|
| |
|
|
|
|
||||
| Home Help Feedback Subscriptions Archive Search Table of Contents | ||||
First published online March 30, 2006
Journal of Experimental Biology 209, 1404-1412 (2006)
Published by The Company of Biologists 2006
doi: 10.1242/jeb.02155
Effects of temperature on maximum acceleration, deceleration and power output during vertical running in geckos
Department of Ecology and Evolutionary Biology, 310 Dinwiddie Hall, Tulane University, New Orleans, LA 70118, USA
* Author for correspondence (e-mail: pbergman{at}tulane.edu)
Accepted 7 February 2006
 |
Summary |
|---|
 TOP Summary IntroductionMaterials and methodsResultsDiscussionReferences |
|---|
1.2x) between 25°C
and 35°C. Mass-specific power output was more temperature-sensitive,
increasing 2.5x up to 25°C and a further 1.4x above that
temperature. Stride length increased 1.5x over the entire temperature
interval studied, while stride duration decreased by a factor of 1.9,
suggesting that velocity is modulated by changes in both stride length and
duration in P. dubia. Duty factor was not significantly influenced by
temperature. Stride length was the only kinematic measure to be influenced by
stride number, with second steps from a standstill being longer than first
steps. We discuss the significance of velocity and acceleration being affected
in a similar manner by temperature, and that speed is modulated by both
changes in stride length and duration.
Key words: performance, acceleration, power, kinematics, lizard, Phelsuma dubia, gecko, temperature, performance
|
Introduction |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
; Huey and
Kingsolver, 1989; DeNardo et
al., 2002; Ishii et al.,
2004; Sollid et al.,
2005). The effects of temperature on steady speed locomotion have
been fairly well studied, particularly in ectotherms such as lizards and fish
(Huey and Bennett, 1987;
Garland, Jr and Losos, 1994).
Ecological studies have also linked variation in preferred body temperature
with variation in some aspects of locomotor performance, such as maximal
velocity, for some taxa (Pough,
1989; Bennett and Huey,
1990; Blouin-Demers et al.,
2003; reviewed by Huey and
Kingsolver, 1989). However, temperature effects on maximum
acceleration during running and other modes of locomotion are generally poorly
understood (but see Vanhooydonck et al.,
2005; Vanhooydonck et al.,
2006; B. Vanhooydonck, A. Herrel and D. J. Irschick, manuscript
submitted).
Although prior studies have focused on maximal velocity as a key measure of
locomotor performance in lizards and other animals
(Bennett, 1990;
Garland, Jr and Losos, 1994;
Irschick and Garland, Jr,
2001), some studies have suggested that maximum speed may be less
relevant than acceleration for animal fitness
(Braña, 2003; see also
Huey and Hertz, 1982;
Huey and Hertz, 1984a). Many
animals move unsteadily in nature, producing bursts of acceleration, and
therefore high acceleration capacities form an important component of their
escape responses (Huey and Hertz,
1982; Huey and Hertz,
1984a; Domenici and Blake,
1997; Irschick and Jayne,
1998; Vanhooydonck et al.,
2005). For example, the C-starts of fish are a stereotyped escape
response composed of high accelerations that are critical for effective escape
from predators and capture of prey
(Domenici, 2003). These
unsteady movements often produce high power outputs, such as when frogs or
birds jump, or when lizards start running from a standstill
(Aerts, 1998;
Irschick and Jayne, 1998;
Wilson et al., 2000).
Therefore, examination of temperature effects on acceleration also provides an
opportunity to examine temperature effects on power output. Finally, frequent
deceleration is another implication of intermittent locomotion as yet
unexamined. The ability to quickly decelerate, as opposed to accelerate
forward, is important for high maneuverability because deceleration
facilitates changes in the direction of movement
(Domenici and Blake, 1997;
Domenici et al., 2004),
whereas acceleration facilitates movement along a chosen trajectory.
Prior work on muscles in vitro provides a testable framework for
relating whole-organism power output with temperature. Swoap et al.
(Swoap et al., 1993) found
that the maximum mass-specific power output of fast-twitch muscle fibers from
the lizard Dipsosaurus dorsalis increased substantially with
temperature (from 20 W kg–1 at 15°C to 154 W
kg–1 at 42°C), but we lack data for testing if this
increase also occurs at the whole organism level
(Askew and Marsh, 2002). Swoap
et al. (Swoap et al., 1993)
showed that at low temperatures, the optimal cycling frequency for producing
maximum power output was attainable for the lizard Dipsosaurus
dorsalis, whereas at higher temperatures, the optimal cycling frequency
of isolated muscle was higher than maximal limb cycling frequency in
vivo (about 20 Hz). Again, however, we lack data on how live animals
modulate their kinematics (e.g. stride frequency, stride length) across a
range of temperatures during unsteady burst locomotion, when they require
maximal power. Furthermore, when considering the whole organism, one must also
consider behavioral alterations across different temperatures
(Bennett, 1980;
Bennett, 1990). For example,
low body temperatures in many lizards correlate with decreased velocity, but
also result in increased aggressiveness and increased flight distance
(Bennett, 1990).
Geckos offer an excellent opportunity to examine ideas regarding maximum
power output, acceleration, deceleration and kinematics, as they will readily
run both uphill and unsteadily, two conditions that should elicit high power
output. Indeed, the escape movements of arboreal geckos are composed largely
of brief, rapid accelerations and decelerations, and so represent an excellent
model system for unsteady locomotion
(Irschick et al., 2003;
Vanhooydonck et al., 2005).
Geckos will also often run readily across a range of temperatures. Finally,
geckos are somewhat unique in that they primarily modulate speed by increasing
stride frequency, but not stride length
(Zaaf et al., 2001;
Irschick et al., 2003), thus
providing a simple system in which locomotor performance is modulated
primarily by a single kinematic variable. However, these findings were
conducted under a constant temperature, and it is possible that geckos will
modulate both stride frequency and stride length when exposed to a variety of
temperatures.
We examined how maximum velocity, acceleration, deceleration and several
simple kinematic variables (e.g. stride frequency and duration) changed across
a variety of temperatures when a small diurnal gecko (Phelsuma dubia
Boettger) ran uphill. This species was appropriate for study because it is an
agile animal that moves by burst locomotion on vertical surfaces. We induced
the same group of lizards to accelerate uphill from a standstill on a smooth
vertical surface at body temperatures ranging from 15–35°C and
filmed all movements using a high-speed digital camera. From these data, we
asked two specific questions. (1) How do acceleration and deceleration
capacity, as well as mass-specific power output, change with temperature? (2)
How do geckos modulate kinematics (e.g. stride frequency, stride length)
across a variety of temperatures? We then discuss our findings in the context
of previous work investigating relationships between temperature and power
output in single muscle fibers (e.g. Swoap
et al., 1993).
|
Materials and methods |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
We collected body mass and SVL measurements prior to sprinting performance trials. Subsequent to all trials, animals were euthanized with intraperitoneal nembutal injection, fixed with formalin, and preserved in 70% ethanol. All experiments were approved by the Institutional Animal Care and Use Committee at Tulane University (IACUC approval 0189-2-16-0301).
Performance trials and calculations
Sprinting ability for Phelsuma dubia was quantified at five
different temperatures: 15, 20, 25, 30 and 35°C, and each lizard was run
twice at each temperature. The temperature range was chosen because at
15°C the geckos were very sluggish and at 35°C one individual lost
consciousness and was eliminated from inclusion in any trials. Temperatures
outside of the chosen range were not attempted out of concern for the
wellbeing of the subjects. We know of no other studies that provide
information on field, preferred or optimal body temperatures for this species.
Although we know of no studies that directly address the temperature ranges to
which P. dubia are exposed to in the wild, the species lives in
northwestern Madagascar, particularly centered around the Mahajanga region
(Glaw and Vences, 1994), and
temperatures in this area range between 17°C and 33°C
(Boisier et al., 2002).
Furthermore, many diurnal and nocturnal lizards have thermal optima at about
30°C (Autumn, 1999).
Lizards were induced to run upwards on a vertically oriented custom built
race track, 10 cm wide and 1.5 m long, with Plexiglas walls (see
Irschick et al., 2003). The
wooden base of the race track was covered in Plexiglas, ensuring a smooth and
uniform surface for running. Lizards were placed on the track, facing upward,
and were induced to run with a tap on the tail base. All geckos were placed in
a Tritech Research Inc. (Los Angeles, CA, USA) DigiThermTM DT2-MP
incubator set to the desired temperature 1 h prior to sprinting trials. Their
body temperature was measured immediately prior to trials using a Cox
Technologies DE-305 digital thermometer (Belmont, NC, USA) to ensure that it
was within 1.5°C of the desired temperature. Lizards were placed back into
the incubator immediately following each trial, and were allowed at least 1 h
between trials to rest for their body temperature to stabilize at the desired
temperature.
Sprinting trials were filmed from dorsal view using a high-speed video
camera (Redlake Motionscope PCI camera; San Diego, CA, USA) at 250 frames per
second (f.p.s.) and saved to computer in avi format (following
Irschick et al., 2003;
Vanhooydonck et al., 2005).
Only sequences in which the lizard ran from a standstill were analysed because
we were interested in acceleration capacity during non-steady state movements
(Irschick and Jayne, 1998).
Furthermore, trials were only included when the lizard ran predominantly
vertically, without undue lateral movement
(Farley, 1997), and when the
lizard appeared to be well motivated. Phelsuma dubia was chosen
because it moves intermittently, but this quality made it difficult to obtain
trials including movement over long distances. Only trials where the subject
moved greater than 0.1 m in total distance were included.
All included sequences were imported into MOTUS Peak Performance software
(2000; Peak Motus® 6.0 User Manual, Peak Performance Technologies,
Englewood, NJ, USA) and the tip of the snout was digitized at 250 f.p.s. The
issue of frame rates is an important one for studies of acceleration due to
potential effects on digitizing error
(Walker, 1998). Based on
simulation studies, error rates are lower at frame rates of 250 f.p.s. than at
other frame rates, and we have also used this frame rate in other studies of
lizard acceleration (Irschick and Jayne,
1998; Irschick et al.,
2003; Vanhooydonck et al.,
2005; Vanhooydonck et al.,
2006; B. Vanhooydonck, A. Herrel and D. J. Irschick, manuscript
submitted). Frame-by-frame digitization commenced about 20 frames prior to any
movement to minimize edge effects associated with smoothing
(Walker, 1998; B.
Vanhooydonck, A. Herrel and D. J. Irschick, manuscript submitted), and ended
when the lizard either stopped or ran from the field of view. Inter-observer
digitizing error was eliminated by using only a single person for initial
digitizing. Digitizing error was further minimized by frame-by-frame
proof-reading and correction of initial outliers, acting to increase precision
and decrease noise (Crenshaw et al.,
2000). Digitizing error was quantified by digitizing a trial five
times, calculating instantaneous velocities and accelerations, and calculating
the coefficient of variation (CV) for maximal velocity, acceleration and
deceleration.
Another important issue in studies of acceleration is the algorithm used
for smoothing and filtering raw XY data
(Walker, 1998). The
XY coordinates obtained from digitization were smoothed using a
quintic spline processor implemented in the MOTUS software package, and
instantaneous velocity and acceleration were calculated for each frame by
differentiation of the quintic spline functions
(Vanhooydonck et al., 2005).
MOTUS implements the quitic spline using a generalized cross-validatory
algorithm (GCV) (2000; Peak Motus® 6.0 User Manual). We used a quintic
spline procedure because this approach is least biased and error prone,
outperforming most other available methods
(Walker, 1998). Although the
mean square error algorithm outperforms even the GCV, this approach is not
implemented in Peak MOTUS. The GCV algorithm suffers from increased error at
low magnifications and very high sampling rates, so we used the 2x
magnification tool in MOTUS while digitizing and a frame rate of 250 f.p.s.
These settings are optimal for the GCV algorithm, resulting in estimates of
velocities and accelerations on a par with the more stable mean-square error
algorithm for the quintic spline (Walker,
1998).
The largest value for each of these measures, as well as maximal
deceleration (highest negative acceleration), at each temperature was retained
for each individual. Only the single best trial was retained for any one
temperature for each individual. Mass-specific power (MSP) was then
calculated for each trial in Microsoft Excel using the equation:
 | (1) |
 | (2) |
 | (3) |
;
Vanhooydonck et al., 2006; B.
Vanhooydonck, A. Herrel and D. J. Irschick, manuscript submitted). A caveat of
our approach is that it assumes that movements of the center of mass are well
approximated by the tip of the snout. The validity of this assumption is
untested, to our knowledge, but may be justified by the observation that the
snout is displaced in similar ways to the body. Calculating power from
XY coordinates has also been done by Irschick et al.
(Irschick et al., 2003), but
during steady state locomotion. Power was calculated for each frame in a
trial, and the maximal MSP in the trial selected for further
analysis. This accounts for the fact that maximal acceleration and velocity,
and therefore MSP, may not be generated at the same time during
locomotion. Finally, we calculated basic kinematic variables for the right hind limb from a dorsal view from displacement and frame number data. These included stride length and stride duration, step length and step duration, and duty factor. A stride was defined from foot up until the next foot up. A step was defined while the foot was in contact with the ground (foot down until foot up). Duty factor was defined as the proportion of the step cycle that the foot is in contact with the ground (step duration divided by stride duration).
Statistical analysis
All statistical analyses were carried out using SYSTAT 10.2
(Wilkinson, 2002). Performance
data (velocities, accelerations and MSP) were log-transformed prior
to analysis because untransformed data yielded residuals that were often not
normal and always heteroscedastic. Kinematic data (lengths, durations and duty
factor) were not log-transformed because these data yielded residuals that
were almost always normal and homoscedastic. The assumptions of normality and
homoscedasticity of residuals were tested using Kolmogorov–Smirnov (KS)
and Fmax tests, respectively.
Maximal instantaneous velocity, acceleration, deceleration and MSP
were analyzed using repeated-measures analyses of variance (RM-ANOVAs)
(Farley, 1997) with
temperature as a fixed factor (Model I;
Sokal and Rohlf, 1995). These
data were also analysed using repeated-measures analyses of covariance
(RM-ANCOVA) with log-transformed mass as a covariate to evaluate the
influences of mass on performance measures. Stride duration and length, step
duration and length, and duty factor were analyzed using two-factor RM-ANOVAs,
with temperature and step number as fixed factors. In all analyses,
temperature included five treatment levels (15, 20, 25, 30 and 35°C). For
two-factor ANOVAs, step included two levels: steps one and two. This was
deemed appropriate because the majority of acceleration occurs during the
first two strides (fig. 7 in Irschick and
Jayne, 1998), and because missing data for some individuals for
the third stride would have decreased the sample size of the analysis.
Pairwise post-hoc tests for repeated-measures designs
(Wilkinson, 2002) were used to
examine specific differences in dependent variables among temperature levels,
and all pairwise comparisons were run. A sequential Bonferroni correction
(Rice, 1989) was applied for
each analysis conducted (five treatment levels resulting in ten pairwise
comparisons).
|
Results |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Maximal instantaneous velocity, acceleration, deceleration and MSP were unaffected by mass (Table 1) and significantly affected by temperature (Tables 2 and 3). All analyses presented henceforth are RM-ANOVAs that ignore mass because it had no significant effects. Table 2 shows mean values for each of these performance measures at each temperature and Table 3 shows RM-ANOVA results. In all cases, there was a general trend of increase in the performance measure as temperature increased (Fig. 1). However, when examined in more detail, the degree to which this trend was pronounced differed among measures. For example, post-hoc tests for maximal instantaneous velocity (Fig. 1A) and maximal MSP (Fig. 1D) showed a similar trend of significant temperature dependence at temperatures below 25°C, with a plateau at temperatures above 25°C (i.e. no significant differences). This trend is still apparent for maximal instantaneous acceleration (Fig. 1B) and deceleration (Fig. 1C), but is less pronounced, with fewer significant differences between adjacent temperature levels. A lower relative significance to this increasing trend with temperature is indicated by far greater F statistics associated with RM-ANOVAs for velocity and power, than for acceleration and deceleration (Table 3). Despite the observed differences in the degree of significance between these performance measures, all show a similar increase in magnitude with increases in temperature (Table 2). Maximal velocity shows a 2.3x increase between 15°C and 35°C, while maximal acceleration shows a 2.2x increase between 15°C and 30°C and maximal deceleration shows a 2.1x increase over the same temperature range (Table 2). In contrast, maximal MSP increases 3.5x in magnitude between 15°C and 35°C.
|
|
|
|
For most of the kinematic variables considered, step number (one versus two) had no significant influence (Table 4). The only exception to this was stride length, in which the second stride was significantly (1.25x) longer than the first stride (Table 4). In contrast, temperature had a significant effect on almost all kinematic variables considered, except duty factor, which was unaffected by either temperature or step number, and had a mean value of 0.91 (Table 4). Although temperature had a significant effect on both step duration and step length, the trend was less pronounced, but in the same direction, as for stride duration and length (F statistics; Table 4). Therefore, only graphs for the stride data are shown (Fig. 2). Stride duration significantly decreased with increasing temperature (Fig. 2A), while stride length increased with temperature (Fig. 2B). As temperature increased, P. dubia took longer and faster (or higher frequency) steps. However, changes in stride duration (a 1.9x decrease between 15°C and 35°C) were more pronounced than changes in stride length (a 1.4x increase).
|
|
|
Discussion |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
;
Marsh and Bennett, 1986;
Swoap et al., 1993).
Diurnal lizards generally have high temperature preferences and optima
(Huey and Bennett, 1987), and
this is also the case for secondarily diurnal geckos
(Autumn, 1999). This pattern
was supported by our data for Phelsuma dubia
(Fig. 1). We found that
velocity increased 1.8x as temperature increased from 15°C to
25°C, and then levelled off between 25°C and 35°C (increasing only
1.2x; Fig. 1A). Such a
trend, complete with a performance plateau at high temperatures, has also been
found in lygosomine skinks (Huey and
Bennett, 1987), a number of other disparate lizard taxa
(Bennett, 1980;
Marsh and Bennett, 1985), and
various ectotherms in general (Huey and
Kingsolver, 1989). Quantitatively, this compares quite closely
with reported Q10 values of 2–3 below 25°C and
1–1.5 above that temperature for a variety of vertebrate ectotherms
(Bennett, 1990). Low but
apparent thermal dependence of performance is contrasted by much higher
thermal dependence of underlying physiological processes
(Bennett, 1980).
Acceleration has rarely been studied from a thermal-dependence perspective
(with emphasis being placed on power output instead – see below), but
has been shown to be independent of incline and comparable in the
phrynosomatid lizards Callisaurus draconoides and Uma
scoparia (Irschick and Jayne,
1998). We find that acceleration follows a similar trend to that
of velocity, increasing 1.7x as temperature increases between 15°C
and 25°C, but only 1.2x above that temperature
(Fig. 1B). Vanhooydonck and
coworkers also found a positive correlation between maximal acceleration and
velocity for the small nocturnal gecko Hemidactylus garnoti running
on different substrates, but at a single temperature (30°C)
(Vanhooydonck et al., 2005).
Interspecifically, Vanhooydonck and coworkers (B. Vanhooydonck, A. Herrel and
D. J. Irschick, manuscript submitted) also found that acceleration capacity
correlates positively with sprint speed in Anolis lizards.
We observed that thermal dependence was less apparent for maximal deceleration. Although this performance measure also increased 1.7x below 25°C and 1.2x above that temperature, no significant increases were found above 20°C (Fig. 1C). Such low thermal dependence may be partially explained by the fact that the geckos were not forced to decelerate quickly. Although lizards were tapped on the tail to obtain maximal velocity and acceleration, no analogous procedure was implemented to force them to decelerate quickly, possibly contributing large variance around temperature means for deceleration (Fig. 1C). Future studies considering deceleration as a performance measure might require experimental designs forcing animals to use high degrees of manoeuvrability, such as a race track with obstacles. This design would further test whether geckos or lizards in general, can control deceleration in order to maximize manoeuvrability.
We found a highly pronounced trend of increasing mass-specific power output
with increasing temperature, similar to that for maximal velocity
(Fig. 1D). That is,
MSP increased by a factor of 2.4 up to 25°C and then levelled
off, increasing 1.4x up to 35°C. Such a trend is unsurprising, given
that MSP was calculated as the product of instantaneous velocity and
acceleration (see Materials and methods), and it is similar to the trend found
for other in vitro studies of lizard muscle function, but with a
lower thermal optimum (Marsh and Bennett,
1985; Marsh and Bennett,
1986; Swoap et al.,
1993). For example, Swoap et al.
(Swoap et al., 1993) found the
power output optimum for fast glycolytic fibres of the iliofibularis muscle in
Dipsosaurus dorsalis occurred at 42°C, and Marsh and Bennett
(Marsh and Bennett, 1985)
detected a very similar value of 40°C for the same muscle in the same
species. Marsh and Bennett (Marsh and
Bennett, 1986) also found that maximal isometric force generation
in the diurnal lizard Sceloporus occidentalis levels off between
20°C and 35°C. Given that we found that both maximal velocity and
maximal MSP level off above 25°C in Phelsuma dubia, it
is possible that velocity is limited by power output at high temperatures in
this species as well (see also Irschick et
al., 2003).
However, the performance measures considered herein may be further
influenced by the experimental setup and hence are not easily generalized to
horizontal locomotion. Studying vertical locomotion in geckos is ecologically
meaningful on account of their adhesive abilities
(Ruibal and Ernst, 1965;
Hiller, 1976;
Russell, 1979), and other
studies have employed a similar setup
(Irschick et al., 2003;
Vanhooydonck et al., 2005).
However, due to the effects of gravity, velocity and acceleration are expected
to be negatively influenced, while deceleration and power output are expected
to be enhanced because during vertical locomotion more power must be produced
than during horizontal locomotion to overcome the effects of gravity
(Farley, 1997; B.
Vanhooydonck, A. Herrel and D. J. Irschick, manuscript submitted).
Finally, our study, like many others, is focused on maximal instantaneous performance, which may not yield a complete picture of locomotion in animals. Specifically, further research that incorporates measures of average performance (i.e. average velocity, acceleration, etc.) would coincide more closely with our kinematic variables of stride length and duration. However, the interpretation of such data for our study may be confounded by our focus on unsteady locomotion, and would be more straightforward for studies of steady state locomotion.
Thermal dependence of kinematics
An animal's velocity is a product of its stride length and stride frequency
(Biewener, 2003), and hence
velocity, can be modulated by changing either or both of these kinematic
variables. Most non-mammalian quadrupeds increase speed by increasing both,
with an increased reliance on modulating stride length at high speeds
(Biewener, 2003). Geckos are a
noted exception to this rule because they primarily modulate their speed by
changing stride frequency, at least under steady state locomotion
(Zaaf et al., 2001;
Irschick et al., 2003). We
documented that as temperature increased from 15°C to 35°C, stride
duration decreased (i.e. stride frequency increased) by a factor of 1.9, and
stride length increased by a factor of 1.5
(Fig. 2). Hence, our findings
are typical for quadrupeds, but atypical for geckos. These results underscore
that changes in temperature can result in behavioural alterations that might
not be observed at a single temperature
(Huey and Hertz, 1982;
Huey and Hertz, 1984b).
However, Fig. 2 also shows that
increases in speed result more through the modulation of stride duration than
of stride length. A similar trend was documented by studies of the iguanid
lizard Dipsosaurus dorsalis
(Marsh and Bennett, 1985;
Swoap et al., 1993; but see
Fieler and Jayne, 1998).
Stride length has been shown to increase with speed in horses during steady
state locomotion, along with a decrease in stride duration
(Hoyt et al., 2000). The
stork, Ciconia ciconia, also increases speed primarily by increasing
stride frequency, and only secondarily by increasing stride length during
steady state locomotion (van Coppenolle
and Aerts, 2004). Our study is somewhat unique in that we examined
unsteady state locomotion, but this may also be a confounding factor, as
stride length increases over the first few steps of acceleration
(Irschick and Jayne, 1998)
(Table 4).
Although we examined duration and length data for both strides and steps
(stance phase) for P. dubia, stride data are emphasized because they
give clearer, more significant patterns than step data. Stride and step data
also show similar patterns (i.e. decreases in duration and increases in length
with temperature). The importance of the stance phase should not be
discounted, however, as this is the part of the stride during which all force
is generated (Hoyt et al.,
2000). Since the rate of force application to the substrate is
inversely proportional to step duration
(Hoyt et al., 2000), the
shorter steps (e.g. shorter durations) exhibited by P. dubia at high
temperatures translate into more force being applied per unit time, even if
the geckos' velocity did not increase with temperature.
Duty factor has variously been reported to change with the velocity of
locomotion. In general, duty factor decreases as velocity increases, and this
has been documented in animals as disparate as storks
(van Coppenolle and Aerts,
2004) and horses during level and incline locomotion
(Dutto et al., 2004). In
contrast, duty factor increased in the newt Taricha torosa when
walking in water relative to on land
(Ashley-Ross and Bechtel,
2004). Duty factor again decreased with increased velocity in
lizards: Dipsosaurus dorsalis
(Fieler and Jayne, 1998),
Callisaurus draconoides and Uma scoparia
(Irschick and Jayne, 1998).
Irschick et al. (Irschick et al.,
2003) also found that duty factor decreased with increasing speed
in two species of gecko. Our findings show a different pattern from that
documented in these studies, in that duty factor did not change with
increasing temperature or stride number
(Table 4), although speed did
increase. This has the implication that in P. dubia moving
vertically, reductions in stride duration and step duration are coincident as
speed and temperature increase. These findings are surprising because Irschick
et al. (Irschick et al., 2003)
also examined geckos and forced them to run vertically. However, they varied
loading of the geckos, as opposed to temperature, which may contribute to
observed differences between the two studies.
An increasing number of studies are examining acceleration and power output
during different modes of locomotion in various animals. Jumping has received
considerable attention in this regard in cats
(Harris and Steudel, 2002),
frogs (Wilson et al., 2000)
and Anolis lizards (Toro et al.,
2003). Similar considerations have also arisen for flight in quail
(Askew and Marsh, 2001;
Askew and Marsh, 2002), escape
response in lobster (Nauen and Shadwick,
1999), and in fishes (Ellerby
et al., 2001; Domenici,
2003; Domenici et al.,
2004). Our study is one of relatively few to consider acceleration
and power output in lizards (but see Huey
and Hertz, 1982; Huey and
Hertz, 1984a; Farley,
1997; Vanhooydonck et al.,
2005; Vanhooydonck et al.,
2006; B. Vanhooydonck, A. Herrel and D. J. Irschick, manuscript
submitted). To our knowledge, our study is the first to consider deceleration
ability, which may be correlated with manoeuvrability, as a performance
measure. Although velocity may be ecologically relevant when outrunning a
predator (Bennett and Huey,
1990; Irschick and Garland,
Jr, 2001), and acceleration may be important during prey capture
or initial evading of a predator (Huey and
Hertz, 1982; Vanhooydonck et
al., 2005), deceleration may also be a key component of evading
predators and capturing prey. While our study was not specifically designed to
evaluate maximal deceleration capacity, it provides a starting point for
further studies that could examine deceleration and manoeuvrability in more
ecologically realistic designs (Domenici
and Blake, 1997).
In general, our findings support the expected notion that lizards are
faster, accelerate/decelerate better, and produce more power at higher
temperatures. These findings are, at least partially, explained by modulation
of both stride length and stride duration, in contrast to other studies of
locomotion in geckos. However, all of our performance measures show a distinct
levelling off at high temperatures (typically above 25°C). This is
consistent with the assertion that evolution appears to have minimized the
impact of temperature on performance
(Bennett, 1980). Our findings
of relatively broad temperature optima for acceleration and power output
suggest that there is little cost in utilizing suboptimal body temperatures,
as long as they are in the broad plateau
(Huey and Hertz, 1984b;
Huey and Bennett, 1987),
resulting in a relatively shallow performance gradient
(Arnold, 1983).
|
Acknowledgments |
|---|
|
References |
|---|
|
TOPSummaryIntroductionMaterials and methodsResultsDiscussionReferences |
|---|
Aerts, P. (1998). Vertical jumping in Galago senegalensis: the quest for a hidden power amplifier.Philos. Trans. R. Soc. Lond. B 353,1607 -1620.[CrossRef]
Arnold, S. J. (1983). Morphology, performance and fitness. Am. Zool. 23,347 -361.
Ashley-Ross, M. A. and Bechtel, B. F. (2004).
Kinematics of the transition between aquatic and terrestrial locomotion in the
newt Tarisha torosa. J. Exp. Biol.
207,461
-474.
Askew, G. N. and Marsh, R. L. (2001). The
mechanical power output of the pectoralis muscle of blue-breasted quail
(Coturnix chinensis): the in vivo length cycle and its
implications for muscle performance. J. Exp. Biol.
204,3587
-3600.
Askew, G. N. and Marsh, R. L. (2002). Muscle
designed for maximum short-term power output: quail flight muscle.
J. Exp. Biol. 205,2153
-2160.
Autumn, K. (1999). Secondarily diurnal geckos return to cost of locomotion typical of diurnal lizards. Physiol. Biochem. Zool. 72,339 -351.[CrossRef][Medline]
Bennett, A. F. (1980). The thermal dependence of lizard behaviour. Anim. Behav. 28,752 -762.[CrossRef]
Bennett, A. F. (1990). Thermal dependence of locomotor capacity. Am. J. Physiol. 259,R253 -R258.
Bennett, A. F. and Huey, R. B. (1990). Studying the evolution of physiological performance. Oxford Surv. Evol. Biol. 7,251 -284.
Biewener, A. A. (2003). Animal Locomotion. Oxford: Oxford University Press.
Blouin-Demers, G., Weatherhead, P. J. and McCracken, H. A. (2003). A test of the thermal coadaptation hypothesis with black rat snakes (Elaphe obsolete) and northern water snakes (Nerodia spedon). J. Therm. Biol. 28,331 -340.[CrossRef]
Boisier, P., Rahalison, L., Rasolomaharo, M., Ratsitorahina, M., Mahafaly, M., Razafimahefa, M., Duplantier, J.-M., Ratsifasoamanana, L. and Chanteau, S. (2002). Epidemiologic features of four successive annual outbreaks of Bubonic Plague in Mahajanga, Madagascar. Emerg. Infect. Dis. 8,311 -316.[Medline]
Braña, F. (2003). Morphological correlates of burst speed and field movement patterns: the behavioural adjustment of locomotion in wall lizards (Podarcis muralis). Biol. J. Linn. Soc. Lond. 80,135 -146.[CrossRef]
Crenshaw, H. C., Ciampaglio, C. N. and McHenry, M. (2000). Analysis of the three-dimensional trajectories of organisms: estimates of velocity, curvature and torsion from positional information. J. Exp. Biol. 203,961 -982.[Abstract]
DeNardo, D. F., Luna, J. V. and Hwang, M. (2002). Ambient temperature activity of horned adders, Bitis caudalis: how cold is too cold? J. Herpetol. 36,688 -691.
Domenici, P. (2003). Habitat, body design and the swimming performance of fish. In Vertebrate Biomechanics and Evolution (ed. V. L. Bel, J. P. Gasc and A. Casinos), pp.137 -160. Oxford: Bios Scientific.
Domenici, P. and Blake, R. W. (1997). The kinematics and performance of fish fast-start swimming. J. Exp. Biol. 200,1165 -1178.[Abstract]
Domenici, P., Staden, E. M. and Levine, R. P.
(2004). Escape manoeuvers in the spiny dogfish (Squalus
acanthilas). J. Exp. Biol.
207,2339
-2349.
Dutto, D. J., Hoyt, D. F., Cogger, E. A. and Wickler, S. J.
(2004). Ground reaction forces in horses trotting up an incline
and on the level over a range of speeds. J. Exp. Biol.
207,3507
-3514.
Ellerby, D. J., Spierts, I. L. Y. and Altringham, J. D. (2001). Slow muscle power output of yellow- and silver-phase European eels (Anguilla anguilla L.): changes in muscle performance prior to migration. J. Exp. Biol. 204,1369 -1379.[Abstract]
Farley, C. T. (1997). Maximum speed and mechanical power output in lizards. J. Exp. Biol. 200,2189 -2195.[Abstract]
Fieler, C. L. and Jayne, B. C. (1998). Effects
of speed on the hindlimb kinematics of the lizard Dipsosaurus dorsalis.J. Exp. Biol. 201,609
-622.
Garland, T., Jr and Losos, J. B. (1994). Ecological morphology of locomotor performance in reptiles. In Ecological Morphology: Integrative Organismal Biology (ed. P. C. Wainwright and S. M. Reilly), pp. 240-302. Chicago: University of Chicago Press.
Glaw, F. and Vences, M. (1994). A Field Guide to the Amphibians and Reptiles of Madagascar (2nd edn.). Köln: Vences and Glaw Verlag.
Harris, M. A. and Steudel, K. (2002). The
relationship between maximum jumping performance and hind limb
morphology/physiology in domestic cats (Felis slivestris catus).
J. Exp. Biol. 205,3877
-3889.
Hiller, U. (1976). Comparative studies on the functional morphology of two gekkonid lizards. J. Bombay Nat. Hist. Soc. 73,278 -282.
Hoyt, D. F., Wickler, S. J. and Cogger, E. A. (2000). Time of contact and step length: the effect of limb length, running speed, load carrying and incline. J. Exp. Biol. 203,221 -227.[Abstract]
Huey, R. B. and Bennett, A. F. (1987). Phylogenetic studies of coadaptation-preferred temperatures versus optimal performance temperatures of lizards. Evolution 41,1098 -1115.[CrossRef]
Huey, R. B. and Hertz, P. E. (1982). Effects of
body size and slope on sprint speed of a lizard [Stellio
(Agama) stellio]. J. Exp. Biol.
97,401
-409.
Huey, R. B. and Hertz, P. E. (1984a). Effects
of body size and slope on acceleration of a lizard (Stellio stellio).
J. Exp. Biol. 110,113
-123.
Huey, R. B. and Hertz, P. E. (1984b). Is a jack-of-all-temperatures a master of none? Evolution 38,441 -444.
Huey, R. B. and Kingsolver, J. G. (1989). Evolution of thermal sensitivity of ectotherms performance. Trends Ecol. Evol. 4,131 -135.
Irschick, D. J. and Garland, T., Jr (2001). Integrating function and ecology in studies of adaptation: investigations of locomotor capacity as a model system. Annu. Rev. Ecol. Syst. 32,367 -396.[CrossRef]
Irschick, D. J. and Jayne, B. C. (1998). Effects of incline on acceleration, body posture, and hindlimb kinematics in two species of lizard, Callisaurus draconoides and Uma scoparia.J. Exp. Biol. 201,273 -287.[Abstract]
Irschick, D. J., Vanhooydonck, B., Herrel, A. and Androsceu,
A. (2003). Effects of loading and size on maximum power
output and kinematics in geckos. J. Exp. Biol.
206,3923
-3934.
Ishii, Y., Watari, T. and Tsuchiya, T. (2004).
Enhancement of twitch force by stretch in a nerve-skeletal muscle preparation
of the frog Rana porosa brevipoda and the effects of temperature on
it. J. Exp. Biol. 207,4505
-4513.
Marsh, R. L. and Bennett, A. F. (1985). Thermal dependence of isotonic contractile properties of skeletal muscle and sprint performance in the lizard Dipsosaurus dorsalis. J. Comp. Physiol. B 155,541 -551.[CrossRef][Medline]
Marsh, R. L. and Bennett, A. F. (1986). Thermal
dependence of contractile properties of skeletal muscle from the lizard
Sceloporus occidentalis with comments on methods for fitting and
comparing force–velocity curves. J. Exp. Biol.
126, 63-77.
Nauen, J. C. and Shadwick, R. E. (1999). The scaling of acceleratory aquatic locomotion: body size and tail flip performance of the California spiny lobster (Panulirus interruptus). J. Exp. Biol. 202,3181 -3193.[Abstract]
Pough, F. H. (1989). Organismal performance and Darwinian fitness: approaches and interpretations. Physiol. Zool. 62,199 -236.
Rice, W. R. (1989). Analyzing tables of statistical tests. Evolution 43,223 -225.[CrossRef]
Ruibal, R. and Ernst, V. (1965). The structure of digital setae of lizards. J. Morphol. 117,271 -294.[CrossRef][Medline]
Russell, A. P. (1979). Parallelism and integrated design in the foot structure of gekkonine and diplodactyline geckos. Copeia 1979,1 -21.
Sokal, R. R. and Rohlf, F. J. (1995). Biometry (3rd edn.). New York: W. H. Freeman and Co.
Sollid, J., Weber, R. E. and Nilsson, G. E.
(2005). Temperature alters the respiratory surface area of
crucian carp Carassius carassius and goldfish Carassius auratus.J. Exp. Biol. 208,1109
-1116.
Swoap, S. J., Johnson, T. P., Josephson, R. K. and Bennett, A. F. (1993). Temperature, muscle power output and limitations on burst locomotor performance of the lizard Dipsosaurus dorsalis.J. Exp. Biol. 174,185 -197.[Abstract]
Toro, E., Herrel, A., Vanhooydonck, B. and Irschick, D. J.
(2003). A biomechanical analysis of intra- and interspecific
scaling of jumping and morphology in Caribbean Anolis lizards.
J. Exp. Biol. 206,2641
-2652.
van Coppenolle, I. and Aerts, P. (2004). Terrestrial locomotion in the white stork (Ciconia ciconia): spatio-temporal gait characteristics. Anim. Biol. 54,281 -292.
Vanhooydonck, B., Andronescu, A., Herrel, A. and Irschick, D. J. (2005). Effects of substrate structure on speed and acceleration capacity in climbing geckos. Biol. J. Linn. Soc. Lond. 85,385 -393.[CrossRef]
Vanhooydonck, B., Aerts, P., Irschick, D. J. and Herrel, A. (2006). Power generation during locomotion in Anolis lizards: an ecomorphological approach. In Ecology and Biomechanics: A Mechanical Approach to the Ecology of Animals and Plants (ed. A. Herrel, T. Speck and N. Rowe), pp. 253-269. Boca Raton: CRC Press.
Walker, J. A. (1998). Estimating velocities and accelerations of animal locomotion: a simulation experiment comparing numerical differentiation algorithms. J. Exp. Biol. 201,981 -995.[Abstract]
Wilkinson, L. (2002). Systat. Richmond: Systat Software.
Wilson, R. S., Franklin, C. E. and James, R. S. (2000). Allometric scaling relationships of jumping performance in the striped marsh frog Limnodynastes peronii. J. Exp. Biol. 203,1937 -1945.[Abstract]
Zaaf, A. R., Van Damme, R., Herrel, A. and Aerts, P. (2001). Spatio-temporal gait characteristics of level and vertical locomotion in a level-running and a climbing gecko. J. Exp. Biol. 204,1233 -1246.[Abstract]
This article has been cited by other articles:
|
|
 |
|
  B. Vanhooydonck, A. Herrel, and D. J. Irschick Out on a limb: the differential effect of substrate diameter on acceleration capacity in Anolis lizards J. Exp. Biol., November 15, 2006; 209(22): 4515 - 4523. [Abstract] [Full Text] [PDF]
|
|
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
