Effects of loading and size on maximum power output and gait characteristics in geckos
Department of Ecology and Evolutionary Biology, 310 Dinwiddie Hall, Tulane University, New Orleans, LA 70118, USA
* Author for correspondence (e-mail: Irschick{at}tulane.edu)
Accepted 21 July 2003
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Summary |
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Key words: Hemidactylus garnoti, Gekko gecko, speed modulation, stride frequency, kinematics, mass-specific power output
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Introduction |
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Loading studies are ideal for testing hypotheses regarding limitations on
power output because, relative to unloaded locomotion, moving with loads
increases the amount of work expended to move a given distance for a given
speed and surface, and thus necessarily increases the total power output.
Moreover, many organisms move in nature with large loads, such as when females
carry large eggs (Bauwens and Thoen,
1981; Vitt and Congdon,
1978
), or when animals consume large meals
(Garland and Arnold, 1983
).
Thus, studying the effects of loads on locomotor performance has ecological
relevance (Aerts, 1990
;
Vanhooydonck and Van Damme,
1999
), although many studies (including the present work) have
used loads that are generally greater than animals experience in nature.
Biologists have studied the effects of adding external loads to a variety of
animals, including birds (Chai et al.,
1997
), horses (Hoyt et al.,
2000
; Wickler et al.,
2001
) and insects (Kram,
1996
). In some cases, the loads had a substantial effect on
performance and kinematics (e.g. Hoyt et
al., 2000
; Wickler et al.,
2001
), whereas for other species, particularly insects
(Kram, 1996
), no significant
effects were found. Despite these reports, few studies have examined how loads
affect power output, particularly during vertical locomotion, when one would
predict that the effects of loading would be most profound.
A second factor that could influence power output during locomotion is
animal size (Hill, 1950;
Marden, 1987
). Previous
authors have suggested that large animals should produce less power than small
animals per unit body mass because of the manner by which surface area (and
hence force) scales with size (e.g. Wilson
et al., 2000
; Toro et al.,
2003
), although this expectation has not always been borne out
(Pennycuick, 1969
,
1972
;
Marden, 1987
). While several
studies have addressed the general issue of whether large and small animals
differ in power output during various activities
(Marden, 1987
;
Wilson et al., 2000
), we are
aware of no studies that have examined this issue for vertical locomotion,
such as observed in many arboreal lizard or insect species (but see
Farley, 1997
). Thus, another
aspect of our study concerns a comparison of power output between two gecko
species that vary greatly in size (see below). While such two-species
comparisons are commonplace in physiological studies, their interpretation is
often controversial (Garland and Adolph,
1994
), so we interpret these data cautiously.
The effects of size and loading on limb kinematics are also poorly resolved
for vertical locomotion. As the amount of a load increases, one predicts that
maximum speed should decrease when moving vertically, but whether animals
achieve this by equally diminishing stride length or stride frequency is
unknown. Furthermore, how the addition of loads affects the manner by which
animals increase in speed on vertical surfaces has rarely been examined, and
there are no studies on the interactive effects of size and loading on
kinematics. This last issue is of particular interest to physiologists because
previous work has shown that, on horizontal surfaces, small animals tend to
modulate speed by changing stride frequency, whereas larger animals tend to
change stride length (Gatesy and Biewener,
1991). Furthermore, a recent study has shown that a climbing gecko
(Gekko gecko) modulates speed almost entirely by changing stride
frequency, whereas a similarly sized terrestrial gecko (Eublepharis
macularius) changes speed primarily by changing stride length
(Zaaf et al., 2001
). Thus,
data on how size and loading affect limb kinematics during vertical climbing
might shed light on these issues.
Small climbing lizards such as geckos provide an excellent opportunity for
testing the effects of size and loading on locomotion. Female geckos
frequently carry large eggs prior to laying, which can approximate 10-30% of
their body mass (D. J. Irschick, personal observation), so geckos are
accustomed to carrying large loads. Furthermore, climbing geckos differ
dramatically in size among species (e.g. 1-70 g difference in mass among
species) (Zaaf and Van Damme,
2001).
In the present study, we tested the effects of size and loading on the vertical locomotion of two species of geckos (Gekko gecko and Hemidactylus garnoti). Whereas G. gecko is the largest extant gecko with derived toepads, and achieves a mass greater than 70 g, H. garnoti is a small (<5 g) climbing gecko that is more representative of the large family of geckos. However, these two species are generally similar in terms of their morphology, relative toepad dimensions and natural history, making them an excellent case study for comparison. We addressed three primary issues. First, does mass-specific power output limit locomotor performance in geckos? If the hypothesis of power limitation is correct, then as lizards are loaded with successively greater weights, speed should decrease, but mass-specific power (per unit body mass) should remain constant. Alternatively, if power is not limiting, then as successively greater weights are added, speed should decrease, but mass-specific power (per unit body mass) should increase. Second, how does loading affect the kinematics of limb movement? Third, does size affect mass-specific power output? More specifically, we predicted that larger geckos (G. gecko) would produce less mass-specific power (relative to size) than smaller geckos (H. garnoti).
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Materials and methods |
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Locomotion trials
We induced geckos to run vertically up a custom-built racetrack. The
racetrack had Plexiglas walls attached on either side to a wooden base that
was 13 cm wide and 150 cm long. We filmed the lizards from a dorsal
perspective at 250 Hz with a motionscope PCI camera (Redlake, San Diego, CA,
USA) attached to a PC computer. All locomotion clips were digitized using Peak
performance MOTUS software.
Prior to each locomotion trial, lizards were placed either in plastic bags (H. garnoti) or canvas bags (G. gecko) inside an incubator set to 30°C for at least 30 min. We placed loads of 100-200% body mass (BM) on all individuals of H. garnoti, and loads of 100% BM on all individuals of G. gecko. For G. gecko, we acquired locomotion for movement uphill when unloaded and with a 100% BM load, whereas for H. garnoti, we acquired locomotion when moving uphill unloaded and with loads of 100%, 150% and 200% BM. We used small, thin lead weights that were wrapped approximately around the center of mass of each lizard (placed centrally between each girdle) (Fig. 2). The weights were attached to the body by placing a small piece of tape on the dorsal and ventral sides of the lizard. The width and thickness of the strips for the four load types were similar for each species, but the strips for the heavier loads were longer, and hence wrapped around the body to a greater degree. The loads did not appear to affect the overall locomotor behavior of the lizards, or the amount of lateral flexion of the back (see below). To determine whether the presence of the weight itself affected locomotion, we wrapped a piece of thin paper around the body of each H. garnoti that was similar in dimensions to the above weights, but only approximated 2% BM.
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Each lizard was given ten opportunities to run at maximum speed with each of these weights. Loading condition was randomly assigned across days and lizards were tested on multiple, non-consecutive, days with the same loads. For each trial, we attempted to gain 2-5 strides of steady speed locomotion. We did not include any strides in which the animal was clearly accelerating or decelerating over the course of several strides. All data were analyzed on a stride-by-stride basis. We recorded footfall patterns of the hindfoot for each lizard, and defined a stride as the interval between consecutive footfalls of the right hindfoot (from a dorsal perspective). For each stride, we calculated stride length and stride frequency, and duty factor, speed and mean mass-specific power output per stride. Stride length was calculated as the displacement of the tip of the snout between consecutive footfalls; stride frequency was calculated as the reciprocal of stride duration (the time between consecutive footfalls); duty factor was calculated as the duration of foot contact (i.e. step duration) divided by stride duration; speed was calculated as stride length divided by stride duration. Since we used strides of steady speed locomotion, we only took into account gravitational forces to calculate mass-specific power output per unit body mass. Thus, mass-specific power output per unit body mass was calculated as the product of total mass m, gravitational acceleration (i.e. F=mg) and speed, divided by body mass. In this case, total mass equals the sum of body mass and the weight of the load.
To determine whether the addition of loads altered locomotor posture, we digitized the tip of the snout and tail, and three small evenly spaced white dots on the back, and calculated the angles of the head, trunk and tail over the whole stride cycle. The angle of the head was defined as the angle between the tip of the snout and the two dorsal points closest to the head, with angles of 180° indicating that the head was in alignment with the body, and angles greater or less than 180° indicating movement of the head towards the left or right, respectively. The angle of the trunk was defined as the angle between the three dorsal points, with angles of 180° indicating that the trunk was straight, and angles greater or less than 180° indicating lateral flexion towards the left or right, respectively. The angle of the tail was defined as the angle between the tip of the tail and the two most posterior dorsal points, with angles of 180° indicating that the tail was in alignment with the body, and angles greater or less than 180° indicating movement of the tail towards the left or right, respectively. For the same set of strides used in step (1) below, we calculated maximum and minimum values of each kinematic variable for each stride and compared loading conditions.
Statistical analyses
All values were log10-transformed prior to statistical analyses.
To determine whether loading affected angular kinematics, we conducted
separate multivariate analyses of variance (MANOVAs) within each species,
using the maximum and minimum values for each kinematic variable as dependent
variables, and loading condition as the independent variable. If the MANOVA
was significant within either species, we then used ANOVAs with loading
condition as a factor and the different angles as dependent variables. We then
used LSD post-hoc tests to determine where differences lie in the
data structure.
We conducted several other analyses to address our primary questions. (1) For the issue of power limitation, we calculated, for each individual of each species, their maximum mass-specific power output and speed for each loading condition (based on stride-by-stride data). Because some individuals did not provide high quality runs for every loading condition, our sample sizes differ slightly among loading conditions within a species. To test for statistical differences among loading conditions for these data, we performed two one-way ANOVAs within each species using loading condition as a factor, and mass-specific power output and speed as dependent variables, respectively. We then conducted post-hoc tests to determine where the differences existed. (2) To address the issue of whether size affects mass-specific power output, we examined only those strides for which lizards produced the maximum amount of power for each species regardless of loading condition, and then used one-way ANOVAs to compare the two species. (3) To address the issue of whether speed modulation changes under different loading conditions, we performed bivariate linear regressions, using speed as independent variable and stride length, stride frequency and duty factor as dependent variables within each species. We then used multiple regression analyses within each species, using stride length, stride frequency and duty factors as dependent variables, and speed and loading condition (i.e. unloaded, 2% BM, 100% BM, 150% BM and 200% BM for H. garnoti and unloaded and 100% BM for G. gecko) as independent variables to test for the effect of loading condition on stride length and stride frequency. (4) We conducted a multiple regression pooling both species (unloaded and 100% BM only), using stride length, stride frequency or duty factor as dependent variables, and speed, loading condition and species as independent variables, to test whether the two species react to the different loads in similar ways.
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Results |
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Power output and speed
Mean speed generally declined with the addition of increasingly larger
loads for both species (Table
3). In H. garnoti, mean speed declined 25% between the
unloaded and 100% BM conditions, and 37% between the unloaded and 200% BM
conditions. In G. gecko, mean speed declined 31% between the unloaded
and 100% BM conditions. As loads were added, mean mass-specific power output
increased substantially at first for both species
(Table 3), but for H.
garnoti, power production leveled off at higher loads, (1% increase in
power between the 150% and 200% BM conditions, 21% decline in velocity). The
one-way ANOVAs testing for loading differences in power and speed were
statistically significant for both variables within both species
(Table 4). However,
post-hoc comparisons showed that mass-specific power differed between
the unloaded condition and all the loaded ones (i.e. 2% BM, 100% BM, 150% BM
and 200% BM; all P<0.01), but not among the loaded conditions in
H. garnoti (all P values >0.05). In contrast, speed
differed significantly between the control (i.e. 2% BM) and all other
conditions (i.e. unloaded, 100% BM, 150% BM and 200% BM; all P values
<0.05).
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Analyses using only the strides that produced the maximum mass-specific power within each species (regardless of loading condition) show that mean maximum mass-specific power output is 33% greater in H. garnoti than in G. gecko (one-way ANOVA, F1,1=7.2, P<0.025; Fig. 3A), whereas maximum speed is only slightly, and non-significantly, greater (19%) in G. gecko (one-way ANOVA, F1,1=1.6, P>0.20; Fig. 3B).
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Speed modulation
The bivariate regression analyses show that under all loading conditions,
and in both species, stride frequency increases to a greater extent with speed
than does stride length (Table
5;Fig. 4). This
suggests that in all cases, the geckos modulate speed primarily by altering
stride frequency. However, duty factor shows no obvious relationship with
speed, with the exception of H. garnoti moving unloaded
(Table 5). Based on multiple
regression analyses, speed and loading condition (independent variables)
explain 70% and 89% of the variation in stride length and frequency,
respectively, for H. garnoti
(Table 6), whereas for G.
gecko, they explain 69% and 70% of the variation, respectively. Speed and
loading condition explain 58% (H. garnoti) and 70% (G.
gecko) of the variation in duty factor from these multiple
regressions.
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With the addition of increasingly large loads, both gecko species take smaller but more strides per unit distance for a given speed (Table 7). The multiple regression analyses with stride length or stride frequency as dependent variable, and species, loading condition and speed as independent variables, show that for a given speed and load, the two species differ in stride length and stride frequency: G. gecko takes larger but fewer strides than H. garnoti (Table 7). For a given speed and load, G. gecko has a greater duty factor than H. garnoti, which is not surprising, as larger lizards likely need more time to push off with larger loads (Table 7).
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We also repeated the analyses in Table 7 by analyzing speed and stride length on a size-adjusted basis, by dividing both variables by mass, but keeping the other variables (independent variables = loading and species type; dependent variables = stride frequency and duty factor) constant (Table 8). This reanalysis shows that for a given relative speed and load, G. gecko takes larger relative strides at a lower frequency. At a given relative speed, both species use similar duty factors (no species effect) (Table 8).
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Discussion |
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The fact that H. garnoti produces similar amounts of power with
the 2% BM, 100% BM, 150% BM and 200% BM loads suggest a leveling-off of
mass-specific power output, which may prevent them from moving with larger
loads, or at faster speeds with a given load (see also
Fig. 5A). However, as a
cautionary note, our speeds in the unloaded condition for G. gecko
may be slightly less than maximum speed, which is not unusual when comparing
different locomotor performance studies on the same animals
(Irschick and Garland, 2001).
Indeed, it is important to compare maximum speeds across different data sets
(Irschick and Garland, 2001
).
R. Van Damme and A. Zaaf (unpublished data) measured maximal speeds on a
vertical incline for (unloaded) G. gecko of 1.44 m s-1
(measured over a fixed distance of 25 cm). Extrapolation of our data results
in a corresponding mass-specific output of 14.13 W kg-1. This new
value is similar to the maximal mass-specific power output obtained under the
100% BM loading condition (16.04 W kg-1). Again, this suggests a
leveling-off of mass-specific power output (see also
Fig. 5B). However, more data on
the maximum speeds of G. gecko may be necessary to determine which of
the above values more correctly estimates maximum speed in this species.
Moreover, another possible explanation for the pattern observed within either
species is that power does not limit maximum speed, but rather some other
factor that covaries with power is responsible.
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Irschick et al. (2001)
examined the power output of H. garnoti running at submaximal
preferred speeds with 30% BM and 60% BM loads on a vertical force platform,
and concluded that power output did not limit maximum speed. However, that
conclusion was based on submaximal running, as opposed to maximal or
near-maximal running in the current study. Thus, power may not limit uphill
loaded locomotion until geckos run at maximum speeds. Farley
(1997
) examined power output
in two species of small (<10 g) terrestrial lizards when running unloaded
on level and inclined surfaces (+20°, +40°) and concluded that the
mechanical power required to lift the body vertically was 3.9 times greater
than the external mechanical power output when moving on the level surface. By
comparison, H. garnoti double their mean power output on changing
from running unloaded uphill to running uphill with a 200% BM load. Farley
(1997
) found that power output
continued to increase as each lizard species ran up successively steeper
inclines, even though maximum speed declined, thus refuting the hypothesis
that mass-specific power limits maximum speed. This difference between the
work of Farley (1997
) and ours
can be explained by the different demands of horizontal and vertical running
in lizards. When running either horizontally or on an incline when unloaded,
maximum power output clearly does not limit maximum speed in lizards, but in
our experiments, we forced the lizards to conduct tasks (running uphill with a
load) that we knew would result in much higher total power outputs. Thus, it
is possible that power output does not limit maximum speed for lizards running
up relatively shallow inclines, or that move on horizontal surfaces, but power
may limit vertical locomotion in lizards, particularly when moving with large
loads.
A general finding emerging from comparative studies is that animals are
capable of producing substantially more power than they may use for everyday
activities (Askew and Marsh,
1997; Chai et al.,
1997
; Chai and Dudley,
1995
; Farley,
1997
). Activities that require high power output include take-off
(quail; Askew and Marsh, 2002
),
running vertically with loads (present study), and hovering under high loading
conditions (hummingbirds; Chai et al.,
1997
). However, an unresolved question for most animal groups is
the ecological context in which these high power outputs are used (if at all).
In the case of geckos, one possibility is the need to run uphill effectively
when carrying large loads in the form of eggs, or large food items (R. Huey,
personal communication). Female geckos and other lizards
(Bauwens and Thoen, 1981
) can
carry eggs weighing as much as 10-30% of their body mass. In the present work,
we examined geckos carrying loads much greater than they are ever likely to
carry in nature, but our data do indicate that the muscular and locomotor
apparatus of geckos appears to be highly `overbuilt' relative to their
ecological requirements. An important reason for this could be the subdigital
toepads used by geckos to grasp onto surfaces
(Russell, 1979
;
Irschick et al., 1996
). In a
recent study of gecko setae, Autumn et al.
(2000
) estimated that tokay
geckos (G. gecko) are capable of generating forces up to 100 N with
one foot, while whole-organism clinging studies
(Irschick et al., 1996
) showed
that these lizards typically achieve clinging forces of about 10 N for a
single foot. Thus, if tokay geckos were able to recruit all of their setae
simultaneously, they would be capable of carrying very large loads indeed.
Consequently, even based on the whole-organism clinging studies by Irschick et
al. (1996
), the ability of the
toepads to cling is not the limiting step as to why either species could not
carry greater loads.
Another aspect of locomotion that requires high power output is
acceleration, especially during sharp turns such as observed in the C-start
escape response of fish (Wakeling and
Johnston, 1998). The ability to make abrupt turns is a key part of
the escape response of geckos, although few studies have examined such
`maneuvering' ability in lizards (but see
Van Damme and Vanhooydonck,
2002
; Vanhooydonck and Van
Damme, 2003
), and its relation to power output.
Does body size affect mass-specific power output?
Due to a lack of loading studies for animals moving uphill, the most
relevant available studies for examining the effects of loading on
mass-specific power output are of flying organisms such as insects, bats and
birds. The dynamics of moving directly uphill and flying are similar, in that
in both cases animals must work against gravity, and thus produce a
substantial amount of power. Marden
(1987) examined the largest
load that several insect, bat and bird species could carry to understand
whether species of different sizes can carry the same percentage of body mass.
Contrary to theoretical predictions, the maximum lift per unit flight muscle
mass was similar among taxonomic groups (54-63 N kg-1). On this
basis, large flying animals (e.g. birds, bats) were capable of carrying
similar loads (as a percentage of body mass) to relatively small flying
animals, such as insects. In addition, interspecific differences in
short-duration power output were primarily related to the flight muscle ratio
(ratio of the mass of flight muscles divided by all other muscles in the wing;
Marden, 1987
), suggesting that
species with high mass-specific power outputs have evolved large amounts of
flight muscle.
While our results show that H. garnoti has a higher maximal mass-specific power output than G. gecko, one should interpret this difference cautiously. Because the unloaded speeds of G. gecko may be slightly less than maximum capacity, it is possible that we have underestimated their maximum power output. Extrapolation of our results to the maximal speed measured by Van Damme and Zaaf (see above) gives a mass-specific power output of 14.13 W kg-1. If we replace lower values of `maximal mass-specific power output' (for each individual) with this value, the difference between H. garnoti and G. gecko is not significant (one way ANOVA; F1,16=2.63, P=0.12). This result corresponds to those from studies on flying animals (see above). Thus, more data on the maximum speeds of G. gecko as well as its relationship to power output and loading appear to be necessary before firm conclusions can be drawn.
Does loading condition affect speed modulation?
Several studies have investigated the effects of loading on energetics
(Taylor et al., 1980;
Herreid and Full, 1985
;
Kram, 1996
), kinematics
(Wren et al., 1998
;
Zani and Claussen, 1995
;
Hoyt et al., 2000
) and
performance (Zani and Claussen,
1995
; Wren et al.,
1998
), but few studies have studied the effects of loading on
mass-specific power output and kinematics when moving uphill.
First, it is clear from our results that the addition of weights does not
affect the speed modulation strategy of either H. garnoti or G.
gecko. Regardless of loading condition, speed increases primarily by
increasing stride frequency in both species. The fact that geckos modulate
their speed mainly by altering stride frequency and not stride length is in
accordance with the results of Zaaf et al.
(2001), who found that G.
gecko is primarily a frequency modulator on both vertical and horizontal
surfaces.
At a given speed, however, the addition of loads significantly affects both
stride length and stride frequency. Both species take smaller but more strides
with heavier loads and thus, the effect of loading condition seems to be the
same in H. garnoti and G. gecko. It is unclear why this is
the case. Smaller steps (and hence strides) with heavier loads might reflect
`uncertainty' on part of the animal, analogous to the hesitant small steps of
humans walking on slippery surfaces, or of impaired or elderly people
(Zatsiorsky et al., 1994;
Grabiner, 1997
;
Vaughan, 1997
). The increase
in stride frequency when carrying a load, as observed in this study,
corresponds to the results of some studies on load carrying (e.g.
Cooke et al., 1991
), but
differs from others (e.g. Hoyt et al.,
2000
). The effects of loading and size on duty factor are also
apparent. First, within H. garnoti at a given speed, duty factor
increases with increased loading, while for a given load, duty factor declines
with speed. Similarly, within G. gecko at a given speed, duty factor
also increases with loading. These results make intuitive sense, as the
addition of loads probably forces these lizards to spend more time pushing
against the ground to generate the required forces for movement.
Problems with comparing findings from previous loading studies are not only
the difference in locomotor speeds examined, but also the taxonomic diversity
among studies. Some studies examined the effects of loading on animals moving
at slow preferred speeds (Hoyt et al.,
2000; Wickler et al.,
2001
), whereas other studies examined loading effects on maximum
speeds (Zani and Claussen,
1995
; Wren et al.,
1998
). The addition of loads up to 150% BM significantly decreased
maximum speed, stride length and stride frequency in turtles
(Zani and Claussen, 1995
;
Wren et al., 1998
). However,
for several mammal species moving over a range of speeds, and with loads of
7-27% BM, no significant effects of loading on stride frequency were observed
(Taylor et al., 1980
). From
the interspecific comparison, on the other hand, it is clear that, for a given
load and at a given speed, G. gecko takes longer strides while H.
garnoti takes more strides. Surprisingly, this does not seem to be the
result of the differences in dimensions between the two species. At similar
relative speeds, G. gecko still takes longer relative strides than
H. garnoti. Thus, loading effects on gait characteristics seem to be
both speed- and species-dependent; more comparative data for different species
moving with loads on level and inclined surfaces would be welcome.
In sum, several key findings are apparent from our data. First, several lines of evidence suggest that power limits maximum speed in both gecko species. Stride frequency does not level off as speed increases for any loading condition in either species, suggesting that lizards do not reach a maximum stride frequency that they cannot exceed. Further, even though mass-specific power output increases significantly between the unloaded and any loaded condition, the small H. garnoti produces similar amounts of power when running with 150% and 200% BM loads, suggesting that they have reached their power limit. Second, while the large gecko produced approximately 33% less maximum power than the smaller H. garnoti, this difference disappeared when we used the slightly higher speeds for G. gecko gathered by other researchers. Finally, speed is primarily modulated by changes in stride frequency, regardless of loading condition and species. At a given speed, on the other hand, the addition of loads causes both species to take smaller, but more, strides per unit distance.
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Acknowledgments |
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Footnotes |
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