A biomechanical analysis of intra- and interspecific scaling of jumping and morphology in Caribbean Anolis lizards
1 Universidad de los Andes, Bogota, Colombia
2 University of Antwerp, Dept Biology, Universiteitsplein 1, B-2610 Wilrijk,
Antwerpen, Belgium
3 Tulane University, Dept Ecology & Evolutionary Biology, 310 Dinwiddie
Hall,New Orleans, LA 70118, USA
* Author for correspondence (e-mail: aherrel{at}uia.ua.ac.be)
Accepted 25 April 2003
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Summary |
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Key words: geometric scaling model, jumping, hindlimb, acceleration capacity, morphology, lizard, Anolis, biomechanics, force plate technology
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Introduction |
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Given the importance of size on animal function, several authors have
proposed models that predict the effects of size on the physiology and
function of animal movement (e.g. Hill,
1950; McMahon,
1984
). If these predictive models are valid, they could shed light
on ontogenetic changes in ecology or behaviour, as well as variation in animal
function among species. Although universal quarter power scaling laws have
been proposed in the past decade (e.g.
Brown et al., 2000
), these
scaling laws appear unable to explain the observed scaling patterns of
functional data. Indeed, to date, no single general scaling model can explain
the range of observed scaling patterns in morphology, function and behaviour
(Biewener, 2000
). However,
given specific conditions and assumptions, certain models may still apply.
Geometric scaling models (i.e. models based on the assumption of isometric
growth) might be such an example. Because many ectothermic vertebrates tend to
scale geometrically for most characters, they provide an excellent study
system for testing the predictions of these models
(Wainwright and Richard, 1995
;
Meyers et al., 2002
). Hill
(1950
) proposed a scaling
model for geometric systems based on the premise that velocity does not change
with increases in body size (Hill,
1950
). However, little experimental support has been obtained for
this model, even when using ectothermic study organisms
(Reilly, 1995
;
Richard and Wainwright, 1995
;
Wainwright and Richard, 1995
;
Wainwright and Shaw, 1999
;
Nauen and Shadwick, 1999
,
2001
;
Hernandez, 2000
;
Quillin, 2000
;
Wilson et al., 2000
;
Meyers et al., 2002
). One
notable exception is a study investigating the scaling of toad tongue
kinematics (O'Reilly et al.,
1993
). Still, most experimental studies tend to support an
alternative model that also assumes geometric scaling but differs in the
assumption that velocity increases linearly with increases in linear
dimensions (Richard and Wainwright,
1995
).
Lizards are good models for scaling studies because much of their growth is
geometric (e.g. Meyers et al.,
2002). Moreover, lizards in general, and Anolis lizards
in particular, show substantial variation in adult body size. For example,
adult body size ranges from 0.5 g (Anolis occultus;
Losos, 1990a
) to almost 100 g
(e.g. Anolis equestris). Furthermore, within species, body size
increases dramatically from newly hatched lizards to adults, typically by more
than one order of magnitude (or a more than threefold increase in hindlimb
length). As lizards typically do not display parental care, they need to
function from the day they hatch, and thus the selection for high performance
at all sizes will probably be strong
(Carrier, 1996
;
Irschick, 2000
;
Irschick et al., 2000
).
Locomotion is of particular interest in scaling studies because of its
obvious ecological relevance (e.g. Van
Damme and Vanhooydonck, 2001;
Irschick and Garland, 2001
).
Moreover, as the biomechanics of locomotion in general, and jumping in
particular, are fairly simple and reasonably well understood
(Alexander, 2000
;
Harris and Steudel, 2002
), one
can generate specific predictions concerning the effects of size on the
dynamics (i.e. displacements, forces, velocities and accelerations) and
performance aspects (i.e. distance, jump angle and time) of jumping (see also
Table 1;
Hernandez, 2000
). As
Anolis lizards are highly arboreal and jump in a variety of
behavioural contexts (e.g. escape and feeding;
Moermond, 1979
; Losos,
1990a
,b
;
Irschick and Losos, 1998
), the
study of jumping behaviour in anoles is relevant. Another advantage of
studying jumping behaviour is that the forces generated during jumping are
easily and accurately measured using force plate technologies
(Wilson et al., 2000
). The
accurate measurement of forces is of particular interest, as previous studies
have found large differences in the scaling of forces with body size
(Wilson et al., 2000
;
Nauen and Shadwick, 2001
;
Harris and Steudel, 2002
;
Meyers et al., 2002
).
|
In the present study, we test whether hindlimb dimensions and the dynamics
of jumping in Anolis lizards scale as predicted by geometric growth
models (see Table 1;
Hill, 1950;
Richard and Wainwright, 1995
).
To investigate this issue, we will examine intraspecific scaling patterns for
three species of Anolis lizard that differ in body size and ecology.
Additionally, we investigate whether the evolution of body size in 12 West
Indian Anolis species is accompanied by proportional increases in
limb dimensions and jumping dynamics as predicted by two theoretical models of
geometric growth (Table 1).
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Materials and methods |
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Jumping data
All animals were induced to jump in 3-5 jumping sessions, each on different
days. At least three good trials were obtained per individual in each session.
Before and in-between each jumping trial, animals were placed in an incubator
set at 32°C (28°C for A. gundlachi; see Hertz,
1981,
1992
;
Huey, 1983
;
Huey and Webster, 1976
) for at
least 1 h. This temperature is close to the preferred field temperatures of
these 12 anoles (see references above; D. J. Irschick, unpublished data).
During jumping trials, animals were removed from the incubator, placed on the
force plate and induced to jump to a horizontal branch positioned at the level
of the force plate and placed just outside of the presumed maximal reach of
each individual. Maximal efforts were further elicited by startling the
animals using a sudden clapping of hands or a slight tap on the base of the
tail (only for larger individuals). We only included jumps in which all four
feet were squarely on the force plate and for which the tap on the tail did
not coincide with the timing of the jump. We only included the maximal jump
(longest distance) for each individual obtained in all trials and sessions
combined as our estimate of maximum jumping performance.
Jumping in Anolis lizards consisted of a preparatory phase, the
actual take-off phase, a flight phase and the landing (see
Bels and Theys, 1989). The
preparatory phase involves the positioning of the feet anterior to the pelvic
girdle, just posterior to, or at the level of, the hands. During this phase,
the lizards also align their bodies with the jump direction. The actual
take-off phase involves the rapid extension of the hindlimbs from a standstill
and the stretching of the vertebral column (see also
Bels and Theys, 1989
). The
take-off phase ends when the toes no longer touch the force plate. Only the
forces exerted during the take-off phase were analysed here.
A custom-designed force plate (30 cmx18 cmx1 cm, length x
width x height) was used to measure the three-dimensional ground
reaction forces during jumping (see
Heglund, 1981). The output of
the strain gauges was sent to a 12-bridge, 8-channel amplifier (K & N
Scientific, Greenfield, MA, USA) and subsequently AD converted at 10
kHz (Instrunet, model 100B). Digital traces were read into a G4 Macintosh
computer using Superscope (GW Instruments, Somerville, MA, USA). Force traces
were smoothed using a low-pass filter before further analysis. First, body
mass was subtracted from the forces in the vertical direction (Z).
Next, the resultant force vector was calculated using the vector sum of the
individual X-, Y- and Z-forces. The acceleration of
the centre of mass was obtained by dividing the resultant ground reaction
force (3-D) by the body mass of the animal. Numerical integration of the
acceleration profile yielded the instantaneous velocity of the centre of mass.
As the animals started the jump from a standstill (i.e. no movement or dip in
the force trace was noted prior to rapid extension of the hindlimbs in all
species examined), the integration constant for the velocity integration was
set to zero. Instantaneous mass-specific power was calculated by multiplying
the instantaneous velocity and acceleration profiles. The displacement of the
centre of mass was obtained by numerical integration of the instantaneous
velocity during take-off. The angle of take-off was determined using the
horizontal (X+Y) and vertical (Z) ground reaction
forces during jumping.
From these traces, we extracted the peak acceleration during take-off, the
velocity at take-off (i.e. the terminal velocity at the end of the take-off
phase), the peak power during take-off, the time to peak power, the time to
peak acceleration, the displacement of the centre of mass during take-off
(further referred to as contact time distance) and the duration of the entire
take-off phase. Using the take-off angle (), the take-off velocity
(Vt) and the horizontal displacement of the centre of mass
during take-off (Dh), we calculated the horizontal jump
distance as
D=Dh+Da+Df,
where Df is the horizontal distance travelled from
take-off height back to resting height, and Da is the
distance travelled during the ballistic phase of jumping
[
;
see Marsh and John-Adler,
1994
]. The output of the force plate (i.e. calculations of
acceleration, velocity, take-off angle and jump distance) was validated using
high-speed video recordings (250 frames s-1) of maximal jumps for
seven individuals of A. valencienni (see
Wilson et al., 2000
).
Morphometrics
Immediately after measuring their jumping performance, all animals were
weighed (to the nearest 0.0001 g using an M-220 electronic balance; Denver
Instruments, Denver, CO, USA) and measured (to the nearest 0.01 mm using
digital callipers; Mitutoyo, Sakato, Japan). For each individual, the
following morphological variables were measured on the right side (from a
dorsal perspective): snout-vent length, forelimb length (length of the entire,
fully extended forelimb, including the length of the longest toe), hindlimb
length (length of the entire, fully extended hindlimb, including the length of
the longest toe), femur length (from the articulation of the femur with the
hip to the end of the femur), tibia length (from the joint with the femur to
the articulation with the metatarsi), metatarsus length (from the articulation
with the tibia to the base of the longest toe) and the length of the longest
toe (see also Losos, 1990a).
Additionally, the length of the tail, including regenerated parts, was
measured from vent to tail tip. All measurements were taken externally. To
increase our sample size, morphometric data were collected for an additional
17 A. sagrei and 12 A. equestris using preserved
specimens.
Analyses
All data were analysed using reduced major axis regressions. Deviations of
predicted slopes were considered significant if the predicted slope fell
outside the 95% confidence interval of the reduced major axis regression
slope. To investigate whether limb proportions in each species increased
isometrically, we regressed the log10-transformed limb proportions
against the log10-transformed snout-vent length for each
individual. We did not use body mass, as it was subject to substantial
day-to-day variation in small animals. The scaling of jumping performance was
investigated by regressing the log10-transformed jumping
performance data against the log10-transformed hindlimb length for
all individuals. Hindlimb length was chosen as the independent variable in
these regressions as (1) it is functionally related to the performance
variables investigated and (2) to allow a comparison of data across species,
given that hindlimb length scaled with significant negative allometry relative
to snoutvent length in A. carolinensis only. All regression analyses
were performed using SPSS (version 10; Statsoft Inc., Tulsa, OK, USA).
To investigate the interspecific scaling of limb dimensions and jumping
performance, we gathered data on a wide range of species differing in body
size (Fig. 1). However, as
species are not independent data points but are related evolutionarily
(Felsenstein, 1985;
Harvey and Pagel, 1991
), we
used independent contrast analysis to investigate the interspecific scaling of
morphological and functional data (see also
Blob, 2000
;
Van Damme and Vanhooydonck,
2001
). Only data for adults of all species (i.e. reproductively
active animals) were included in the interspecific analysis. We used the PDAP
package (Garland et al., 1999
)
to calculate the independent contrasts of all variables of interest using the
log10-transformed species means of all variables. To do so, we
constructed a tree depicting the phylogenetic relationships among the species
included in our analysis based on literature data (see Jackman et al.,
1999
,
2002
;
Fig. 1). As no data on
divergence times are available for all the species in the analysis, all branch
lengths were set to unity. To check that constant branch lengths were adequate
for all traits, we inspected the diagnostic graphs in the pdtree program
(Garland et al., 1999
). To
calculate the slopes of the regressions, the standardised contrasts of all
morphometric variables were regressed against the standardised contrasts of
snout-vent length, and the standardised contrasts of jumping performance were
regressed against the standardised contrasts of hindlimb length, using a
reduced major axis regression analysis forced through zero
(Garland et al., 1992
).
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Results |
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Ontogenetic scaling of jumping performance
Although the different species showed differences in the scaling of
functional variables relative to body size
(Table 3), overall trends were
similar (see Fig. 3;
Table 3). On average, our
experimental data supported the Richard and Wainwright
(1995) model more closely than
the Hill (1950
) model (see
Tables 1,
3). Interestingly, the data for
both acceleration capacity and peak power showed different trends when
comparing data for A. carolinensis with the data for the other two
species. Whereas peak acceleration capacity and peak power scaled
significantly with hindlimb length in A. carolinensis, no significant
correlations could be observed in the other two species. Moreover, peak power
scaled with significant positive allometry in A. carolinensis
(Table 3). Peak acceleration
scaled according to the Richard and Wainwright
(1995
) model (see Tables
1,
3). The scaling of peak force
(all species) is predicted by neither of the two models. Peak force scaled
with significant positive allometry relative to hindlimb length in all three
species.
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Interspecific scaling of morphology and jumping performance
The interspecific scaling of hindlimb dimensions, tail length and body mass
did not show any significant deviations from the predicted values. Thus,
across species, evolutionary increases in snout-vent length change in concert
with evolutionary increases in limb, body and tail dimensions, as predicted
for geometrically growing systems (Table
4; Fig. 4).
Take-off angle did not scale with hindlimb length, as predicted by both models
(Table 1). Both jump distance
and peak force production also scaled in accordance with model predictions
(i.e. slopes not significantly different from 1 and 2, respectively;
Table 4). The other functional
variables all scaled with slopes intermediate between those predicted by the
Hill (1950) or Richard and
Wainwright (1995
) models (see
Tables 1,
4).
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Discussion |
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Predicting jumping dynamics from hindlimb length
Given its obvious and direct relevance to jumping
(Losos, 1990a;
Wilson et al., 2000
;
Harris and Steudel, 2002
), we
used hindlimb length as a size indicator to investigate the scaling of jumping
dynamics. Hindlimb length is often considered a good indicator of jumping and
running performance and is often used in ecomorphological and evolutionary
studies as a proxy for locomotor capacity (e.g. Losos,
1990a
,c
;
Garland and Losos, 1994
;
Vanhooydonck and Van Damme,
1999
; Melville and Swain,
2000
). However, within the species of Anolis studied
here, the dynamics of jumping were generally poorly predicted by scaling
models based on limb length (i.e. compare
Table 1 with
Table 3). Velocity increased
with hindlimb length as predicted by Richard and Wainwright
(1995
) in both A.
equestris and A. sagrei. However, in A. carolinensis,
velocity increased with significant negative allometry (slope less than 1; see
Table 3). Jump distance again
increased with hindlimb length, as predicted, in A. sagrei and A.
equestris but scaled with positive allometry in A. carolinensis
(see Table 3). Given that
velocity scaled with negative allometry relative to hindlimb length in A.
carolinensis and that jump distance (scaling with positive allometry
relative to hindlimb length) is proportional to take-off velocity and take-off
angle (invariant with hindlimb length), this suggests that variables other
than limb length affect take-off velocity in this species. Across species,
both take-off velocity and jump distance increased significantly with hindlimb
length. However, whereas take-off velocity scaled with significant negative
allometry, jump distance increased isometrically with hindlimb length. Here
too, hindlimb length does not seem to be the sole predictor of take-off
velocity.
Scaling of jumping dynamics
The maximal forces generated during take-off scaled with significant
positive allometry for all species. However, interspecifically, peak force
scaled as predicted by both scaling models (see Tables
1,
4). The deviations of the
ontogenetic scaling of forces from model predictions indicate that as animals
grow, muscle physiological cross section increases disproportionately with
hindlimb length. This could, in turn, be the result of disproportionate
increases in muscle mass with size and/or could be the result of changes in
muscle architecture throughout ontogeny. The existing data for the
interspecific scaling of leg muscles in mammals indicate that allometries in
the scaling of fibre lengths, muscle masses and moment arms can potentially
all occur (Castiella and Casinos,
1990). Other parameters that might be important in determining the
scaling of force output are the pennation angle of the muscle
(Gans and De Vree, 1987
) and
fibre type (Peters, 1989
). To
our knowledge, no data are available on the intraspecific scaling of
functional properties of muscle in ectotherms (but see
Zimmerman and Lowery, 1999
).
Given that deviations from model predictions for scaling of forces are common
(Quillin, 1999
;
Herrel et al., 1999
;
Nauen and Shadwick, 2001
;
Meyers et al., 2002
), these
kinds of data would be especially useful.
As a consequence of the scaling of forces and body mass versus
hindlimb length (see Tables 2,
3), maximal acceleration
capacity increased significantly with hindlimb length in A.
carolinensis (force increasing proportionally to body mass) but did not
change with `size' for the other two species. Despite the fact that body mass
increased disproportionately with length in A. sagrei
(Table 2) and that increases in
force are not as dramatic in A. equestris when compared with the two
other species (Table 3), we
still would have expected a significant positive relationship between limb
length and acceleration capacity with a slope of approximately 1, as predicted
by the Richard and Wainwright
(1995) model. Whereas we
observed a slope of approximately 1 in A. sagrei (not significant,
however), the regression of hindlimb length versus acceleration
capacity was negative in A. equestris (see
Table 3; Fig. 3). Clearly, more
experimental data on jumping in A. sagrei and A.
equestris are needed to determine whether the absence of a correlation
between hindlimb length and acceleration is a real phenomenon or simply a
sampling artefact (note the broad confidence limits in
Table 3 and spread of the data
in Fig. 3).
Size and the evolution of jumping capacity in Anolis lizards
Across species, we also did not detect a significant relationship between
maximal acceleration capacity and size. Inspection of the relationship between
acceleration and hindlimb length across species
(Fig. 4) suggests that the
absence of a correlation is largely driven by the inclusion of two large
species in the analysis (i.e. large contrast in hindlimb length but small
contrast in acceleration capacity between A. garmani and A.
equestris and their respective sister nodes/taxa). Indeed, when rerunning
the independent contrast analysis without the two large species (A.
equestris and A. garmani), we obtain a highly significant
positive relationship with a slope not significantly different from 1
(r=0.83, P<0.01, N=10, slope=0.72, confidence
limits=0.3-1.12). Why is there this disproportionate scaling of force to body
mass in small versus big species? The data gathered here indicate
that there might be a size limit above which a positive allometric scaling of
limb muscle force is no longer possible or, alternatively, no longer required.
Along these lines, two explanations are possible. First, there is some
mechanical limit to the absolute amount of force that can be exerted by the
limbs, which in turn might be driven by the scaling of bone or tendon
strength. Given that forces scale with length to the fourth power (in the two
smaller species), the stresses exerted on the bones and tendons will become
disproportionately large if bone or tendon surface area scales geometrically
(i.e. as length to the second power). Consequently, larger animals will be
operating at lower safety factors (see also
Biewener, 2000), which may
limit the scaling of force output of the system. Alternatively, there might be
a lack of selective pressure for disproportionately strong muscles in large
lizards. Because large animals have absolutely long limbs, they are capable of
jumping long distances in nature, and increasing jumping performance even more
may not be ecologically relevant (but see
Van Damme and Van Dooren,
1999
). On the other hand, large anoles might also be big enough
such that alternative anti-predator strategies become feasible. Indeed, large
Anolis lizards such as A. equestris or A. garmani
often attempt to bite with their powerful jaws when confronted with (human)
predators (A. Herrel, personal observation).
A similar pattern was observed for the scaling of peak mass-specific power. Whereas a significant increase with hindlimb length was observed for A. carolinensis, mass-specific power output did not scale with hindlimb length in the other two species. Again, low sample sizes for A. equestris and A. sagrei do not allow us to speculate whether these differences are real or not. Interestingly, also across species, mass-specific power output did not scale with hindlimb length. Here too, the absence of a relationship seems to be driven by the inclusion of the two large species in our analysis. Given that take-off velocity increases with hindlimb length across all species, this suggests that force production (and thus acceleration capacity) is limited in the largest species.
Interestingly, Wilson et al.
(2000) found similar results
for the scaling of jumping in frogs using methods comparable to ours. Whereas
across small sizes of frogs (metamorphs up to 1 g), forces, velocities and
accelerations scaled as observed for A. carolinensis (strong positive
relationships with size), the data for the larger post metamorphs corresponded
more closely to the scaling patterns observed for the largest species in our
analysis. Wilson et al. (2000
)
suggested that these trends could be explained by relaxed selection for
jumping performance in larger animals. However, whereas in large frogs jump
distance was invariant across different body sizes, in the larger lizards
acceleration capacity and power output did not change with body size (see
Fig. 3). If length or mass
independence is indeed the criterion to determine which performance parameters
are critical (Emerson, 1978
)
then this indicates differences in selective pressures for frogs and lizards.
Whereas for some frogs (Wilson et al.,
2000
) jump distance seems to be the critical variable, for the
large lizards studied here, as well as for the frogs studied by Emerson
(1978
), acceleration capacity,
and thus quickness of movement, seems to be more important. Also, across
species, acceleration capacity and power output are invariant of hindlimb
length, indicating that acceleration capacity (rather than jump distance)
might be the key aspect of jumping, driving the evolution of jumping
performance in Anolis lizards.
In summary, our data indicate that scaling laws cannot be applied
universally to predict changes in function with size, even when considering
closely related species that grow according to model assumptions. Whereas no
universal laws seem to apply, deviations from general laws or predictions seem
to be common (see also Biewener,
2000). However, once the scaling of certain key functional aspects
(e.g. velocity and forces) has been derived experimentally, other functional
parameters can be predicted. Our data, together with data from previous
studies, suggest that natural selection may have driven some aspects of the
evolution of jumping among anole species of varying sizes, but much variation
remains to be explained (Tyler-Bonner and
Horn, 2000
; Alexander,
2000
). Further studies investigating the limits on scaling of
forces, muscle architecture and geometry and muscle contraction
characteristics might prove to be especially insightful in explaining the
differential scaling of force output across different body sizes (see
Wilson et al., 2000
).
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Acknowledgments |
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References |
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![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Alexander, R. McN. (2000). Hovering and jumping: contrasting problems in scaling. In Scaling in Biology (ed. J. H. Brown and G. B. West), pp.37 -50. Oxford: Oxford University Press.
Bels, V. L. and Theys, J.-P. (1989). Mechanical analysis of the hind limb of Anolis carolinensis (Reptilia: Iguanidae) in jumping. In Trends in Vertebrate Morphology (ed. H. Splechtna and H. Hilgers), pp.608 -611. Stuttgart: Gustav Fischer Verlag.
Biewener, A. A. (2000). Scaling of terrestrial support: differing solutions to mechanical constraints of size. Scaling in Biology (ed. J. H. Brown and G. B. West), pp. 51-66. Oxford: Oxford University Press.
Blob, R. W. (2000). Interspecific scaling of the hindlimb skeleton in lizards, crocodilians, felids and canids: does limb bone shape correlate with limb posture. J. Zool. Lond. 250,507 -531.
Brown, J. H. and West, G. B. (2000). Scaling in Biology. Oxford: Oxford University Press.
Brown, J. H., West, G. B. and Enquist, B. J. (2000). Scaling in biology: patterns and processes, causes and consequences. In Scaling in Biology (ed. J. H. Brown and G. B. West), pp. 1-24. Oxford: Oxford University Press.
Carrier, D. R. (1996). Ontogenetic limits on locomotor performance. Physiol. Zool. 69,467 -488.
Castiella, M. J. and Casinos, A. (1990). Allometry of leg muscles in insectivores and rodents. Ann. Sci. Nat. Zool. Paris Ser. 13e 11,165 -178.
Emerson, S. B. (1978). Allometry and jumping in frogs: helping the twain to meet. Evolution 32,551 -564.
Felsenstein, J. (1985). Phylogenies and the comparative method. Am. Nat. 125, 1-15.[CrossRef]
Gans, C. and De Vree, F. (1987). Functional bases of fiber length and angulation in muscle. J. Morph. 192,63 -85.[Medline]
Garland, T., Jr and Losos, J. B. (1994). Ecological morphology of locomotor performance in Squamate reptiles. In Ecological Morphology: Integrative Organismal Biology (ed. P.C. Wainwright and S. M. Reilly), pp. 240-302. Chicago: University of Chicago Press.
Garland, T., Jr., Harvey, P. H. and Ives, A. R. (1992). Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst. Biol. 41, 18-32.
Garland, T., Jr., Midford, P. E. and Ives, A. R. (1999). An introduction to phylogenetically based statistical methods, with a new method for confidence intervals on ancestral states. Am. Zool. 39,374 -388.
Harris, M. A. and Steudel, K. (2002). The relationship between maximum jumping performance and hindlimb morphology/physiology in domestic cats (Felis silvestris catus). J. Exp. Biol. 205,3877 -3889.[Medline]
Harvey, P. H. and Pagel, M. D. (1991). The Comparative Method in Evolutionary Biology. New York: Oxford University Press.
Heglund, N. C. (1981). A simple design for a force-plate to measure ground reaction forces. J. Exp. Biol. 93,333 -338.
Hernandez, L. P. (2000). Intraspecific scaling
of feeding mechanics in an ontogenetic series of zebrafish, Danio rerio.J. Exp. Biol. 203,3033
-3043.
Herrel, A., Spithoven, L., Van Damme, R. and De Vree, F. (1999). Sexual dimorphism of head size in Gallotia galloti: testing the niche divergence hypothesis by functional analysis. Funct. Ecol. 13,289 -297.[CrossRef]
Hertz, P. E. (1981). Adaptation to altitude in two West Indian anoles (Reptilia: Iguanidae): field thermal biology and physiological ecology. J. Zool. Lond. 195, 25-37.
Hertz, P. E. (1992). Temperature regulation in Puerto Rican Anolis lizards: A field test using null hypotheses. Ecology 73,1405 -1417.
Hill, A. V. (1950). The dimensions of animals and their muscular dynamics. Sci. Prog. 38,209 -230.
Huey, R. B. (1983). Natural variation in body temperature and physiological performance in a lizard (Anolis cristatellus). In Advances in Herpetology and Evolutionary Biology: Essays in Honor of Ernest E. Williams (ed. A. G. J. Rhodin and K. I. Miyata), pp. 484-490. Cambridge: Museum of Comparative Zoology, Harvard University.
Huey, R. B. and Webster, T. P. (1976). Thermal biology of Anolis lizards in a complex fauna: the Cristatellus group on Puerto Rico. Ecology 57,985 -994.
Irschick, D. J. (2000). Effects of behaviour and ontogeny on the locomotor performance of a West Indian lizard, Anolis lineatopus. Funct. Ecol. 14,438 -444.[CrossRef]
Irschick, D. J. and Losos, J. B. (1998). A comparative analysis of the ecological of maximal locomotor performance in Caribbean Anolis lizards. Evolution 52,219 -226.
Irschick, D. J. and Jayne, B. C. (2000). Size
matters: ontogenetic differences in the three-dimensional kinematics of
steady-speed locomotion in the lizard Dipsosaurus dorsalis. J. Exp.
Biol. 203,2133
-2148.
Irschick, D. J. and Garland, T., Jr (2001). Integrating function and ecology in studies of adaptation: studies of locomotor capacity as a model system. Annu. Rev. Ecol. Syst. 32,367 -396.[CrossRef]
Irschick, D. J., Macrini, T. E., Koruba, S. and Forman, J. (2000). Ontogenetic differences in morphology, habitat use, behavior and sprinting capacity in two West Indian Anolis lizards. J. Herpetol. 34,444 -451.
Jackman, T. R., Larson, A., de Queiroz, K. and Losos, J. B. (1999). Phylogenetic relationships and tempo of early diversification in Anolis lizards. Syst. Biol. 48,254 -285.[CrossRef]
Jackman, T. R., Irschick, D. J., de Queiroz, K., Losos, J. B. and Larson, A. (2002). Molecular phylogenetic perspective on evolution of lizards of the Anolis grahami series. J. Exp. Zool. 294,1 -16.[CrossRef][Medline]
Losos, J. B. (1990a). Ecomorphology, performance capability and scaling of West Indian Anolis lizards: an evolutionary analysis. Ecol. Monogr. 60,369 -388.
Losos, J. B. (1990b). Concordant evolution of locomotor behavior, display rate and morphology in Anolis lizards. Anim. Behav. 39,879 -890.
Losos, J. B. (1990c). The evolution of form and function: morphology and locomotor performance in West Indian Anolis lizards. Evolution 44,1189 -1203.
Marsh, R. L. and John-Adler, H. B. (1994).
Jumping performance of hylid frogs measured with high-speed cine film.
J. Exp. Biol. 188,131
-141.
McMahon, T. A. (1984). Muscles, reflexes and locomotion. Princeton: Princeton University Press.
Melville, J. and Swain, R. (2000). Evolutionary relationships between morphology, performance and habitat openness in the lizard genus Niveoscincus (Scincidae: Lygosominae). Biol. J. Linn. Soc. 70,667 -683.[CrossRef]
Meyers, J. J., Herrel, A. and Birch, J. (2002). Scaling of morphology, bite force and feeding kinematics in an Iguanian and a scleroglossan lizard. In Topics in Functional and Ecological Vertebrate Morphology (ed. P. Aerts, K. D'Aout, A. Herrel and R. Van Damme), pp. 47-62. Maastricht: Shaker Publishing.
Moermond, T. C. (1979). Prey attack behavior of Anolis lizards. Z. Tierpsychol. 56,128 -136.
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. J. Exp.
Biol. 202,3181
-3193.
Nauen, J. C. and Shadwick, R. E. (2001). The
dynamics and scaling of force production during the tail-flip escape response
of the California spiny lobster Panulirus interruptus. J. Exp.
Biol. 204,1817
-1830.
O'Reilly, J. C., Lindstedt, S. L. and Nishikawa, K. C. (1993). The scaling of feeding kinematics in toads (Anura: Bufonidae). Am. Zool. 33, 147.
Pedley, T. J. (1977). Scale Effects in Animal Locomotion. New York: Academic Press.
Peters, S. E. (1989). Structure and function in vertebrate skeletal muscle. Am. Zool. 29,221 -234.
Quillin, K. J. (1999). Kinematic scaling of
locomotion by hydrostatic animals: ontogeny of peristaltic crawling by the
earthworm Lumbricus terrestris. J. Exp. Biol.
202,661
-674.
Quillin, K. J. (2000). Ontogenetic scaling of
burrowing forces in the earthworm Lumbricus terrestris. J. Exp.
Biol. 203,2757
-2770.
Reilly, S. M. (1995). The ontogeny of aquatic feeding behavior in Salamandra salamandra: stereotypy and isometry in feeding kinematics. J. Exp. Biol. 198,701 -708.[Medline]
Richard, B. A. and Wainwright, P. C. (1995). Scaling of the feeding mechanism of large mouth bass (Micropterus salmoides): kinematics of prey capture. J. Exp. Biol. 198,419 -433.[Medline]
Schmid, P. E., Tokeshi, M. and Schmid-Araya, J. M. (2002). Scaling in stream communities. Proc. R. Soc. Lond. B. Biol. Sci. 269,2587 -2594.[CrossRef][Medline]
Schmidt-Nielsen, K. (1984). Scaling: Why is Animal Size so Important? Cambridge: Cambridge University Press.
Tyler-Bonner, J. and Horn, H. S. (2000). Allometry and natural selection. In Scaling in Biology (ed. J. H. Brown and G. B. West), pp. 25-35. Oxford: Oxford University Press.
Van Damme, R. and Van Dooren, T. J. M. (1999). Absolute versus per unit body length speed of prey as an estimator of vulnerability to predation. Anim. Behav. 57,347 -352.[CrossRef][Medline]
Van Damme, R. and Vanhooydonck, B. (2001). Origins of interspecific variation in lizard sprint capacity. Funct. Ecol. 15,186 -202.[CrossRef]
Vanhooydonck, B. and Van Damme, R. (1999). Evolutionary relationships between body shape and habitat use in lacertid lizards. Evol. Ecol. Res. 1, 785-805.
Wainwright, P. C. and Richard, B. A. (1995). Scaling the feeding mechanism of largemouth bass (Micropterus salmoides): motor pattern. J. Exp. Biol. 198,1161 -1171.[Medline]
Wainwright, P. C. and Shaw, S. S. (1999).
Morphological basis of kinematic diversity in feeding sunfishes. J.
Exp. Biol. 202,3101
-3110.
Wilson, R. S., Franklin, C. E. and James, R. S.
(2000). Allometric scaling of jumping performance in the striped
marsh frog Limnodynastes peronii. J. Exp. Biol.
203,1937
-1946.
Zimmerman, A. M. and Lowery, M. S. (1999). Hyperplastic development and hypertrophic growth of muscle fibers in the white seabass (Atractoscion nobilis). J. Exp. Zool. 284,299 -308.[CrossRef][Medline]