of segmental contractions
(Belanger and Trimmer, 2000;
Trimmer and Issberner, 2007).
This might have implications for locomotion in the vertical orientation as the
COM is moved further away from the substrate. Furthermore, the location of the
COM is likely to vary during locomotion even when measured in relation to the
body. There are no septa dividing body segments, so body fluids and tissues
can be displaced along the anterior–posterior axis. For instance, the
gut does not move in tandem with the moving body segments during locomotion
(M. A. Simon and B.A.T., unpublished data). During locomotion some body
segments stretch while others do not and, as body segments do not have a fixed
volume as seen in earthworms, this drastically complicates locating the COM
along the body axis. Although the COM might change relative to the body when
the caterpillar is moving, during rest in a horizontal orientation the COM is
located between A3 (abdominal segment three) and A4 (abdominal segment
four).
Given these marked differences from other climbing animals, it is interesting to compare the kinematics of upright horizontal and upward vertical crawling. Our hypothesis is that M. sexta larvae should minimize torque during vertical climbing by adjusting their kinematics. Minimizing torque can prevent bending of the body and also minimizes the forces with which a caterpillar needs to pull its upper body towards the substrate and push its lower body away from the substrate.
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MATERIALS AND METHODS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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). Animals used for experiments were in their second day of
the fifth-instar. Data were collected from 25 animals.
Preparation
Before data collection, the M. sexta were anesthetized on ice for
30–60 min and five 168 µm diameter fluorescent beads (Duke
Scientific, Palo Alto, CA, USA) were attached to the cuticle using Elmer's
rubber cement (Elmer's Products, Columbus, OH, USA). Beads were attached to
the tip of each left proleg, above the planta, as well as on the left TP (see
Fig. 1B–D). The animals
were placed on wooden dowels (0.78 cm in diameter) and given time to fully
recover from the anaesthesia. The same substrate was used in the
experiments.
Experiment
The crawling substrate was illuminated by an ultraviolet lamp (Model B, 100
W, long wavelength; Blak-Ray, Upland, CA, USA). Crawling behaviour was
captured on a digital camera (Canon ZR10, Canon USA, Lake Success, NY, USA)
with a Hoya green (X1) filter (Edmund Optics, Barrington, NJ, USA) at 29.97
frames s–1, transferred to a computer using an IEEE 1394
multimedia connection and recorded through Video Wave Professional 7 software
(Roxio, Santa Clara, CA, USA). All the crawling used in this analysis was in a
straight line without lateral movements hence a second camera was not
essential. Both the crawling substrate and the camera were mounted to a frame
that could be rotated to study both horizontal and vertical upward crawling
while keeping the camera position (and aspect ratio) fixed relative to the
caterpillar.
Data analysis
Using APAS software (Ariel Performance Analysis System, v. 1.0, Ariel
Dynamics, San Diego, CA, USA) video recordings were cropped, making sure that
for each animal at least five crawls (five waves of steps, each proleg lifted
five times in total) were visible both in vertical and horizontal
orientations. The positions of the beads were tracked relative to a fixed
point in space and the workspace was calibrated using a custom-built marker
frame. The position, displacement and velocity of the beads were calculated
off-line using a 2-D direct linear transform. Further analysis was done in
Sigmaplot 2000 v. 6.10 (SPSS Inc., Chicago, IL, USA). The following parameters
were calculated.
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)]. The timing of the peaks in forward velocity was used to
align displacement data for successive steps in each segment and to calculate
mean displacement perpendicular to the substrate (proleg lift) for each
segment over several steps. The maximum proleg lift in the mean step was
determined from a Weibull curve fit (see
Fig. 2C). Differences in
caterpillar sizes are corrected for by paired statistical analysis.
Swing duration
When a leg is in stance phase, its point of contact with the substrate
should have a velocity of zero. Velocity along the substrate was used to
calculate the duration of swing. For each animal, the mean velocity over a
step was calculated using three to seven steps per animal per orientation as
described above. This mean step was then used to determine the timing of the
start and the stop of the swing phase from a Weibull curve fit. Start and stop
were measured at 10% of the maximum velocity for each proleg and used to
calculated swing duration (see Fig.
1C; Fig. 2D).
Stride length
A stride for each proleg consists of swing and stance phases. Hence, the
distance moved during the swing phase is the stride length. Stride length was
calculated by determining the time between successive peaks in proleg velocity
and measuring how much the leg had moved along the substrate during that time.
This was calculated for A3p as the stride length should be similar for all
prolegs. The mean stride length per animal was calculated for each orientation
(see Fig. 2A).
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Timing within crawl, duration of crawl and total duration of swing
A crawl is a wave of steps, beginning with the onset of swing in TP and
ending with the onset of stance in A3p. Crawls can overlap in time. Therefore,
a stride or cycle (e.g. start of swing of TP to next start of swing of TP) is
not appropriate for comparing the timing of prolegs relative to each other; a
new stride can start before a crawl is finished and there is considerable
variation among animals in the timing between crawls. The coordination of
proleg movements relative to each other was calculated from the times between
peaks in the velocities of successive prolegs in a crawl. In combination with
data about the duration of the swing phases, the total duration of crawl was
calculated (see Fig. 1B). To
find differences in the timing of the prolegs (and to compensate for speed
differences), the time points were expressed as a percentage of the entire
crawl; the onset of swing phase in TP was defined as 0% and the onset of
stance phase of A3 at the end of the wave of steps was defined as 100%. The
beginning of swing, the timing of the peak of velocity and the beginning of
stance phase were then compared for the horizontal and vertical orientations.
These data were also used to calculate the duration of swing for each proleg
relative to the duration of the crawl. Durations of swing (as a percentage of
the duration of the crawl) for all five prolegs were summed and compared for
horizontal and vertical crawling.
Timing between crawls
To standardize for different crawling speeds, swing and stance timing for
each proleg were normalized to the time taken to complete a stride (see
Fig. 2B). The peak of velocity
in TP was considered 0% and the peak of velocity in TP in the next crawl was
considered 100%. The timing of peak velocity of A3p was then expressed as a
percentage of the stride duration.
Statistical analysis
Stride length, crawling speed, timing between crawls, stride frequency,
duration of crawl and total duration of swing in the horizontal and vertical
orientation were compared using paired t-tests in SPSS (v. 16.0.1,
SPSS Inc.). Proleg lift, swing duration and timing within crawls were tested
using repeated-measures MANOVAs in JMP (v. 5.0.1.2, SAS Institute, Cary, NC,
USA). Descriptive statistics are indicated in means ± standard error
(±s.e.m.).
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RESULTS |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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The caterpillars covered significantly more distance per stride in the horizontal orientation (0.852±0.022 cm) than in the vertical orientation (0.801±0.020 cm) (t=2.918, d.f.=24, P=0.0075). As Fig. 5 shows this difference is small compared with the variation between animals. The caterpillars' stride frequencies were higher in the horizontal orientation (21.34±1.50 strides min–1) than in the vertical orientation (17.31±1.36 strides min–1) (t=3.064, d.f.=24, P=0.0053). The timing of A3p swing in one stride (midswing TP to midswing TP) was significantly later in the horizontal (54.66±1.49%) than in the vertical orientation (49.44±1.47%) (t=3.486, d.f.=24, P=0.0019) (Fig. 6). This increase in time between crawls and, together with the larger distance covered per crawl, contributed to slower crawling in the vertical orientation (0.241±0.021 cm s–1) compared with the horizontal orientation (0.310±0.024 cm s–1) (t=3.165, d.f.=24, P=0.0042). An overview of the parameters tested, descriptive statistics and the results of comparing horizontal and vertical locomotion can be found in Table 1.
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DISCUSSION |
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TOPSummaryINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONReferences |
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)] and mostly remain hidden by holding onto the stem or
reaching to eat from the underside edges of leaves. They can crawl from branch
to branch by lifting their anterior portions away from the substrate and
casting back and forth until they contact a new surface and then by bridging
gaps that can be almost an entire body length. During the later part of the
fifth-instar, the larvae begin `wandering' behavior in which they climb down
the plant to the ground and move considerable distance away before burrowing
to begin pupation.
For most animals living in three-dimensional complex environments, gravity
would be expected to be an important force and indeed most animals have
special gravity-sensing organs. In larger mammals, these are the semi-circular
canals that can sense orientation and head acceleration. For M. sexta
no special gravity sensors have been reported but behavioral evidence suggests
that they do sense gravity, perhaps through proprioreception. First, on the
substrate we used for testing, the caterpillars tended to circle around the
dowel in the vertical orientation but would stay on top of the dowel in the
horizontal orientation. Circling a vertical substrate keeps the COM close to
the substrate, which can be advantageous when climbing on bending twigs.
Similar behavior is seen in climbing snakes
(Astley and Jayne, 2007).
Second, if the planta hairs are touched during locomotion the caterpillar
withdraws that proleg; reattachment to the substrate occurs faster in animals
hanging upside down than in animals on top of a dowel
(Belanger et al., 2000).
Crawling is robust for climbing
When an animal climbs upward there are two effects of gravity that are not
present in horizontal crawling: (1) a backwards force that resists forward
motion and (2) torque pulling and pushing different body parts in the plane of
the substrate. Both forces are strongly influenced by the weight of the animal
(see Fig. 1). Although M.
sexta caterpillars appear to sense gravity, their kinematics differ very
little between crawling upright horizontally and ascending vertically. Even
for kinematic parameters that were significantly different in each orientation
the differences were extremely small compared with those between different
animals. No combination of measurements can be used to determine if an animal
is crawling horizontally or climbing.
Similarly small differences in kinematics have been found in other animals
within Manduca's weight range. For example, when the effect of speed
was removed, running cockroaches (<1 g) had the same stride frequency and
contact time running horizontally or on inclined surfaces
(Full and Tullis, 1990;
Goldman et al., 2006). Geckos
(
2 g) also have similar kinematics when running horizontally and
vertically (Autumn et al.,
2006).
Torque considerations generally demand that the body is kept close to the
substrate during climbing but proleg lift was unaffected in Manduca.
Similarly, proleg swing duration and the relative timing of the proleg
movements within a crawl were independent of orientation. These results
however cannot exclude the possibility of the timing and sequence of muscle
activation within a crawl in horizontal locomotion being different from those
of a climbing caterpillar. Also, the level of activation might be altered in
order to keep the kinematics the same [as observed in climbing cockroaches
(Watson et al., 2002)] but
this remains to be confirmed by simultaneous electromyography. In addition,
ground reaction forces (GRF) can be different while kinematics are the same
(Jindrich and Full, 1999). GRF
measurements could give more insight in the location and magnitude of forces
acting on a climbing caterpillar. There is a wide variation in each kinematic
parameter, yet these parameters change little between the horizontal and
vertical orientation. This indicates that the caterpillars' mode of locomotion
is relatively insensitive to the orientation the animal is in.
Effects of climbing on movements
Clearly, the need to lift the body during climbing has some consequences
for locomotion even in smaller animals. Locusts (Schistocerca
gregaria 2 g) have similar leg swing duration in horizontal,
vertical and upside down locomotion. However, the time between one flexor
burst and the next is much longer when climbing, resulting in slower
locomotion (Duch and Pflüger,
1995). Manduca also climbed more slowly (on average) than
they crawled horizontally. This was the consequence of two changes: (1) each
crawl covered less distance (94% of that covered in the horizontal
orientation) and (2) the delay between crawls was longer (10%). These
differences are extremely small and are unlikely to have a major effect on
normal survival or growth. Manduca sexta caterpillars are cryptic and
do not rely on speed for survival from predators nor do they compete with
other species for most of their native food sources
(Kingsolver and Woods, 1997;
Ojeda-Avila et al., 2003).
Furthermore, vertical climbing costs for small animals are only a small
component of the total costs of locomotion
(Taylor et al., 1972) and
therefore are not a major factor in the kinematics. For soft-bodied animals,
the cost of transport is already relatively high and for caterpillars it is
4.5 times higher than that predicted for animals with similar masses with
stiff skeletons (Casey, 1991).
Presumably energy is spent on tissue movements along and within the body that
do not directly result in locomotion
(Casey, 1991). Because
caterpillars crawl slowly (0.241–0.310 cm s–1 on
average in the present study), and forward momentum is small and episodic,
there is no sustained acceleration and the effect of gravity is therefore
minimized during vertical climbing. Another reason for the high costs of
caterpillar locomotion is that muscles and body wall have low resilience,
dissipating a large proportion of mechanical work (40–60%) during cycles
of strain (Dorfmann et al.,
2008; Dorfmann et al.,
2007; Lin et al.,
2008; Woods et al.,
2008). This inability to store elastic energy makes caterpillar
locomotion less efficient.
Adaptations of Manduca for movement in complex branched structures
Although the small size and slow speed of Manduca are important
factors in its climbing ability, perhaps the most important contribution is
made by the strong gripping system (the prolegs). Each proleg consists of an
extendable pouch on the ventral hemisegment with a fleshy lobe (the planta) at
its tip (Barbier, 1985;
Snodgrass, 1961). There is a
row of hooks (crochets) on the planta that can be deployed to engage with
irregularities on the substrate at the start of stance phase. The gripping
force may far exceed other forces acting on the body during crawling and
attempts to pull a caterpillar off a rough substrate can result in the
crochets tearing out of the planta rather than release from the surface. The
gripping system is used regardless of the orientation the caterpillar is
in.
The passive state of the prolegs is in the adducted position with the
crochets extended by tonic body pressure and body wall elasticity
(Mezoff et al., 2004). Release
is achieved by unhooking the crochets and retracting the prolegs by active
muscle contraction (Belanger and Trimmer,
2000; Belanger et al.,
2000; Mezoff et al.,
2004). As the gripping system is equally strong in horizontal and
vertical orientation, the hooking and unhooking activities do not lead to
differences in the kinematics. It has been argued that a strong gripping
system in climbing can be seen as the animal creating a non-vertical surface
for itself, like climbing a ladder
(Cartmill, 1985). The
interlocking grip on the substrate prevents an ascending or descending
caterpillar from rotating backwards or sideways due to torque. The strong
gripping system in caterpillars also serves another function: lateral
stability. Unlike sprawled legs, caterpillar prolegs on each segment are
located relatively close to each other. A strong gripping system is necessary
to avoid rolling sideways when crawling horizontally. As Brackenbury argues,
this phenomenon also leads to a high duty factor, which limits the crawling
speed (Brackenbury, 1999).
LIST OF ABBREVIATIONS
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Footnotes |
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