Functional trade-offs in the limb bones of dogs selected for running versus fighting
1 Department of Biology, University of Utah, Salt Lake City, UT 84112,
USA
2 Department of Orthopaedics, University of Utah, Salt Lake City, UT 84112,
USA
3 Department of Material Science Engineering, University of Utah, Salt Lake
City, UT 84112, USA
* Author for correspondence (e-mail: carrier{at}biology.utah.edu)
Accepted 25 July 2005
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Summary |
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Key words: locomotion, aggression, bone mechanical properties, Canis lupus familiaris, greyhound, pit bull
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Introduction |
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Bones are adaptive structures that can vary in their mechanical properties
(1) during an organism's lifetime, in response to changing developmental
parameters and functional demands, (2) throughout an individual's body, due to
varying functional requirements, and (3) among different members of a clade,
associated with different life histories and environmental conditions
(Currey, 1979;
Currey and Pond, 1989
;
Biewener, 1990
;
Swartz et al., 1992
;
Carrier, 1996
;
Blob and Biewener, 1999
;
Heinrich et al., 1999
;
Blob and LaBarbera, 2001
).
Currey (1979
) provided a
dramatic illustration of the relationship between bone material properties and
function with a comparison of red deer antler, cow femur and fin whale
tympanic bulla. Of the three types of bone, antler was the least stiff but
absorbed the most energy before it failed, and cow femur resisted the greatest
forces in bending. Currey suggested that these differences represent the need
of antler to withstand large impact loads during male-male aggression and the
need of limb bones to be stiff and strong to transmit muscular forces. This
distinction between the mechanical properties of skeletal elements that
function as weapons (i.e. antlers and tusks) versus those that
function as limb elements has become well documented
(Brear et al., 1993
;
Kitchener, 1991
; Currey,
1987
,
1989
;
Blob and LaBarbera, 2001
; but
see Zioupos et al., 1996). For example, axis deer have antlers that are
composed of relatively stiff tissue (11.6 GPa;
Kitchener, 1991
), but the bone
of their proximal limb elements is almost three times stiffer (31.6 GPa;
Currey, 1999
).
We wondered if similar differences might exist within limb bones of animals
specialized for running versus those specialized for fighting.
Although the limb bones of most species are unlikely to experience the level
of impact loads that deer antlers are subjected to during fighting, many
mammalian species fight by striking and grappling with their forelimbs.
Fighting can be expected to load limb bones with maximal muscle moments and in
directions that are highly variable and unpredictable. Furthermore, during
grappling, bending and torsional moments on limb bones induced by an opponent
might exceed those that the animal's own muscles could produce. Limbs are also
targets of bites during fighting. Biting could fracture limb bones outright or
induce failure from bending or torsion as the two animals struggle. Indeed,
fractures of bones do occur when dogs fight. In a survey of 284 bone fractures
in dogs admitted to a metropolitan small animal hospital over a 2-year period,
fights were the third most frequent cause of fracture and accounted for 14% of
the bone fractures that were due to causes other than encounters with
automobiles, human feet and slamming doors
(Phillips, 1979;
Cook et al., 1997
). Dog attacks
also produce bone fractures in humans, occurring at a frequency of 0.4% of the
nonfatal dog attack-related injuries treated in USA hospital emergency
departments in 2001 (Gilchrist et al.,
2003
). By contrast, other than in racing greyhounds (discussed
below), we were unable to find reference to failure of limb bones during
running in dogs. Thus, there is reason to suspect that selection for fighting
ability might result in limb bones that are more resistant to failure than the
bones of animals specialized for running. Obviously, specialization for
fighting cannot be driven as far in limb bones as it has in deer antlers
because of the conflicting demands of locomotion on the limbs. Nevertheless,
we suspected that the limb bones of animals specialized for fighting would
have lower stiffness and a greater capacity for absorbing energy before
failure than the limb bones of animals specialized for running.
To test these expectations, we compared the mechanical properties of limb bones in two breeds of domestic dog: greyhounds and pit bulls. Greyhounds have undergone intense artificial selection for high-speed running and anaerobic (burst) stamina. By contrast, pit bulls have been selected for physical combat with other dogs. Specifically, we predicted that, to avoid failure during fighting, the limb bones of pit bulls would exhibit lower elastic moduli, lower yield and maximum stresses but higher maximum resistive forces and higher levels of work to fracture than the limb bones of greyhounds. By contrast, we expected that the limb bones of greyhounds would have smaller second moments of area relative to bone length and body mass to minimize the inertia of the bones and thereby reduce the energetic cost of high-speed running. Additionally, because the primary loading direction is relatively predictable during running but unpredictable in a fight, we expected that the limb bones of greyhounds would have less circular diaphyseal cross sections than the bones of pit bulls.
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Materials and methods |
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The cadavers used in this study were the same as those used in a previous
study of the limb muscle of these two breeds
(Pasi and Carrier, 2003). All
the subjects were osteologically mature, with fused epiphyseal plates. The
four greyhound cadavers were donated by the School of Veterinary Medicine at
Colorado State University. All appeared to be healthy at the time of death,
and dissection revealed no visible adipose tissue. Their eviscerated body mass
ranged from 27.34 to 30.80 kg, with a mean ± S.D.
of 28.52±1.98 kg. The four pit bull cadavers used were animals that had
been euthanized at local (Utah) animal shelters and were donated to the study.
These dogs also appeared to be healthy at the time of death and they did not
have visible accumulations of subcutaneous adipose tissue. The eviscerated
body mass of the four pit bulls ranged from 20.91 to 27.87 kg, with a mean
± S.D. of 23.61±3.73 kg.
Caveats and limitations
Although there are well-recognized limitations associated with two species
(or breed) comparisons when studying adaptation
(Garland and Adolph, 1994),
the choice of greyhounds and pit bulls substantially reduces these problems.
First, the types of selection on the two breeds are known and were very
specific. In both cases, the financial incentives of the breeders have been
high, driving the two breeds toward extreme specialization. Second, the
environment in which the two breeds have evolved has been largely controlled.
That is, both breeds have evolved as domesticated animals in which humans
provided their day-to-day care and survival. The ancestors of the subjects we
studied grew up and lived in a temperature-controlled environment, their food
and water was served to them and their mating opportunities were determined by
their human owners. Thus, although differences between the two breeds may
exist due to various founder effects or genetic drift, adaptive differences
other than those due to selection for fighting or running are unlikely to
exist. The study remains unreplicated, however, and that limits the confidence
we can have in any conclusion.
A second limitation of the comparison used in this study is the lack of information about the ancestral configuration. We did not collect similar data from wolves, the species from which domestic dogs are derived. The lack of information about the ancestral state makes it impossible to say anything about the level of specialization in the two domestic breeds. It could be that any difference in bone properties observed between the two breeds is due entirely to selection on running performance in the greyhounds, with the pit bulls being very similar to the ancestral state. Alternatively, differences between the breeds could be entirely due to selection on fighting ability in pit bulls. In which case, the greyhounds would be similar to wolves. Without knowledge of the ancestral state, the level of specialization cannot be addressed. Nevertheless, knowledge of the ancestral state is not necessary to falsify the different hypotheses outlined above. If greyhounds and pit bulls do not differ in the predicted direction, a given hypothesis of conflict for specialization of running versus specialization for fighting would be falsified.
A final caveat that could compromise the interpretation of the results of
this study is the possibility that the subjects of the two breeds experienced
substantially different levels of `functional adaptation' during their lives.
Because the greyhound subjects came from the racing industry, we can be
confident that their limb bones were exposed to the loading of high-speed
running. The pit bull subjects, by contrast, were unlikely to have been
exposed to frequent fighting that could result in functional adaptation. In
most species, however, serious fighting is not a routine behavior and
individuals prepare for true fighting through play
(Pellis and Pellis, 1987;
Pellis et al., 1993
).
Nevertheless, breed differences in functional adaptation could impact this
analysis in unknown ways.
Mechanical testing
After they were euthanized, the subjects were sealed in plastic bags and
frozen. For dissection, the subjects were thawed at room temperature. The
humerus, radius, 4th metacarpal, femur, tibia, and 3rd metatarsal were
dissected from one side of each dog and cleaned of all soft tissue. We chose
to test the radius rather than the radius and ulna together, or just the ulna,
because the dimensions of the radius, by itself, more closely approximate the
shape of a beam. The bones were then stored in sealed plastic bags below
0°C until mechanical testing was performed. Before testing, the bones were
thawed at room temperature and placed in physiological saline at 25°C for
1-2 h.
The bones were removed from the saline and immediately tested to ensure negligible dehydration and temperature change. We used a servo-hydraulic material testing system (model 8500; Instron Corp., Canton, MA, USA) to load the bones in three-point static bending at a rate of 0.16 mm s-1, producing fracture in 60-120 s. The loaded length of the bones included as much of the diaphysis as possible and so varied for each bone. Care was taken to orient the bones on the loading supports in a consistent manner, such that the load was applied perpendicular to the long axis of the bone and in the parasagittal (i.e. anterior-posterior) plane.
Bones were loaded until fracture occurred. This provided a measure of yield
and fracture parameters. Yield represents the point at which the bone ceases
to behave elastically and is difficult to determine precisely in bending
tests. To calculate yield, we used the offset method
(Turner, 1993), in which a
line parallel to the linear portion of the stress-strain curve is calculated
and then offset by a strain of 0.2%. Maximum load is the maximum resistance
that the bone offers to loading. Fracture load is the force applied at the
moment of failure (i.e. when fracture occurs) and is a measure of the strength
of the bone as a whole. Yield and fracture stress were calculated from the
relationship:
![]() | (1) |
where F is yield or fracture force, L is the distance
between supports (length of diaphysis), Y is the outer radius at load
point, and I is the second moment of area at the site of loading
(Turner, 1993).
The modulus of elasticity (E) is a measure of the stiffness of the
bone. It was calculated from the relationship:
![]() | (2) |
where Fy is the force at some deflection, D,
at a low strain (prior to yield; i.e. Fy/D is the
slope of the initial linear portion of the curve), L is the length of
the loaded beam, and I is the second moment of area at the site of
loading. Because the loaded length of the bones was less in the pit bulls than
the greyhounds, and was in all cases less than is typically needed for
application of simple beam theory (i.e. aspect ratio >15), the analysis was
corrected for effects of shear stresses using the CS term
(see Eqn 4). To correct for shear, we first approximated shear stresses in the
cross section of the beam by modifying methods used to evaluate shear in solid
beams (Gere, 2001) to the
geometry of a hollow beam. By using force balance within a hollow beam, the
total shear stress (
) on any radial cross section of the hollow beam was
found to be:
![]() | (3) |
where r1 and r2 are the inner and
outer radii of the bone cylinder, respectively, and is the angle from
the horizontal plane to the position of the radial cross section. These shear
stresses are maximal, as expected, in the horizontal cross section of the beam
(
=0°) and zero on the vertical cross section (
=90°). We
next equated the energy in the beam due to both normal stresses and the above
shear stresses to the energy of deformation (Fy
D/2) and found the correction term to be:
![]() | (4) |
where Emod is the elastic modulus and
Gmod is the shear modulus. We used values for
Emod and Gmod from human cortical bone
(Martin and Burr, 1998) to
evaluate CS. Note that the correction only depends on the
ratio Emod/Gmod for bone, and this
ratio is fairly uniform among species of mammals: 2.74 for humans
versus 2.85 for cows (Martin and
Burr, 1998
).
Thus, to correct for shear stress, the bones were modeled as hollow or thick-walled cylinders with an inner radius r1 and an outer radius r2. Although this is an approximation of the bone shape, we believe it is reasonable for extracting shear correction. Taking into account actual cross sections and variations in cross sections along the bone would require numerical analysis and would be unlikely to change the results from any of the comparisons.
After mechanical testing, the broken ends of the bones were cut as near to
the fracture as possible for dimensional analysis. To measure the second
moment of area of the cross sections, we analyzed digital images of the cut
cross sections with Optimas, version 6 software (Media Cybernetics, San Diego,
CA, USA). Because the bones of the two breeds differ significantly in length,
we calculated an index of shape that relates the second moment of area
(I) of the bone cross section to a reference force moment:
![]() | (5) |
where I is the second moment of area of the mid-diaphysis, Mb is body mass, L is the length of the diaphysis, and Ymd is the outer radius at mid-diaphysis. Length of the diaphysis was measured between epiphyseal lines (estimated when not visible) on the cranial surface of the bone for the radius, metacarpal, femur and metatarsal and measured on the caudal surface of the bone for the humerus and tibia. High values of this index indicate a relatively large second moment of area for the bone's length and the animal's mass.
Lastly, we determined whether or not there were differences in the
cross-sectional shape of the mid-diaphysis by calculating an index of
circularity (Cornhill et al.,
1980; Hueck, 2000
)
of the cross sections for the two bones that most closely approximated a
circular cross section, the humerus and femur. The circularity index
(CI) is defined as a dimensionless ratio of the total area contained
within the periosteal perimeter at the mid-diaphysis (A) divided by
the square of the periosteal perimeter (P):
![]() | (6) |
The ratio of area to perimeter-squared was normalized by 4 so that the
ratio has a value of unity for a circle. This CI gives a value less
than one for noncircular cross sections.
Statistics
Data were collected for 48 bones (six bones per dog, four dogs per breed,
two breeds). To address whether or not there were differences between the
breeds for a given bone (e.g. radius), we grouped the data by bone and checked
for breed differences using unpaired t-tests with a sequential
Bonferroni correction (Sokal and Rohlf,
1981). To address whether the breeds differed for each parameter
(e.g. whether the modulus of elasticity was higher on average in the greyhound
bones than in the pit bull bones), we used Fisher's combined probability test
(Sokal and Rohlf, 1981
),
comparing the P-values of all six bones. A fiducial limit for
significance of P<0.05 was chosen.
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Results |
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Diaphyseal length was 1.48 (±0.02) times greater on average in the greyhounds than in the pit bulls. This difference made a functional comparison of mid-shaft diameter or second moment of area inappropriate for the two breeds because of the effect that bone length has on bending moment. Hence, we compared the two breeds with a shape index (Eqn 5) that relates the second moment of area of the bone's cross section to a reference moment. High values of this index indicate relatively large mid-diaphyseal second moments of area for the bone's length and the animal's mass. For three of the proximal limb bones (humerus, radius and femur), the pit bulls had significantly higher mid-diaphyseal second moments of area for their length than did the greyhounds (Table 1). The shape index did not differ between the two breeds for the distal bones (metacarpal and metatarsal). Nevertheless, using the P-values from all six bones, the shape indexes were higher in the pit bulls than in the greyhounds (P<0.005; Fisher's combined probability).
The two breeds also differed in the cross-sectional shape of the proximal limb bones (Fig. 1). The circularity indexes for the humeri and femurs of the pit bulls were closer to unity, indicating a more circular cross section than was the case in the greyhounds (P<0.05; unpaired t-test).
|
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The limb bones of greyhounds sustained higher stresses at yield than the limb bones of pit bulls (P<0.025; Fisher's combined probability; Table 2). The maximum stress sustained by the bones, however, was not different between the two breeds.
Differences were observed in the material properties of the bones of the forelimb versus the hindlimb, as well as among the bones within each limb (Table 2). Comparing serially homologous elements between the fore- and hindlimb in both breeds, the bones of the hindlimb had higher elastic moduli than those of the forelimb (P=0.046; paired t-test). Of the three skeletal elements within each limb, the central elements (i.e. radius and tibia) had higher elastic moduli (P=0.006; unpaired t-test) and higher yield stresses (P=0.004, unpaired t-test) than the proximal and distal elements. These intra-limb patterns were observed in both breeds.
Whole bone properties
The mass-specific maximum resistive force that the bones sustained during
three-point bending was not different between the breeds (P>0.4;
Fisher's combined probability; Table
3). There was a clear trend of higher maximum resistive force
among the four proximal bones in the pit bulls but none of these bones
exhibited a significant difference under the constraint of a sequential
Bonferroni test.
|
The mass-specific energy absorbed (i.e. work) at fracture was greater in the pit bulls (P<0.001; Fisher's combined probability; Table 3). This was the most dramatic difference observed between the two breeds. The work to fracture was on average 2.2-fold greater in the pit bulls than in the greyhounds. All four of the proximal bones exhibited a significant difference (Table 3). The work to fracture the long bones of the feet, however, did not differ between the two breeds.
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Discussion |
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Based on these expected differences in specialization for running versus fighting, we predicted that, under three-point static bending, the limb bones of greyhounds would exhibit higher elastic moduli, higher yield and maximum stresses, lower levels of work to fracture and lower maximum resistive force than the bones of pit bulls. We also expected that the limb bones of greyhounds would have smaller second moments of area relative to bone length and body mass and less circular diaphyseal cross sections then the bones of pit bulls. We found that elastic moduli and yield stresses were higher in the greyhounds whereas the work to fracture was much higher in the pit bulls. On average, the elastic modulus was 60% greater, yield stress was 17% greater and the work to fracture was 57% less in the greyhound bones than in the pit bull bones. The second moments of area relative to bone length and body mass were higher in the pit bulls, and the diaphyseal cross-sectional shape of the humerus and femur was more circular in the pit bulls. These observations are consistent with expectations based on specialization for running versus fighting.
Two of the measured variables, however, did not fit our expectations. No significant differences between the breeds were found in maximum stress and maximum resistive force. Peak loads and stresses in most materials are highly dependent on material flaws that facilitate crack growth. Thus, the lack of significant difference in these variables is not surprising. In contrast to failure stress, which represents flaw-dominated crack growth, the onset of yielding is typically a bulk process associated with shear deformation rather than crack growth. Yield stresses are therefore less variable than flaw-dominated strength properties, making them a more reliable metric.
The long bones of the feet, metacarpal and metatarsal, presented a
consistent contrast to the more proximal limb bones. Although the long bones
of the feet differed between breeds in mid-diaphyseal second moment of area
(Table 1), they did not differ
in the other parameters we measured. In greyhounds, the metacarpal and
metatarsal tended to have low elastic moduli and yield stresses relative to
the other greyhound bones. It is possible that loading of the skeletal
elements of the feet during high-speed running in greyhounds roughly equals
that which typically occurs in dogs during fighting, such that these bones in
greyhounds need to have a high capacity to absorb energy. Indeed, the highest
rates of skeletal injury in greyhound during races occur in the bones of the
feet rather than the more proximal limb bones
(Prole, 1976;
Sicard et al., 1999
;
Johnson et al., 2000
).
Alternatively, the demands of high-speed running may constrain the mechanical
and shape properties of the distal elements to be lightly built for efficient
locomotion regardless of the specialization of the more proximal elements. The
similarity might also be due to a simple lack of genetic variation in the two
breeds for mechanical traits in these two bones. Whatever the explanation, the
mechanical properties of the long bones of the feet appear not to differ in
these two breeds.
The most dramatic differences we observed between the two breeds, in terms
of both amplitude and statistical significance, were the higher elastic moduli
of the greyhound bones and the higher work to fracture of the pit bull bones.
Our analysis did not address which aspects of the bone material account for
these differences between the breeds, and this issue warrants future
investigation. Nevertheless, differences observed in this study mirror those
that Currey (1979) found
between the femur of a cow and the antler of a deer. He suggested that because
male deer crash their antlers together with considerable force and speed, they
are loaded in impact and should therefore have a high work to fracture. By
contrast, he suggested that limb bones need to be stiff to function
effectively as levers and struts. Currey acknowledged that limb bones must
also bear large stresses and be resistant to impact but that, in general, the
danger of impacts is less in limb bones than in antlers because limb bones are
protected by muscle and skin. Although this is true, the results of this
analysis suggest that the physical demands of high-speed running influence the
evolution of limb bones differently than do the physical demands of
fighting.
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Acknowledgments |
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References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Biewener, A. A. (1990). Biomechanics of mammalian terrestrial locomotion. Science 250,1097 -1103.[Medline]
Blob, R. W. and Biewener, A. A. (1999). In vivo
locomotor strain in the hindlimb bones of Alligator mississippiensis
and Iguana iguana: implications for the evolution of limb bone safety
factor and non-sprawling limb posture. J. Exp. Biol.
202,1023
-1046.
Blob, R. W. and LaBarbera, M. (2001). Correlates of variation in deer antler stiffness: age, mineral content, intra-antler location, habitat, and phylogeny. Biol. J. Linn. Soc. 74,113 -120.[CrossRef]
Brear, K., Currey, J. D., Kingsley, M. C. S. and Ramsay, M. (1993). The mechanical design of the tusk of the narwhal (Monodon monoceros: Cetacea). J. Zool. Lond. 230,411 -423.
Carrier, D. R. (1996). Ontogenetic limits on locomotor performance. Physiol. Zool. 69,467 -488.
Clark, A. R. and Brace, A. H. (1995). The International Encyclopedia of Dogs. New York: Nowell Book House.
Cavagna, G. A. and Kaneko, M. (1977). Mechanical work and efficiency in level walking and running. J. Physiol. 268,467 -481.[Medline]
Cook, J., Cook, C. R., Tomlinson, J. L., Millis, D. L., Starost, M., Albercht, M. A. and Payne, J. T. (1997). Scapular fractures in dogs: epidemiology, classification, and concurrent injuries in 105 cases 1988-1994. J. Am. Anim. Hosp. Assoc. 33,528 -532.[Abstract]
Cornhill, J. F., Levesque, M. J., Herderich, E. E., Nerem, R. M., Kilman, J. W. and Vasko, J. S. (1980). Quantitative study of the rabbit aortic endothelium using vascular casts. Atherosclerosis 35,321 -337.[Medline]
Currey, J. D. (1979). Mechanical properties of bone with greatly differing functions. J. Biomech. 12,313 -319.[CrossRef][Medline]
Currey, J. D. (1987). The evolution of the mechanical properties of amniote bone. J. Biomech. 20,1035 -1044.[CrossRef][Medline]
Currey, J. D. (1989). Strain rate dependence of the mechanical properties of reindeer antler and the cumulative damage model of bone fracture. J. Biomech. 22,469 -475.[CrossRef][Medline]
Currey, J. D. (1999). The design of mineralized
hard tissues for their mechanical functions. J. Exp.
Biol. 202,3285
-3294.
Currey, J. D. and Pond, C. M. (1989). Mechanical properties of very young bone in the axis deer (Axis axis) and humans. J. Zool. Lond. 218, 59-67.
Fedak, M. A., Heglund, N. C. and Taylor, C. R. (1982). Energetics and mechanics of terrestrial locomotion: II. Kinetic energy changes of the limbs and body as a function of speed and body size in birds and mammals. J. Exp. Biol. 79, 23-40.
Gans, C. (1988). Adaptation and the form-function relation. Am. Zool. 28,681 -697.
Garland, T., Jr and Adolph, S. C. (1994). Why not to do two-species comparative studies: limitations on inferring adaptation. Physiol. Zool. 67,797 -828.
Gere, J. M. (2001). Mechanics of Materials. Pacific Grove, CA: Brokes/Cole Thomson Learning.
Gilchrist, J., Gotsch, K. and Ryan, G. (2003). Nonfatal dog bite-related injuries treated in hospital emergency departments - United States, 2001. Morb. Wkly Rep. 52,605 -610.
Heinrich, R. E., Ruff, C. B. and Adamczewski, J. Z. (1999). Ontogenetic changes in mineralization and bone geometry in the femur of muskoxen (Ovibos moschatus). J. Zool. Lond. 247,215 -223.
Hildebrand, M. and Goslow, G. (2001). Analysis of Vertebrate Structure. New York: John Wiley & Sons.
Hildebrand, M. and Hurley, J. P. (1985). Energy of the oscillating legs of a fast-moving cheetah (Acinonyx jubatus), pronghorn (Antilocapra americana), jackrabbit (Lepus californicus) and elephant (Elephas maximus). J. Morph. 184,23 -32.[CrossRef][Medline]
Hueck, I. S., Hollweg, H. G., Schmid-Schönbein, G. W. and
Artmann, G. M. (2000). Chlorpromazine modulates the
morphological macro- and microstructure of endothelial cells. Am.
J. Physiol. Cell Physiol. 278,C873
-C878.
Johnson, K. A., Muir, P., Nicoll, R. G. and Roush, J. K. (2000). Asymmetric adaptive modeling of central tarsal bones in racing greyhounds. Bone 27,257 -263.[CrossRef][Medline]
Kitchener, A. (1991). The evolution and mechanical design of horns and antlers. In Biomechanics and Evolution (ed. J. M. V. Rayner and K. J. Wooton), pp.229 -253. Cambridge: Cambridge University Press.
Lauder, G. V. (1991). An evolutionary perspective on the concept of efficiency: how does function evolve? In Efficiency and Economy in Animal Physiology (ed. R. W. Blake), pp. 169-184. Cambridge: Cambridge University Press.
Martin, R. B. and Burr, D. B. (1998). Skeletal Tissue Mechanics. New York: Springer-Verlag.
Maynard Smith, J., Burian, R., Kauffman, S., Alberch, P., Campbell, J., Goodwin, B., Lande, R., Raup, D. and Wolpert, L. (1985). Developmental constraints and evolution. Q. Rev. Biol. 60,265 -287.[CrossRef]
Pasi, B. M. and Carrier, D. R. (2003). Functional tradeoffs in the limb muscles of dogs selected for running versus fighting. J. Evol. Biol. 16,324 -332.[CrossRef][Medline]
Pellis, S. M. and Pellis, V. C. (1987). Play-fighting differs from serious fighting in both target of attack and tactics of fighting in the laboratory rat Rattus norvegicus. Aggressive Behav. 13,227 -242.
Pellis, S. M., Pellis, V. C. and McKenna, M. M. (1993). Some subordinates are more equal than others: play fighting among adult subordinate male rats. Aggressive Behav. 19,385 -393.
Phillips, I. R. (1979). A survey of bone fractures in the dog and cat. J. Small Anim. Pract. 20,661 -674.[Medline]
Pough, F. H., Janis, C. M. and Heiser, J. B. (1999). Vertebrate Life. New Jersey: Prentice Hall.
Prole, J. H. B. (1976). A survey of racing injuries in the greyhound. J. Small Anim. Pract. 17,207 -218.[Medline]
Sicard, G. K., Short, K. and Manley, P. A. (1999). A survey of injuries at five greyhound racing tracks. J. Small Anim. Pract. 40,428 -432.[Medline]
Sokal, R. R. and Rohlf, F. J. (1981). Biometry. New York: W. H. Freeman and Co.
Steudel, K. (1991). The work and energetic cost of locomotion: I. The effects of limb mass distribution in quadrupeds. J. Exp. Biol. 154,273 -286.
Swartz, S. M., Bennett, M. B. and Carrier, D. R. (1992). Wing bone stresses in free flying bats and the evolution of skeletal architecture in flying vertebrates. Nature 359,726 -729.[CrossRef][Medline]
Taylor, C. R. (1994). Relating mechanics and energetics during exercise. Adv. Vet. Sci. Comp. Med. A 38,181 -215.
Turner, C.H. (1993). Basic biomechanical measurements of bone: a tutorial. Bone 14,595 -608.[CrossRef][Medline]
Van Damme, R., Wilson, R. S., Vanhooydonck, B. and Aerts, P. (2002). Performance constraints in decathletes. Nature 415,755 -756.
Vanhooydonck, B., Van Damme, R. and Aerts, P. (2001). Speed and stamina trade off in lacertid lizards. Evolution 55,1040 -1048.[Medline]
Willems, P. A., Cavagna, G. A. and Heglund, N. C. (1995). External, internal and total work in human locomotion. J. Exp. Biol. 198,379 -393.[Medline]
Zioupos, P., Currey, J. D., Casinos, A. and De Buffrenil, V. (1997). Mechanical properties of the rostrum of the whale Mesoplodon densirostris, a remarkably dense bony tissue. J. Zool. London 241,725 -737.
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