The relationship between maximum jumping performance and hind limb morphology/physiology in domestic cats (Felis silvestris catus)
1 Biology Core Curriculum, University of Wisconsin-Madison, 307 Noland Hall,
250 N. Mills Street, Madison, WI 53706, USA
2 Department of Zoology, University of Wisconsin-Madison, Birge Hall, 430
Lincoln Drive, Madison, WI 53706, USA
* Author for correspondence (e-mail: maharris{at}facstaff.wisc.edu)
Accepted 23 September 2002
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Summary |
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Key words: takeoff velocity, muscle, morphology, physiology, formfunction, locomotion, jumping, cat, Felis silvestris catus
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Introduction |
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Relationships between morphology and locomotor performance
Although theoretical expectations about the relationship between limb
design and locomotor performance have been available for many years (e.g.
Hall-Craggs, 1965; Alexander,
1968
,
1977
;
Gambaryan, 1974
;
Bennet-Clark, 1977
;
Alexander and Jayes, 1983
;
Gabriel, 1984
;
Hildebrand, 1985
), only
recently have these expectations been subjected to rigorous empirical study.
Much of the impetus for this work resulted from Arnold's
(1983
) conceptual model of
natural selection gradients, which proposed that performance is an
intermediate step between morphology and fitness.
The empirical demonstration of relationships between morphological characters and their predicted functions can be problematic. Recent tests of theoretical expectations about the effects of many aspects of morphology/physiology on locomotor performance have had very mixed results. If a system is found that reliably predicts locomotor performance from limb morphology, it will allow us to produce hypotheses about evolutionary selective pressures that have affected limb design.
Increasing limb length is thought to positively affect locomotor
efficiency, endurance and speed and to increase jumping ability. To date,
however, all studies involving limb skeletal morphology and endurance or
efficiency have reported no statistically significant correlations (e.g.
Garland, 1984;
Garland and Else, 1987
;
Bennett et al., 1989
;
Tsuji et al., 1989
;
Huey et al., 1990
;
Steudel and Beattie, 1995
).
Many, although not all, studies of the relationship between limb morphology
and maximum speed have demonstrated positive correlations. All interspecific
studies of maximum speed (Losos and
Sinervo, 1989
; Losos,
1990b
; Garland and Janis,
1993
; Miles, 1994
;
Bauwens et al., 1995
;
Bonine and Garland, 1999
) and
some intraspecific studies of the limb-lengthspeed relationship (Miles,
1987
,
1994
;
Snell et al., 1988
;
Huey et al., 1990
;
Sinervo and Losos, 1991
;
Miles et al., 1995
;
Macrini and Irschick, 1998
)
have produced positive results, while other intraspecific studies of this
relationship have not (Garland,
1984
,
1985
;
Bennett et al., 1989
;
Losos et al., 1989
;
Tsuji et al., 1989
;
Sinervo and Losos, 1991
; see
Fig. 1).
|
Searches for a correlation between morphology and jump distance have
generally fared better in both interspecific
(Rand, 1952;
Zug, 1972
;
Dobrowolska, 1973
;
Losos, 1990b
;
Emerson, 1991
;
Choi and Park, 1996
) and
intraspecific (Rand and Rand,
1966
; Emerson,
1991
; see Fig. 1)
examinations; however, see Losos et al.
(1989
) and Choi and Park
(1996
). These leaping studies
have used frogs or lizards as subjects, but the present study uses a novel
mammalian experimental system, the domestic cat, to further elucidate the
relationship between jump performance and morphology.
Jump performance depends on takeoff velocity
Previous studies on jumping have invoked ballistics formulae to predict
that the velocity with which an animal's center of mass (CM) leaves the ground
determines the distance or height that it will travel after leaving the ground
(Hill, 1950;
Hall-Craggs, 1965
;
Alexander, 1968
;
Bennet-Clark, 1977
; Emerson,
1978
,
1985
,
1991
;
Gabriel, 1984
). The direction
of this movement is determined by the angle of takeoff. Marsh
(1994
) concluded that jump
performance can indeed be accurately predicted using ballistics equations if
horizontal and vertical distances traveled by the CM before takeoff are also
included. Because jump distance and height are largely dependent on takeoff
velocity (TOV), morphologies predicted to optimize TOV are the focus of the
current study. TOV should also be important for cats, which are proficient
predators that often hunt by pouncing on an unsuspecting prey item after
springing from a stationary crouch (Turner
and Meister, 1988
). The faster the takeoff, the more quickly the
cat reaches its prey.
Mechanical energy and takeoff velocity
TOV is determined by the mechanical work generated from hind limb extensor
muscles during the time from the deepest crouch to the point of last contact
with the ground (Alexander,
1968; Marsh,
1994
). This extensor muscle work is used to increase both the
kinetic and potential energy of the CM as it is lifted from its original
position to its height at takeoff (ht)
(Marsh, 1994
;
Peplowski and Marsh, 1997
).
Extensor muscle work can be thought of as the product of the extensor muscle
mass (m') and the work done per unit extensor muscle mass
(k):
![]() | (1) |
![]() | (2) |
After substituting %MHC IIx for k and substituting hind limb
length (l) for ht, equation 2 can be solved for
TOV:
![]() | (3) |
Ballistics and takeoff velocity
Most previous studies have expected increasing hind limb length to have a
positive influence on leaping distance
(Alexander, 1968;
Bennet-Clark, 1977
; Emerson,
1978
,
1985
), which is the opposite
of the prediction in equation 3. This expectation is based on the ballistics
formula:
![]() | (4) |
There is considerable empirical evidence that lizards and frogs with longer
hind limbs do indeed jump further than those with shorter hind limbs
(Rand, 1952;
Rand and Rand, 1966
;
Zug, 1972
;
Dobrowolska, 1973
;
Emerson, 1991
;
Choi and Park, 1996
; Losos,
1990a
,b
;
however, see Losos et al.,
1989
). These results suggest that increasing limb length does
positively affect TOV despite changing acceleration rates during the takeoff
period and the increasing investment made by extensor muscles in raising
potential energy. The effect of hind limb length on TOV can be seen more
clearly if we combine equations 2 and 4:
![]() | (5) |
Takeoff velocity and body fat
The positive effect of longer limb length on TOV will be decreased,
however, in animals with high body fat contents. The hind limb extensor
muscles in an animal with high body fat levels will expend more work in
increasing the body's potential energy during takeoff than would the muscles
of a leaner animal of equal body mass and hind limb length. Although previous
jump performance studies report significant positive correlations between jump
distance and body size in both frogs (Zug,
1978; Emerson,
1978
,
1991
;
Marsh, 1994
) and lizards
(Pounds, 1988
;
Losos et al., 1989
;
Losos, 1990b
;
Bels et al., 1992
, although see
Choi and Park, 1996
), none of
these studies present data on body fat levels in their subjects. It is likely
that body fat levels were uniformly low in the animals used such that `body
size' largely represented lean mass. Little is known about the extent of body
fat in wild carnivores (Pond,
1978
). Studies on other species suggest considerable variability.
Sherry (1981
) reports a 17%
seasonal weight change in red deer stags Cervus elaphus, and Scollay
(1980
) reports a 14% weight
change for male squirrel monkeys Saimiri sciureus during the breeding
season. Prestrud and Nilssen
(1992
) present data on wild
trapped arctic foxes Alopex lagopus showing fat content as percent
skinned carcass mass, averaging around 10% during the summer but over 20%
during winter months. Winter data include many values between 20% and 30% fat,
with one value over 40%. Furthermore, we would expect that the increased
weight of female cats during pregnancy would affect jumping performance in a
manner similar to that of body fat. Thus, the percentage of mass in most of
our laboratory specimens that is not due to lean mass is not seriously
incompatible with that seen in the wild.
The present study
In the present study, we investigate the morphological/physiological
determinates of among-individual variation in domestic cat jump performance,
measured by maximum TOV. We looked for correlates between TOV and body mass,
hind limb length, extensor muscle mass, body fat content and the percentage of
fast-twitch muscle fibers in the lateral gastrocnemius muscle in 18
individuals. It was hypothesized that individual cats would show significant
variation in their TOVs, and that this variation would be explained by
differences in the morphological/physiological variables listed above.
Specifically, we predicted that increasing %MHC IIx fibers and increasing hind
limb length and extensor muscle mass relative to lean mass would be positively
related to maximum TOV, while increasing body fat mass relative to lean mass
would negatively affect TOV. We also estimated the jump motivation level for
each cat and tested whether this had a significant effect on TOV (M. A.
Harris, K. Steudel and J. Bachim, in preparation).
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Materials and methods |
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Five (two males and three females) of the 18 cats donated by the Psychology Department were part of a study in which lesions of the visual cortex were made to one side of the brain (a unilateral lesion). The purpose of that research was to study the method of physiological compensation by remaining brain areas after early visual cortex damage. Four of these cats received this lesion when they were eight weeks old, and the remaining cat received the lesion when she was only one day old. Because the jump performance of these lesioned cats was not significantly different from non-lesioned animals, and because there was no difference in the amount or intensity of training required to induce maximal jumps between the two groups, no distinction was made between them in the analyses presented here.
Test subjects
A total of 18 domestic cats (13 intact females and five neutered males),
ranging in body mass from 2.66 kg to 7.93 kg, was used in this study. All cats
were at least two years old and not more than 10 years old, were in excellent
physical health and were accustomed to frequent human contact. Cats were
housed in metal wire mesh kennels (1.9 m highx1.6 m longx1.1 m
wide) with concrete flooring and had access to resting boxes and wooden
shelves within these cages. They were provided with Science Diet cat food
(Hill's company, Topeka, KS, USA) and water ad libitum until 18-24 h
before a jump training or video-taping session (see below).
Jump training
Between three and six sessions were devoted to acclimating each cat to lab
surroundings before jump training was initiated. During these 20-45 min
acclimation sessions, cats were allowed to roam freely in the lab and had
access to canned, moist cat food. Cats were not allowed inside the jump
enclosure during these sessions.
Each cat was subjected to a schedule of jump training sessions before maximum jumps were recorded on video tape. Between two and seven jump training sessions, each 20-60 min long, were required to train each cat to jump maximally. Cats participated in one jump training session per day. Food was withheld from the cats 18-24 h before each of these sessions. After each jump training session, animals were allowed access to their food for at least 60 min before it was again removed in anticipation of the following day's lab session, if one was scheduled.
Cats were trained to jump inside a rectangular enclosure (2.4 m highx0.9 m longx0.4 m wide; see Fig. 2) made of Plexiglas and masonite. This enclosure limited the direction and height of each jump. Cats were introduced to the enclosure through a trap door and were then placed on an adjustable takeoff platform inside the enclosure. Cats jumped from this takeoff platform to a stationary landing box (0.30 m x 0.45 m x 0.40 m) mounted on the upper left edge of the enclosure. The position of this platform, and thus the jump height, was adjustable.
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A training protocol was designed such that placement inside the jump enclosure stimulated jump behavior. In an effort to obtain maximal jumping performances, rewards were offered as soon as each cat successfully jumped to the landing box. Rewards were canned cat food accompanied by affection (petting) from an observer and, ultimately, removal from the enclosure. If jumps were not spontaneous, the takeoff platform was shaken and/or the cat was squirted with water until it jumped to the landing box. In this way, the takeoff platform was presented as an unpredictable, unstable environment, while the landing box represented a safe haven for each cat where rewards were available. Perhaps most importantly, each cat learned that jumping to the landing box was the only means of exit from the enclosure.
After each jump, cats were allowed to eat food and/or receive affection for approximately one minute before being removed from the landing box. Cats that ignored the food and affection attempts, and instead tried to jump out of the landing box, were removed immediately. The takeoff platform was then lowered by 5-10 cm, and the cat was returned to the takeoff platform through the trap door. This procedure continued until the cat had made between five and 10 total jumps or until the cat struggled in an obvious way to reach the landing box. No more than 10 jumps per session were allowed in order to minimize fatigue effects. Cats made approximately 10 jumps before becoming visibly fatigued. During subsequent sessions, the takeoff platform was lowered to within 5 cm of each cat's previous maximum jump, and the process continued until an approximate maximum height was achieved (i.e. the last height at which the cat successfully made it to the landing box, but only after an obvious struggle).
Measurement of takeoff velocity
At least 24 h after an approximate maximal height was determined for each
individual during training, each cat was video-taped jumping to this height.
Approximate maximal heights were either matched or exceeded on video-taping
days. Maximum vertical jump height for each cat was defined as the last
successful jump to the landing platform before consistent misses at the next
greater height (i.e. just 5 cm higher). TOV was measured from high-speed
videos of the takeoff portion of each cat's maximum jump. The maximum TOV for
each cat was measured on two different days in order to determine the
repeatability of each individual's performance. The highest TOV of these two
days was considered to be the maximum performance. Cats performed no more than
10 jumps on video-taping days and were weighed within 24 h of their maximal
jumps.
The movement of reflective markers placed on the cat's body was used to measure the maximum velocity of overall body center of mass (CM) position during the takeoff period. These movements were recorded by a high-speed (200 frames s-1) video camera. Each cat was labeled with reflective dots to indicate the location of the following anatomical landmarks: mid zygomatic arch (head), spinous process of scapula at anterior border, humerus greater tuberosity (shoulder), lateral epicondyle (elbow), styloid process of ulna (wrist), thoraciclumbar vertebral junction (T13), iliac crest, greater trochanter (hip), lateral epicondyle of the femur (knee), lateral malleolus (ankle) and metatarsophalangeal joint (5th MT) (see Fig. 3).
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At least one day prior to video-taping, the 11 anatomical landmarks were shaved, external measurements of body segments between anatomical landmarks were made, and the left side of the cat's body was dyed black. Body segment measurements were used to calculate the CM for each segment (see below). Cats were anesthetized with halothane gas during this process. The reflective dots were attached to the marked anatomical points using rubber cement paste on the day of video-taping. A black `calibration' backdrop inside the jump enclosure was used to convert video digitization units into real distance measures. The takeoff platform was narrowed so that cats jumped perpendicular to the camera.
Spotlights illuminated the reflective dots on the cat's body as it jumped.
Videos were taken using a Nac MOS-TV 200/60 high-speed video camera. The
xy coordinates of each dot were manually digitized by
projecting the video image onto a piece of graph paper using a stop-action VCR
and liquid-crystal display (LCD) projector. Videos were digitized at a rate of
100 frames s-1. A customized computer software program was written
to compute the overall body CM position from the mass of individual body
segments, the CM location for each of these segments, and the position of
segment CMs over time. Regression equations reported by Hoy and Zernicke
(1985) to predict segment
masses from body mass and segment length in domestic cats were used in this
algorithm. The location of this overall CM was located at three key positions
during the jump: the last frame showing hind paw contact with the ground
(`takeoff'), and one frame before and one frame after takeoff. TOV was defined
as the change in CM position over the three frames surrounding and including
takeoff (a 0.02 s time span).
Hind limb dissections and body fat measurement
A standard euthanasia procedure was used in which each cat was first
anesthetized with halothane gas. An injection of sodium pentobarbital was then
administered intravenously in the femoral vein until all respiratory and
cardiac activity had ceased. Hind limb muscles were dissected and measured
within 2 h of euthanasia.
The three hind limb muscles analyzed in this study were the semimembranosus
(hip extensor), the vastus lateralis (knee extensor) and the lateral
gastrocnemius (ankle extensor) (Fig.
4). All of these muscles have been shown to be electrically active
during cat jumps (Zomlefer,
1976; Smith et al.,
1977
; Zomlefer et al.,
1977
; Walmsley et al.,
1978
; Zajac et al.,
1981
,
1983
;
Zajac, 1985
;
Abraham and Loeb, 1985
). These
muscles were removed from the right leg. They were separated and cut at the
termination of muscle fibers at the origin and insertion, and the mass of each
muscle was recorded. Dissected muscles were placed on ice in a standard
freezer until all dissections were completed and were then transferred to a
-80°C freezer and stored until fiber type analysis. The individual masses
of these three muscles were summed to give total muscle mass. We chose to use
these three muscles rather than all of the extensor muscles because each of
the three chosen muscles is a major extender of its respective joint and each
is easily dissected.
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The entire left limb was removed by cutting through the ilio-sacral and pubic articulations. After removal of all muscles and tissues from the leg, the lengths of the femur, tibia, tarsals and third metatarsal were recorded and summed to give a total hind limb length value. After removal of the left leg and the three extensor muscles from the right leg, the percent fat content of the carcasses was measured using a DPX-L X-ray bone densitometer (version 1.5g, copyright 1988-95, Lunar Corp., Madison, USA). Fat mass was calculated for each cat as the product of % body fat and whole body mass. Lean body mass was computed by subtracting fat mass from whole body mass.
Myosin heavy chain analysis
The MHC Type IIb isoform fibers are fast-twitch and develop the largest
tetanic tension in comparison with the Type I slow-twitch and Type IIa
fast-twitch, moderate-tension fibers
(Burke, 1994;
Kelly and Rubinstein, 1994
).
Talmadge et al. (1996
) found
that the IIx isoform, rather than the IIb isoform, is present in cat limb
muscles. In cats, therefore, the percentage of MHC Type IIx isoform in
extensor muscles should be correlated with jump performance.
The lateral gastrocnemius muscle was chosen for fiber type analysis because
it is known to be activated during the cat jump takeoff period
(Smith et al., 1977;
Abraham and Loeb, 1985
) and is
known to contain all three MHC types. The most predominant is the Type IIx
isoform; mean fiber type percentages reported for cats are between 66% and 72%
(Braund et al., 1995
;
Talmadge et. al., 1996
). In
this study, the lateral gastrocnemius muscles from each cat were prepared for
electrophoretic separation in the following manner: the middle one-third,
cross-sectional portion of each muscle was dissected, quick-frozen in liquid
nitrogen, and smashed into smaller pieces with a hammer. These pieces were
then immersed in more liquid nitrogen and ground into a fine powder with
mortar and pestle. Muscle powder was added to chilled rigor buffer solution (5
mmol l-1 KCl, 2 mmol l-1 EGTA, 2 mmol l-1
MgCl2, 2 mmol l-1 NaN3, pH 7.2) to produce a
final concentration of approximately 0.3 mg myofibrillar protein
ml-1. This protein solution was added to ureathiourea sample
buffer (8 mol l-1 urea, 2 mol l-1 thiourea, 0.05 mol
l-1 Tris, pH 6.8), 75 mmol l-1 DTT (dithiothreitol), 3%
SDS (sodium dodecyl sulfate) and 0.05% bromophenol blue to produce a final
concentration of approximately 0.15 µg myofibrillar protein
µl-1. Samples were boiled at 100°C for 3 min and stored at
-70°C.
The three MHC isoforms present in cat skeletal muscle were separated by
pulse electrophoresis in SDS-polyacrylamide (SDS-PAGE) gels using a protocol
modified from Talmadge and Roy
(1993). All gels were run in
vertical slab gel units (Hoefer SE 600, Pharmacia Westshore Technologies,
Muskegon, MI, USA) using ECPS 3000/150 power supplies (Pharmacia). Gels were
18 cmx16 cm and were 0.75 mm thick. The stacking gel was composed of 4%
(w/v) acrylamide, with an acrylamide:
N,N'-methylene-bisacrylamide (bis) ratio of 50:1, deionized
water, 70 mmol l-1 Tris (pH 6.8), 0.4% (w/v) SDS, 30% (v/v)
glycerol, 4.0 mmol l-1 EDTA, 0.04% (w/v) ammonium persulphate (APS)
and 0.36% (v/v) TEMED
(N,N,N',N'-tetramethylethylenediamine). The separating
gel consisted of 9% (w/v) acrylamide, with bis cross-linking of 1.5% (ratio
67:1), deionized water, 200 mmol l-1 Tris (pH 8.8), 0.4% (w/v) SDS,
30% (v/v) glycerol, 100 mmol l-1 glycine, 0.03% APS and 0.15%
TEMED. Polymerization of these gels was initiated with the TEMED and APS. The
electrode buffer was the same for both upper and lower reservoirs and
consisted of 0.38 mol l-1 glycine, 0.05 mol l-1 (w/v)
Tris, 0.01% (w/v) SDS and deionized water (pH 8.9;
Talmadge and Roy, 1993
). The
upper buffer was supplemented with 0.2 mmol l-1 DTT immediately
before the start of electrophoresis. Gels were run at constant current (13 mA)
for 32 h using a pulse unit connected to a Hoefer model SE600. Pulse cycles of
20 s on/off were used, resulting in an overall variation of voltage between 18
mV and 510 mV. Temperature remained constant at 10°C for the duration of
the electrophoresis. Gels were stained with silver and scanned with a BioRad
Imaging Densitometer (Model GS-670; Pharmacia Westshore Technologies).
MHC isoforms were quantified using Molecular Analyst (version 1.4) software
(Pharmacia Westshore Technologies). Relative proportions of each isoform were
calculated by dividing the optical density of each individual isoform band by
the summed optical density of all three bands within each column (i.e. by the
total MHC isoform content within each individual cat). The proportion of each
MHC isoform is thus expressed as the percentage that it contributes to the
total area of MHC bands (Fauteck and
Kandarian, 1995).
Statistical analysis
Linear correlation analyses and paired t-tests were used to
compare maximum velocities on days 1 and 2 to assess performance
repeatability. Fat mass was calculated as % body fat multiplied by body mass,
and lean body mass was calculated as body mass minus fat mass. Significant
correlations were found between lean body mass and hind limb length
(r=0.709, two-tailed P=0.001), muscle mass
(r=0.917, P<0.001) and fat mass (r=0.739,
P<0.001). To examine the effects of these three variables
independent of body size, `lean' mass residuals were calculated from a linear
regression of each variable vs. lean body mass.
Multiple regression analyses were performed to develop a model containing variables that together explain the most variation in TOV. Lean mass residuals for hind limb length, muscle mass and fat mass were entered, together with lean mass and %MHC IIx content, as independent variables. A backwards elimination criterion was then used to eliminate variables that did not explain a significant amount of variation. Kinetic energy was calculated using whole body mass and maximum TOVs measured from each individual. Potential energy was calculated using whole body mass and hind limb length. The ratio of potential to kinetic energy was compared with fat mass. All analyses were performed using SPSS versions 8.0 and 11.0.
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Results |
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MHC IIx was the first variable to be eliminated in the multiple regression, followed by lean mass and residual muscle mass. Backwards elimination of these insignificant predictors yielded a multiple regression model containing only two significant independent variables: residual hind limb length and residual fat mass. This two-variable model explained over 62% of the variation in maximum TOV (r=0.790, F=12.5, P=0.001, N=18). Models containing lean mass and residual muscle mass in addition to residual hind limb length and residual fat mass modestly improved the predictability of the model, to approximately 72% (r=0.847, F=8.26, P=0.002, N=18).
The ratio of potential to kinetic energy
The importance of fat mass in determining TOV may result from its
disproportionate effect on the work that muscles must do to increase potential
energy relative to kinetic energy. A plot of the ratio of potential energy to
kinetic energy as a function of lean residual fat mass shows a significant
positive relationship between these two variables
(Fig. 5). In other words, the
investment in potential energy relative to kinetic energy increases as the
amount of body fat relative to lean body mass increases (r=0.678,
P=0.002, N=18).
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Variation between individuals
Considerable morphological and jump performance variation among individual
cats was observed (see Table
2). The mass of these cats ranged nearly threefold, from 2.66 kg
to 7.93 kg, while maximum TOV ranged from 286.3 cm s-1 to 410.8 cm
s-1. Body fat content also varied widely, from 11% to 48% of total
body mass. This body fat content was probably slightly, but consistently,
overestimated, however, because the carcasses scanned for fat measurement were
missing one (mostly lean) leg and the three dissected muscles from the
remaining leg. There was no difference between mean female (343.5 cm
s-1) and mean male (342.8 cm s-1) maximum TOVs
(t=0.03, two-tailed P=0.98, N=18).
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Because measurement of the proportion of MHC IIx was possible for only 17 of the 18 cats, analyses were constrained to this subset of cats where appropriate. MHC content among these 17 cats ranged almost twofold, from 44.7% to 81.4% of all the MHC isoforms present in the lateral gastrocnemius muscle. MHC Type I isoform content ranged from 0.7% to 30.5% (see Table 2). For all cats, the IIx band was the most predominant isoform present (Fig. 6). For the nine cats for which MHC content was measured on two separate gels, one-way analysis of variance (ANOVA) indicated highly significant variation between cats as compared with the variation between MHC content readings from two different gels (F8,9=9.8, P=0.001 for MHC IIx; F8,9=9.2, P=0.002 for MHC I).
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Jump technique
Jump technique had become very stereotypical by the time each cat had
reached its maximum performance level. It consisted of a very deep crouch,
lift-off of the forelimbs and, finally, an explosive extension of the hind
limbs and back before takeoff (Fig.
3A-C). Each successful jump ended when the cat pulled its entire
body up to the landing box with its forearms. The time interval for all jumps
from deep crouch to takeoff was 150-270 ms, which is comparable to the 150 ms
`launching phase' reported by Zomlefer
(1976) for a maximal vertical
jump made by a cat to a suspended cotton ball 1.3 m above the ground. Zomlefer
also calculated the TOV for one maximal jump from a force-time curve and
estimated it to be 343 cm s-1. This is comparable with the maximal
TOVs measured here. At takeoff, the CM was found to be located between the
13th thoracic vertebra and the iliac crest, approximately midway between the
dorsal and ventral surfaces.
Performance repeatability
A general linear model repeated-measures ANOVA indicated highly significant
variance in the mean TOVs between cats as compared with the variance in TOV
within the two days it was measured for each cat
(F17,18=11.4; P<0.001, N=18). TOV was
a repeatable performance for the 18 cats on the two days it was measured, as
shown in Fig. 7 (Pearson
product-moment correlation coefficient r=0.841,
P<0.0001). A paired t-test indicated no difference in
mean TOV on day 1 vs. day 2 (t=-1.072, P=0.299,
N=18). In other words, TOV on day 1 was not consistently higher or
lower than day 2 TOV. There was no significant relationship between (day 1
day 2) TOV and mean TOV (r=-0.103, P=0.685), which
indicates that better jumpers did not tend to jump with maximal velocity on
day 1 only or on day 2 only. Ten cats achieved their highest TOV on day 1, and
eight cats achieved their highest TOV on day 2.
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Discussion |
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Body fat content, hind limb length and muscle mass
The variation in body fat content among individual cats in this study was
considerable. As stated previously, the absolute measurements for body fat
were probably overestimated, but were done so in a consistent way (in other
words, the tissues removed from each carcass before body fat measurement were
dissected in a consistent manner). In either case, it is accurate to conclude
that body fat content varied nearly fourfold from the leanest to the fattest
cat (mean=28%, S.D.=11.0%, S.E.M.=2.6%). One other study that analyzed the
chemical composition of 20 domestic cat carcasses (14 males and six
non-pregnant females; Hendriks et al.,
1997) also reported a nearly fourfold range, 6.2-23.6%, in lipid
content per unit wet tissue (mean=11.2%, S.D.=5.3%, S.E.M.=1.2%).
Fat mass relative to lean body mass explained the most variation in maximum TOV. The large explanatory power of relative fat mass (standardized ß coefficient=-0.62) reveals the considerable influence of body fat levels on an explosive performance such as jumping. This result appears to be driven by significantly larger portions of extensor muscle work invested in raising potential energy relative to kinetic energy levels during takeoff in fatter animals (see Fig. 5). While this effect may be more important in these laboratory animals than would be the case in the wild, there is considerable variation in % fat in the wild, as documented above, and female cats must still jump even while carrying the extra weight of pregnancy. We believe, therefore, that these results can be generalized.
Hind limb length relative to lean body mass was the second best predictor
of TOV (standardized ß coefficient=0.41) in the four-variable regression
model. These results suggest that the negative effect of increasing limb
length on the amount of extensor muscle work invested in raising potential
energy is surpassed by the positive influence of longer hind limbs on kinetic
energy production. When accelerations during takeoff increasingly exceed
g (9.8 m s-2), the effect that longer limbs have on
increasing CM kinetic energy levels outpaces their contribution to increasing
CM potential energy. In our cats, we calculated average CM accelerations
ranging from 11.9 m s-2 to 24.6 m s-2 [where average
acceleration = (TOV initial velocity)/(takeoff duration)]. If cats
perform like the frogs in the Marsh and John-Alder
(1994) jumping study, the
average accelerations that we measured kinematically underestimate the
accelerations produced during the last half of the takeoff period.
Extensor muscle mass relative to lean body mass was not found to explain a
significant portion of the variation in cat TOV. The lack of a relationship
between residual extensor muscle mass and TOV in the present study may be
explained by the influence of body fat mass on the muscle mass/body mass ratio
(m'/m in equation 3). As fat mass increases,
m'/m decreases, and so TOV should be decreased. Linear
regression analyses of our cat data confirm these relationships:
m'/m decreases as fat mass increases (r=-0.720,
F=17.24, P=0.001, N=18; see
Fig. 8a), and
m'/m is significantly and positively related to TOV
(r=0.647, F=11.51, P=0.004, N=18; see
Fig. 8b). Two interspecific
frog studies did find positive correlations between hind limb muscle mass and
maximum jump distance (Emerson,
1978) and between hind limb muscle mass and TOV
(Choi and Park, 1996
). Miller
et al. (1993
) report that
large leopard frogs (Rana pipiens) jump further than smaller leopard
frogs, and also found that large frogs have relatively larger gastrocnemius
muscles. Although they did not directly examine the relationship between jump
distance and relative gastrocnemius size among their individual frog subjects,
they hypothesize that larger frogs jump further because of their relatively
larger hind limb extensor muscles.
|
Myosin heavy chain isoform content
Variability in the MHC IIx isoform content of the lateral gastrocnemius
muscle among the 17 cats was considerable (mean=69.7%, S.D.=9.83%,
S.E.M.=2.38%). Talmadge et al.
(1996) report a similar mean
± S.E.M. (72±2%) for the lateral gastrocnemius muscle in their
sample of three domestic cats. Similarly, the MHC I isoform content measured
in the present study (mean=9.3%, S.D.=6.85%, S.E.M.=1.66%) demonstrated a
similar central tendency to that reported by Talmadge et al.
(1996
) for the Type I isoform
in the same muscle (mean=13%, S.D.=1.73%, S.E.M.=1%).
Unexpectedly, the amount of fast-twitch fiber present in the lateral
gastrocnemius muscle (an important ankle extensor;
Zomlefer et al., 1977;
Zajac et al., 1981
;
Abraham and Loeb, 1985
) was not
found to be related to TOV. This result is counterintuitive because the
proportion of fast-twitch fibers is known to be correlated with maximum
shortening velocity, and thus should be a good estimate of the work done per
unit muscle during the takeoff period.
The lack of a relationship between fast-twitch fiber content and TOV may be
explained by the biarticular action of the lateral gastrocnemius; this muscle
spans both the knee and the ankle joints. Although the main effect of lateral
gastrocnemius contraction is to extend the ankle joint, the degree and rate of
fiber shortening is limited by knee joint extension during takeoff. It has
been hypothesized that this decrease in lateral gastrocnemius shortening
velocity has two advantages for humans during jumping: (1) it allows larger
forces to be produced at the rapidly extending ankle joint and (2) it allows
knee extensor muscles to be fully activated until takeoff without damaging the
knee joint by the high joint angular velocities produced
(Bobbert and van Ingen Schenau,
1988; van Soest et al.,
1993
).
The degree and rate of lateral gastrocnemius fiber shortening is further
complicated by this muscle's insertion into the Achilles tendon, a series
elastic element (SEE). Stretching (or compliance) of the SEE in the lateral
gastrocnemius and other triceps surae muscles results in storage of energy
before fibers contract. Release of this energy enables fibers to shorten at
lower velocities and produce more force during takeoff, resulting in high
power output at the ankle joint during the latter part of takeoff
(Bobbert, 2001). Our
expectation of a linear positive relationship between lateral gastrocnemius
fiber-shortening velocity and TOV may therefore be too simplistic for this
complicated muscletendon system. Possibly, examination of the
relationship between fast-twitch fiber content and TOV in the monoarticular
vastus lateralis muscle or other hind limb muscles would produce a different
result.
Conclusions
We found that cats with longer hind limbs and lower fat mass relative to
their lean body mass achieved higher TOVs. These two variables explained
significant variation in maximum TOV in a manner consistent with predictions
based on the work done by extensor muscles to increase both kinetic and
potential energy during takeoff. This study is the first to confirm the limb
lengthjump performance relationship in an endothermic vertebrate.
Contrary to predictions, however, extensor muscle mass relative to lean body
mass and percentage composition of MHC IIx were not found to significantly
predict TOV.
The results of the present study as well as of other examinations of the limb morphologyleaping performance relationship suggest that jumping may be more highly and consistently correlated with morphology/physiology than are other performance variables. This implies that the evolution of limb design can most readily be studied on an ecologically relevant performance variable whose relationship to morphology is relatively simple biomechanically and on which data can be collected under carefully controlled lab conditions. Furthermore, the use of a large, easily trained subject will limit additional sources of experimental error. If these criteria are met, significant correlations between morphology and performance are more likely to be revealed.
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