285
Are powerful females powerful enough? Acceleration in gravid green
iguanas (Iguana iguana)
Jeffrey Scales1 and Marguerite Butler
Department of Zoology, University of Hawaii at Manoa, 2538 McCarthy Mall, Edmonson 152, Honolulu, HI 96822 and
Department of Ecology and Evolutionary Biology, 569 Dabney Hall, University of Tennessee, Knoxville, TN 37996–1610
Synopsis One demand placed exclusively on the musculoskeletal system of females is maintaining locomotor
performance with an increasing load over the reproductive cycle. Here, we examine whether gravid (i.e., ‘‘pregnant’’)
iguanas can increase their force and power production to support, stabilize, and accelerate the additional mass of a clutch
of eggs. At any acceleration, gravid iguanas produced very high mechanical power (average total power ¼ 673 w/kg; total
peak power ¼ 1175 w/kg). While the increase in total power was partly a result of greater propulsive power (average
propulsive power ¼ 25% higher, peak propulsive power ¼ 38% higher), increased vertical power (roughly 200% increase)
was the main contributor. Gravid iguanas were also able to increase peak forces (propulsive ¼ 23%, mediolateral ¼ 44%,
vertical ¼ 42%), and step duration (44%) resulting in greater impulses (i.e., the sum of force produced during a step) to
accelerate, balance, and support their increased mass. The increase in step duration and smaller increase in peak
propulsive force suggests that gravid iguanas may be force-limited in the direction of motion. We discuss how
biomechanical constraints due to females’ reproductive role may influence the evolution of the female musculoskeletal
systems and contribute to the evolution and maintenance of ecological dimorphism in lizards.
Introduction
During the lifetime of an animal, many different
functional demands are placed on its locomotor
system, including changes due to growth, reproduction, seasonal cycles in food supply, and predation
intensity. These diverse life history and seasonal
fluctuations may impose very different demands on
the musculoskeletal system, brought about by
changes in mass, overall size, nutritional status, or
increased performance requirements. However, most
locomotion studies consider only a single state at
steady speed (the few studies exploring the range of
functional capabilities are reviewed by Biewener and
Gillis 1999). Understanding how organisms cope
with the fluctuations experienced throughout the life
cycle is critical to understanding the selective
pressures and constraints responsible for the design
of the musculoskeletal system.
One demand placed exclusively on females is
maintaining locomotor performance during the large
increase in mass as females produce offspring or
eggs (gravidity). Since the females of many taxa
carry large reproductive loads, often repeatedly
throughout life, this is a widespread and potentially
important selective pressure that has received
relatively little study. Are females designed for the
gravid state, implying that their musculoskeletal
systems are overengineered for the majority of the
year? Or, alternatively, do they suffer a great
performance decline when they are gravid?
Gravidity is known to reduce sprint speed or
endurance in many taxa (birds: Lee et al. 1996;
Veasey et al. 2001; Kullberg et al. 2002; fish:
Ghalambor et al. 2004; salamanders: Finkler et al.
2003; snakes: Seigel et al. 1987), thereby increasing
the vulnerability of females to predators. Lizards,
which have often served as a model for locomotor
adaptation (Irschick and Garland 2001), have
commonly shown similar reductions in sprint speed
with gravidity (Shine 1980; Bauwens and Theon
1981; Van Damme et al. 1989; Sinervo et al. 1991).
In addition, female lizards with greater performance
capacity may have a competitive advantage for the
best home ranges or nesting sites. Therefore, females
that can effectively undergo locomotion while
carrying a reproductive load may enjoy a fitness
benefit over those that cannot.
One ecologically important locomotor task is
acceleration. Many animals use intermittent locomotion, which requires frequent accelerations.
From the symposium ‘‘Ecological Dimorphisms in Vertebrates: Proximate and Ultimate Causes’’ presented at the annual meeting of the Society
for Integrative and Comparative Biology, January 3–7, 2007, at Phoenix, Arizona.
1
E-mail: [email protected]
Integrative and Comparative Biology, volume 47, number 2, pp. 285–294
doi:10.1093/icb/icm054
Advanced Access publication June 18, 2007
ß The Author 2007. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. All rights reserved.
For permissions please email: [email protected].
286
Additionally, acceleration is important in determining the outcome of predator–prey interactions
(Elliot et al. 1977; Huey and Hertz 1984). The
increased mass of a clutch, however, will directly
reduce acceleration unless greater force is applied in
compensation (by Newton’s second law, we know
that acceleration is force divided by mass). Therefore,
a female carrying a reproductive load must increase
her production of force proportionally to her
increased mass to achieve the same acceleration.
In terrestrial animals, production of force can only
occur while the foot is in contact with the ground.
Therefore, animals carrying loads may compensate
by either increasing the magnitude of force produced, or by producing the same magnitude of force
but instead increasing the time over which it is
applied. The first will result in increased power, as
power is the product of force and velocity (all values
are instantaneous), whereas the second will not.
Green iguanas and acceleration while gravid
Green iguanas (Iguana iguana) provide an exceptional opportunity to investigate whether females can
accelerate when burdened with a clutch. Female
iguanas are excellent runners and carry very large
clutches (ranging from 31% to 63% of their
nongravid body mass). Despite this large reproductive load, female iguanas travel long distances to
reach their preferred nest sites, which presumably
increases their exposure to predators (Rodda 1992).
Upon arrival at the nest site, they excavate large nests
in the sand, all the while fighting off competing
females (Rand 1968). Thus, female iguanas are
probably under strong selection for locomotor
ability, precisely at the time when they perform
their most demanding locomotor tasks.
Additionally, acceleration is especially relevant for
escape of predators by iguanas. Iguanas commonly
use short sprints to refugia (e.g., burrows, bodies of
water) to avoid predators such as crocodiles, boa
constrictors, large birds of prey, tayra, coatis, wild
cats, and humans (Greene et al. 1978, personal
observation).
While most lizards show a reduction in performance
during gravidity (see references cited previously), we
found in a previous study that iguanas exhibit
impressive compensation (Butler, in review). Despite
reproductive loads of 31–63% of maternal mass, gravid
iguanas were able to match the acceleration of nongravid iguanas in the initial burst from a standstill.
This was a kinematic study only, where forces were not
measured. In the present study, we used force plate
analysis to test whether gravid iguanas can increase
their force and power production during a step, in
J. Scales and M. Butler
order to support, stabilize, and accelerate the increased
mass of a clutch.
Materials and methods
Thirteen gravid iguanas were collected from Boca
Raton, Florida (February, 2005) and transported to a
laboratory at the University of Tennessee. The
iguanas were group housed on a 12 h : 12 h D : L
cycle with food and water available ad libitum. UV
lights and ceramic heat lamps provided a temperature gradient suitable for basking, while room
temperature was maintained at 298C. Animal collection, care, and experimental protocols were approved
by the UTK IACUC (protocol no. 1203).
Reproductive conditions
Presence of eggs was determined by ultrasound, and
all iguanas were initially gravid. After 50 days
recovery from oviposition, females were rerun as
controls in running trials. Trials continued from 50
to 80 days postoviposition and no difference in
performance was found over this time. At this time,
iguanas had recovered a normal body tone, resumed
normal eating behavior, and had put on significant
weight. Furthermore, these animals returned to
normal rates of activity and resistance to being
handled by humans. We call this group ‘‘postgravid’’.
Acceleration trials
Prior to all running trials, iguanas were brought to a
standard body temperature of 35–378C by placing
them in a warm water bath. Body temperatures were
verified immediately prior to all runs. Iguanas were
placed immediately in front of a force-plate
embedded in a 7 m trackway. A startle-response
was elicited by rapid movements of a large cloth,
lunging movements towards the animal, or clapping
the tail of the iguana. Video and ground reaction
forces were recorded as the iguanas accelerated across
the force-plate. Gravid iguanas were run 1–2 times
per day, while recovered iguanas were run 2–3 times
per day. Iguanas were given a minimum of 15 min
rest between runs, and 2 days rest between trial days.
Only runs in which the iguana ran straight down the
trackway and an isolated hind limb landed on the
force-plate were considered for analysis (other limbs
were in contact with the ground, but not on the
force plate). Of these trials, the run with the highest
acceleration was selected for each individual for
each reproductive condition, gravid and recovered.
Therefore, while over 300 runs were collected, only
19 trials were used in the analysis. The health of
the iguanas was monitored continuously throughout
the experiment. Animals were removed from the
287
Acceleration in gravid green iguanas
experiment if they showed signs of fatigue, injury,
or poor health.
Video analysis
In order to digitize video images, reflective markers
made of retro-reflective tape (3M Scotchlite 8850
Silver Pressure Sensitive Adhesive Film, Motion Lab
Systems, Inc.) covering 4 mm balsa wood spheres
were attached above the middle of the iguana’s
pelvis. The pelvis was chosen to represent the center
of mass because it is an easily located landmark and
is near the estimated center of mass of iguanas.
Dorsal and lateral views of lizards running on the
track were simultaneously recorded using two
PhotronTM Fast Cam high-speed video cameras
operating at 125 Hz. Kwon CC was used to calibrate
the two camera views and compute DLT parameters
for reconstructing camera coordinates in three
dimensions. Video recordings were digitized using
Kwon 3D 3.0 and position data were smoothed using
QuickSAND’s MSE quintic spline algorithm (Walker
1998). Velocities and accelerations of the center of
mass were calculated by differentiating Quicksand’s
MSE quintic spline (Walker 1998).
Work and power
Ground reaction forces were measured using a
Kistler 9286A force-plate with signals acquired
using BiowareÕ software (Kistler). Force signals
were initially acquired at 125 Hz for gravid iguanas,
while force signals were collected at both 1000 Hz
and 125 Hz for recovered iguanas. As we could not
recollect data on gravid individuals, we tested for an
effect of low collection rate. Having found no
significant difference (see Results section), we
report only data collected at 1000 Hz for recovered
iguanas. Force signals collected at 1000 Hz were
filtered in Bioware using a second-order low-pass
Butterworth filter with a cutoff frequency of 50 Hz.
Force signals acquired at 125 Hz were filtered in
Bioware using a second-order low-pass Butterworth
filter with a cut-off frequency of 30 Hz. Video
recordings and force acquisition were synchronized
using an external trigger.
Force, work, and power estimates are of isolated
hind limbs, not taking the forelimbs into account.
Therefore, the estimates are not of all force and work
performed on the center of mass. However, the hind
limbs provide the majority of propulsive force in
running lizards (Aerts et al. 2003; Chen et al. 2006).
Work can be measured as changes in kinetic energy
(KE) during hind limb footfalls. Thus, KE
was obtained by integrating the forces in each
of three directions (fore-aft, mediolateral, and
vertical) with initial velocities (v1) of the center
of mass obtained from the video analysis and
final velocities (v2) obtained
from force data
work ¼ KE ¼ 1=2 m v22 v21 , where m ¼ mass).
Fore-aft and mediolateral forces contribute to kinetic
energy, while integration of vertical force contribute to
both kinetic and potential energy. Net work was
measured by summing work in all three directions.
Power (P) was calculated by numerical differentiation
of the change in kinetic energy with respect to time
(P ¼ KE/t, where t ¼ length of the time interval).
Hind limb extensor muscles constitute approximately 6% of body mass in the lizard species
Acanthodactylus boskianus (Curtin et al. 2005). We
measured total hind limb mass in three postgravid
iguanas, and obtained a similar figure of 6.2%. We
assumed that hind limb muscle-mass did not change
with reproductive condition, so we estimated the
hind limb mass for each individual based on
this figure and their recovered body mass.
Statistical analysis
We tested whether gravid iguanas vary in measures
of power, force, work, and step duration using
general linear models. We included acceleration as an
explanatory factor in these models because, although
there was no significant difference between accelerations of gravid and postgravid iguanas, there was
significant variation within groups. Also, the mean
difference between groups (over 1 m/s2) may be
biologically, if not statistically, significant (Table 1).
Thus, for each of the above dependent variables, we
tested models with the following independent variables: reproductive state (RS), acceleration (A), and
their interaction (RS A). We began with the full
model, but dropped the interaction if it was not
significant. The final models used in the analysis are
reported in Table 1, where we report both the raw
means and least-square means.
Gravid and postgravid iguanas did differ in step
velocity (Table 1). However, velocity had no
significant affect on work, power, or force differences
between the reproductive classes. Thus, it was not
included in the model for these variables. We also
tested for effects of velocity on acceleration and step
duration (Table 1). All statistical analyses were
performed in the SAS statistical language (SAS 1994).
Results
Differences in collection rate
The difference in collection rate for gravid iguanas
did not result in any significant error in force
measurement. Specifically, it resulted in a 3.2%
[9.0% standard deviation (SD)] underestimation
288
J. Scales and M. Butler
Table 1 Mass, performance variables, and work and power output of gravid (G) and post-gravid (PG) iguanas
(1)
(2)
(3)
Raw data means
(4)
(5)
(6)
(7)
GLM adjusted means
G
PG
G-PG
P
G
PG
Mass (kg)
1.80
1.37
0.43
0.040
–
–
Acceleration (m/s2)
3.59
4.85
1.26
0.173
3.53
4.97
Step velocity (m/s)
2.30
2.72
0.42
0.004
–
–
Total
90.12
40.85
49.27
0.006
94.83
30.65
Propulsive
52.03
30.93
21.10
0.052
55.56
Mediolateral
3.02
1.27
1.75
0.416
3.58
Vertical
35.07
8.65
26.42
0.001
(8)
(9)
(10)
G-PG
Model
F
–
(11)
P
0.040
RS,V
0.14
0.720
–
–
–
64.18
RS,A
17.65
0.003
23.29
32.27
RS,A
12.46
0.003
0.06
3.52
RS,A
2.79
0.115
35.69
7.31
28.38
RS,A
13.61
0.002
0.045
703.9
328.35
375.55
RS,A
9.5
0.007
1.44
Work (J/kg hindlimb)
Average power (w/kg hindlimb)
Total
672.89
395.53
277.36
Propulsive
393.89
314.90
78.98
0.383
417.15
264.5
152.65
RS,A
3.95
0.064
Mediolateral
19.47
12.52
6.94
0.506
23.43
3.93
19.50
RS,A
2.3
0.149
Vertical
265.33
85.17
180.16
50.001
269.76
75.57
194.19
RS,A
11.72
0.004
0.027
1228.27
551.96
676.31
RS,A
13.77
0.002
Peak power (w/kg hindlimb)
Total
1174.85
667.72
507.13
Propulsive
730.63
528.24
202.39
0.170
770.71
441.39
329.32
RS,A
8.1
0.017
Mediolateral
61.13
39.80
21.33
0.393
71.41
17.54
53.87
RS,A
3.48
0.081
Vertical
489.38
168.81
320.57
50.001
498.75
148.49
350.26
RS,A
13.52
0.002
Independent terms included in the general linear model (GLM) for each variable (9) are coded as: RS, reproductive state; A, acceleration; and V,
velocity, and RS A, interaction between reproductive state and acceleration. Dependent terms were those listed in row names. P-values (P) and
F-statistics (F) given refer to differences between reproductive state, either before (5) or after adjusting for other terms in the model (10,11).
in peak fore-aft force, an 11.3% (14.6% SD)
underestimation in peak mediolateral force, and a
1.3% (15.3% SD) underestimation of peak vertical
force. The difference in forces resulted in only 1.0%
(15.3% SD) underestimation in work, a 0.3%
(14.5% SD) overestimation of average powers, and
a 3.5% (8.7% SD) underestimation of peak
instantaneous powers.
Change in mass and work during a step
Gravid iguanas weighed significantly more than did
postgravid iguanas (Table 1). Individuals were, on
average, 51% heavier during gravid trials than
postgravid trials. Gravid iguanas produce 120%
more net work with their hind limbs than did
postgravid iguanas (209% greater if means are
adjusted for acceleration; Table 1, Fig. 1A).
Increases in propulsive and vertical work produce
the increase in network, with vertical work contributing more (Table 1, Fig. 1). Neither group
produces significant mediolateral work (Fig. 1D).
iguanas, respectively (numbers given in Table 3 are
averaged over individuals, whereas here we report
maximal values). Maximal values for peak powers
reached 1565 w/kg and 1344 w/kg for gravid and
postgravid iguanas, respectively. Gravid iguanas
produced 70% greater average (114% more if
means are adjusted for acceleration) and 76%
higher peak mass-specific total power (123% higher
if means are adjusted for acceleration) in the hind
limb than did postgravid iguanas (Table 1, Fig. 2).
Significant increases in the vertical direction are
the main components of power increase for both
average and total measures. Similar to net work,
gravid iguanas increase power (average and total
increased by about 200%, and over 230% if means
are adjusted for acceleration) in the vertical direction, more so than in the propulsive, although both
are significantly increased (Table 1, Fig. 2). Again,
mediolateral power is very small in both groups
(Table 1, Fig. 2).
Power production
Force production
Both gravid and postgravid iguanas produced
extremely high hind limb power output, with the
highest recorded average powers during a run at
1094 w/kg and 807 w/kg for gravid and postgravid
Gravid iguanas produced 100% greater total massspecific impulses than did postgravid iguanas (156%
greater after adjusting for acceleration differences;
Table 2, Fig. 3). Impulses increased in all three
Acceleration in gravid green iguanas
289
Fig. 1 Net work performed by the hind limbs (J/kg of hind limb mass) of gravid (black circles and dashed line) and postgravid
(open squares and solid line) iguanas during accelerations. Trend lines shown are least-squares regression performed on each
group independently. (A) Total, sum of all three directions of movement. (B) Propulsive, the direction of movement. (C) Mediolateral,
side-to-side movements. (D) Vertical, movement normal to the ground.
directions of motion (Table 2, Fig. 3). Gravid
iguanas, however, tended to increase mediolateral
impulse with acceleration more than did postgravid
iguanas (Table 2, Fig. 3).
The increased impulses in each direction can be
partially attributed to gravid iguanas producing
greater mass-specific peak forces in the hind limb
than did post-gravid iguanas for a given acceleration,
with a 23% increase in peak propulsive, 44% increase
in mediolateral, and 42% increase in vertical forces.
(Table 2, Figs. 3 and 4). The increase in impulses is
also driven by a 44% increase in step duration
(Table 2, Fig. 5).
Discussion
Work, power, and acceleration
The increase in mechanical power output by gravid
iguanas is very impressive considering that when they
are nongravid, females are already producing very
high mechanical power (Table 1). Compared to the
average and peak power outputs of other vertebrate
locomotor systems, post-gravid female iguanas produce very high power, but it is even higher when
gravid (Table 3). The increasing mass of females
during gestation places a large demand on their
musculoskeletal system during locomotion, and here
we find that gravid iguanas are able to compensate
for this increased load by greatly increasing vertical
force and power.
Interestingly, the increases in vertical power
approach, or exceed, 200%, which is much greater
than their 51% increase in mass. A super-isometric
increase is also observed in propulsive and vertical
work, and impulses in all directions. Naively, to
maintain the same sprint performance, one might
expect that a fractional increase in mass would
require the same fractional increase in force. The
‘‘extra’’ work, power, and force that we observed
may result from lack of coordination, difficulties in
maintaining stability, or other inefficiencies.
290
J. Scales and M. Butler
Fig. 2 Hind limb power production (w/kg of hind limb mass) by gravid (filled circles, dashed lines) and postgravid (open squares, solid
lines) iguanas during accelerations. Only peak powers are shown as both average and peak powers showed identical trends. See Fig. 1
legend for explanation of panels A–D.
Table 2 Force production and step durations of gravid and postgravid iguanas. See Table 1 for explanation of column/row names
(1)
(2)
(3)
Raw data means
G
(4)
(5)
(6)
(7)
GLM adjusted means
PG
G-PG
P
G
13.54
13.52
50.001
28.89
(8)
(9)
(10)
(11)
PG
G-PG
Model
F
P
11.27
17.62
RS,A
32.15
50.001
Impulse (N s/kg hindlimb)
Total
27.06
Propulsive
11.29
7.40
3.89
0.061
12.10
5.65
6.45
RS,A
16.49
50.001
Mediolateral
5.84
2.59
3.25
0.032
6.88
2.18
4.70
RS,A,RS A
5.77
0.014
Vertical
20.88
9.90
10.98
50.001
21.63
8.27
13.36
RS,A
22.62
50.001
128.33
29.61
0.158
165.66
111.6
54.06
RS,A
9.11
0.008
Peak forces (N/kg hindlimb)
Propulsive
157.94
Mediolateral
107.12
74.62
32.50
0.107
113.80
60.15
53.65
RS,A
5.49
0.032
Vertical
272.74
192.67
80.07
0.034
280.09
176.74
103.35
RS,A
7.51
0.015
0.13
0.09
0.04
0.008
0.13
0.09
0.04
RS,A,V
12.97
0.002
Step duration (s)
P-values (P) and F-statistics (F) given refer to differences between reproductive state, either before (5) or after adjusting for other terms in the
model (10,11).
Acceleration in gravid green iguanas
291
Fig. 3 Hind limb force production (N s/kg of hind limb mass) by gravid and postgravid iguanas during accelerations. Only impulses are
shown as impulses and peak forces for total, propulsive, and mediolateral directions showed identical trends. See Fig. 1 legend for
explanation of symbols and panels A, B, D. (C) Gravid iguanas tended to increase mediolateral impulse with acceleration while
postgravid iguanas did not resulting in higher forces at higher accelerations. The trends in peak mediolateral forces appeared similar to
those seen in impulse, but there was no significant difference in trends.
Fig. 4 Peak vertical force production (N/kg of hind limb mass) by
gravid (filled circles, dashed line) and postgravid (open squares,
solid line) iguanas during accelerations.
Fig. 5 Step durations of gravid (filled circles, dashed line) and
postgravid (open squares, solid line) iguanas during accelerations.
292
J. Scales and M. Butler
Table 3 Mechanical power outputs of several locomotor systems designed for power production
Muscle(s)
Activity
Average
(w/kg)
Power peak
(w/kg)
Power
Reference
Turkey Hindlimb extensors
Running
150
400
Roberts and Scales 2002
Acanthodactylus boskianus hindlimb extensors
Running
214
952
Curtin et al. 2005
Quail pectoralis
Flying
1120
Askew et al. 2001
Female iguana hindlimb
Running
396
668
This study
Gravid female iguana hindlimb
Running
673
1175
This study
Power during acceleration in sprint-running or flying (i.e., take-off). Female iguana hind limbs show very high average and peak power outputs
[iguana power measures (in bold) are means from this experiment].
Maintaining their acceleration while carrying a
heavy load is a remarkable locomotor accomplishment
performed by female iguanas. Two strategies could be
employed by gravid iguanas, in order to produce the
force necessary to maintain their acceleration: they
could apply higher force over the same amount of time
resulting in higher power output, or apply the same
amount of force over a longer period of time resulting
in a longer step duration. Gravid iguanas appear to
use both strategies. While gravid iguanas do increase
peak propulsive force (23% increase) and power
(25% increase in average and 38% increase in peak),
they do not fully compensate for their increased mass
in this manner. Therefore, they also produce force for a
longer period of time resulting in a 44% increase in
step duration, suggesting that acceleration in gravid
iguanas is force limited.
Also consistent with a force-limitation hypothesis
are the changes in peak forces. While gravid iguanas
increased peak vertical and mediolateral forces by
42% and 44%, respectively, peak propulsive force
only increased by 23% suggesting that perhaps they
could not increase peak propulsive forces further.
Additionally, Butler (in review) found that gravid
iguanas swing their legs faster than do recovered
iguanas. In fact, even by the third stride during
acceleration, gravid iguanas were swinging their hind
limbs 21% faster than did recovered iguanas. The
increase in swing speed would allow for longer force
application per distance traveled, without increasing
the duration of the step cycle. Therefore, for a given
distance traveled, gravid iguanas would have more
time for the force production required to accelerate
their mass, but would not suffer a reduction in
absolute performance. All these adjustments should
significantly increase energetic cost. Thus, gravid
iguanas are probably limited in the duration and
number of sprinting bouts.
As a result of sprawling posture, lizards must exert
more mediolateral force to maintain position of their
center of mass than do animals with more upright
postures. Here, we found that gravid iguanas
increased mediolateral force production. Chen et al.
(2006) found that ground reaction forces are likely
important for providing dynamic stability in running
lizards. Therefore, gravid iguanas may need to
produce more mediolateral force in order to
maintain the position and stability of their center
of mass while carrying a clutch, but should not
change mediolateral work or power (i.e., since they
are running in a straight line, positive and negative
work/power should sum to zero).
Given that recovered iguanas can produce such
high power, which is what we observed, how do they
increase power output when they are gravid? The
ability for increased power output may come from
the added mass of the clutch itself. In humans,
external loading has been shown to increase shortterm power output (Caiozzo and Kyle 1980; Kyle
and Caiozzo 1985). While these authors concluded
that optimal loading conditions must exist for
maximizing power output, they do not apply this
idea to sprinting. There is evidence, however, that
this concept applies to sprinting animals. McGowan
et al. (2006) found that guinea fowl were able to
maintain locomotor performance while bearing an
external load. This was partly achieved by increasing
muscle activation. In addition, the loading increased
the active stretching of the locomotor muscles.
Active stretching of muscles enhances force production, which in turn, can enhance power output.
Additionally, at high loads, stretch-induced power
enhancement of muscle may last for an extended
length of time (Cronin et al. 2001). Therefore, if
nongravid iguanas are suboptimally loaded for
maximum power output, the added mass of a
clutch may load the locomotor muscles in a
manner that prestretches them and enhances force
and power output over the duration of a step.
Locomotion, reproductive role, and ecological
dimorphism
Only females must contend with the problem of
locomotion while carrying a clutch. If this is a
293
Acceleration in gravid green iguanas
significant selective pressure, it may lead to
sexual dimorphism in relative limb and body
proportions. For example, accelerating with a
reproductive load probably increases stress and
strain on the musculoskeletal system of females.
However, female lizards commonly have shorter
limbs for a given body size than do males (Butler
and Losos 2002; Irschick et al. 2005; Schwarzkopf
2005). This sexual dimorphism may be advantageous
for accelerating with a load.
The relationship between limb length, posture,
and joint mechanics in lizards is complex. The
sprawling posture of lizards results in moment arms
at joints, even when the animal is at rest. Shorter
limbs would decrease moment arms, thereby reducing
joint moments. Also, during acceleration, the shorter
moment arm will result in greater force output.
Additionally, one way to effectively support an
increased mass effectively is to move the support
limbs more directly under the mass. While lizards
are capable of using a more upright posture,
this increases stresses to their limb bones because
of the details of their bone curvature (Blob
and Biewener 2001). Therefore, shorter limbs in a
sprawling animal will place the feet closer to the
center of mass, without adopting a more upright
posture. Smaller joint moments and lower bone
stresses may be especially important for gravid
animals, who need to increase propulsive force to
counteract their increased load while remaining within
safety factors for their bones and joints. Thus, the
limb morphology of females may be constrained by
reproductive role.
Relative limb length commonly reflects performance capabilities in lizards (Losos and Sinervo
1989; Losos 1990; Garland and Losos 1994; Bonine
and Garland 1999 but see Vanhooydonck et al. 2006
for a study on limb muscles). Since the sexes differ in
limb morphology and sometimes performance,
biomechanical constraints may be responsible for
this broad suite of sexual differences (Snell et al.
1988; Cullum 1998; Miles et al. 2001; Lailvaux et al.
2003; Irschick et al. 2005). Many studies have
examined the influence of reproductive role on the
evolution of performance and morphology, especially
with regard to male behaviors (Garland et al. 1990;
Perry et al. 2004; Husak et al. 2006). However, the
mechanistic basis for these performance differences
has been little studied. A research program integrating biomechanics, ecological pressures, and lifehistory changes is needed to understand the
significance of sexual dimorphism in form and
function.
Acknowledgments
The authors thank B. England, A. Fuller, K. Root,
S. Tucker, M. Moses, C. Ross, T. Ives, S. Stanley, and
J. Vandiver for assistance in care and running trials
of iguanas. We thank D. Creer, K. Krysko, K. Enge,
E. Lynk, J. Higa, R. Higa, and CrandonPark Zoo and
Fairchild Tropical Gardens for help in animal
collection. Helpful comments from Tom Roberts
and Dave Carrier regarding data analysis and
comments from two anonymous reviewers improved
this manuscript.
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