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Differential sex-specific walking kinematics in leghorn chickens (Gallus gallus
domesticus) selectively bred for different body size
Running title: Sexual dimorphisms in chicken gait kinematics
Kayleigh A. Rose, Jonathan R. Codd and Robert L. Nudds*
Faculty of Life Sciences, University of Manchester, Manchester, M13 9PT, UK
* Address for reprints and other correspondence:
Dr. Robert Nudds
Faculty of Life Sciences
University of Manchester
Manchester M13 9PT, UK
E-mail: robert.nudds@manchester.ac.uk
Tel: +44(0)161 275 5447
KEY WORDS: Froude number; locomotion; posture; sexual dimorphism; walking
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Summary statement: In two size classes of layer chicken, sexually dimorphic
walking kinematics is linked to the differential muscle force, work and power
demands of varied visceral and muscle proportions
ABSTRACT
The differing limb dynamics and postures of small and large terrestrial animals may
be mechanisms for minimising metabolic costs under scale-dependent muscle force,
work and power demands; however, empirical evidence for this is lacking. Leghorn
chickens (Gallus gallus domesticus) are highly dimorphic: males have greater body
mass and relative muscle mass than females, which are permanently gravid and have
greater relative intestinal mass. Furthermore, leghorns are selected for standard (large)
and bantam (small) varieties and the former are sexually dimorphic in posture, with
females having a more upright limb. Here, high-speed videography and
morphological measurements were used to examine the walking gaits of leghorn
chickens of the two varieties and sexes. Hind limb skeletal elements were
geometrically similar among the bird groups, yet the bird groups did not move with
dynamic similarity. In agreement with the interspecific scaling of relative duty factor
(DF, proportion of a stride period that a foot has ground contact) with body mass,
bantams walked with greater DF than standards and females with greater DF than
males. Greater DF in females than in males was achieved via variety-specific
kinematic mechanisms, associated with the presence/absence of postural dimorphism.
Females may require greater DF in order to reduce peak muscle forces and minimize
power demands associated with lower muscle to reproductive tissue mass ratios and
smaller body size. Furthermore, a more upright posture observed in the standard, but
not bantam, females, may relate to minimizing the work demands of being larger and
having proportionally larger reproductive volume. Lower DF in males relative to
females may also be a work-minimizing strategy and/or due to greater limb inertia
(due to greater pelvic limb muscle mass) prolonging the swing phase.
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INTRODUCTION
The size of an animal influences its walking kinematics. When moving at the same
speed (U, m s-1) larger animals generally take longer and fewer strides per unit time
than smaller animals. Comparison of the walking kinematics of different sized
animals can be conducted at speeds at which the ratios of inertial to gravitational
forces acting upon the body centre of mass (CoM) are equal, using either the Froude
number (Fr = U2/ghhip) or its square root, often termed relative speed:
(1),
where hhip is hip height (m) and g is gravitational acceleration (9.81 m s-2) (Alexander,
1976; Alexander and Jayes, 1983). Dynamic similarity of motion between different
sized animals requires geometric similarity in body plan and equal values of
dimensionless kinematic parameters (scaled appropriately to negate the effects of
size) for a given relative speed (Alexander, 1976; Alexander and Jayes, 1983; Hof,
1996).
Animals may move in such a way as to minimize metabolic cost. The
metabolic cost of transport is the energy required to move a unit body weight over a
unit distance ([power]/body weight x speed). Geometrically similar animals of
different size moving in a dynamically similar fashion are expected to have equal
metabolic costs of transport (Alexander and Jayes, 1983). The dynamic similarity
hypothesis of Alexander and Jayes (1983) postulated that different quadrupedal
mammals would locomote with dynamic similarity at equivalent relative speeds.
Within non-cursorial (<1 kg) and cursorial (>10 kg) mammalian groups (Jenkins,
1971) the hypothesis was supported. Observed kinematic differences between the two
groups, however, were not accounted for (Alexander and Jayes, 1983). Furthermore,
between avian species of small and large body size, there is considerable deviation
from dynamic similarity of locomotion (Gatesy and Biewener, 1991; Abourachid and
Renous, 2000; Abourachid, 2001). A general pattern, however, exists across these
vertebrates, whereby smaller species move with greater relative duty factors (DF,
proportion of a stride with ground contact for any given foot) and relative stride
lengths. These deviations from dynamic similarity of locomotion have been attributed
to differences in the relative lengths of the limb segments and limb posture
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(Alexander and Jayes, 1983; Gatesy and Biewener, 1991; Abourachid and Renous,
2000; Abourachid, 2001). Crouched and upright limb postures are generally adopted
by small and large vertebrate species, respectively, which are clear departures from
geometric similarity in body form (Biewener, 1989; Gatesy and Biewener, 1991).
The differing gait kinematics and postures of small and large terrestrial
animals may be mechanisms for minimising metabolic costs under scale-dependent
muscle force, work and power demands; however, empirical evidence for this is
lacking. Body weight (l3 v1) increases at a faster rate with body size than the
strength (i.e. ability to resist forces, cross-sectional area l2 v2/3) of the biological
materials, which must support it (Biewener, 1989). An erect limb aligns body weight
with each limb bone’s long axis reducing mechanical loading on the muscles
associated with turning moments about the joints (Biewener, 1989). The ‘cost of
muscle force’ hypothesis for the scaling of limb posture and gait with body size states
that the more upright limbs of larger species serve to reduce the large forces that
would otherwise have to be exerted by the limb muscles (Biewener, 1989). An
alternative to the ‘cost of muscle force’ approach is that animals of differing size
optimise active muscle volume under scale-dependent muscle work and power
demands (Usherwood, 2013). A more erect limb requires shorter stance (push-off)
periods, reducing fore-aft speed fluctuations and, consequently, muscle work (J kg-1)
requirements (Usherwood, 2013). Although the same benefits of an upright limb (in
terms of reducing muscle work) would apply to smaller animals, theoretically, their
muscle power (J s-1 kg-1) requirements may be disproportionately high (Usherwood,
2013). Therefore, a more crouched limb, requiring a longer push-off period, may act
to minimise power requirements in smaller animals (Usherwood, 2013). Indeed, for a
given relative speed, human (Homo sapiens) toddlers were found to deviate more
from work-minimising gaits than adults, via longer relative stance periods (Hubel and
Usherwood, 2015).
The understanding of the gaits and postures of different sized animals is
compromised because the majority of comparisons are conducted between different
species (Alexander and Jayes, 1983; Gatesy and Biewener, 1991; Abourachid and
Renous, 2000; Abourachid, 2001). Intraspecifically, the sexes may differ not only in
body size (Lislevand et al., 2009; Remes and Szekely, 2010), but also in
morphological proportions, which are likely to influence muscle force, work and
power demands. For example, in many vertebrate species, the relative proportions of
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total body mass (Mb) allocated to different somatic and reproductive components are
usually biased towards males and females, respectively (Shine et al., 1998; Hammond
et al., 2000; Lourdais et al., 2006). Furthermore, female reproductive specialisation
may even require specific skeletal proportions (e.g. a wider pelvis (Baumel, 1953;
Smith et al., 2002; Cho et al., 2004)), or posture, during pregnancy (Franklin and
Conner-Kerr, 1998) or gravidity (Rose et al., 2015b). Most studies on gait kinematics,
however, have been conducted using either individuals of only one sex (Reilly, 2000);
without comparing sexes (Rubenson et al., 2004; Watson et al., 2011); or using
individuals whose sexes were not reported (Gatesy and Biewener, 1991; Abourachid,
2000; Abourachid and Renous, 2000; Abourachid, 2001; Griffin et al., 2004; Nudds et
al., 2010). Previous studies have identified sex differences in walking kinematics in
humans (Bhambhani and Singh, 1985) and two species of bird (Lees et al., 2012; Rose
et al., 2014), but whether size variations alone, or both size, and additional
unidentified sexual dimorphisms were behind the differences in kinematics was not
determined.
The leghorn chicken (Gallus gallus domesticus) is highly dimorphic, with
males having greater body size and muscle mass than females (Mitchell et al., 1931;
Rose et al., 2016a). Female leghorns have greater digestive organ masses than males
and remain permanently gravid (Mitchell et al., 1931). Furthermore, leghorns are
selectively bred for standard (large) and bantam (small) varieties, and only the
standard variety is sexually dimorphic in limb posture, with females possessing a
more upright limb than males at mid stance during a walking gait (Rose et al., 2015b).
For a given sex, the two varieties are expected to be closer to geometric similarity in
anatomical proportions (a prerequisite for dynamic similarity of motion). Whilst the
males of the two varieties are geometrically similar in their axial and appendicular
skeletons, the bantam males adopt a more upright posture at mid stance than the
standards during a walking gait (Rose et al., 2015a). The morphological variations to
have resulted from selective breeding in these leghorns provide a novel opportunity to
investigate the effects of limb posture and differing relative locomotor muscle,
digestive and reproductive tissue masses (i.e. varied muscle force, work and power
demands) on walking dynamics.
Here, high-speed videography and morphological measurements were used to
test the hypothesis that male and female standard and bantam varieties of leghorn
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would show clear departures from dynamic similarity of motion associated with their
morphological variations.
MATERIALS AND METHODS
Animals
Male and female bantam brown leghorns (B♂ and B♀) and standard breed white
leghorns (L♂ and L♀) were obtained from local suppliers and housed in the University
of Manchester’s Animal Unit. All leghorns (> 16 weeks < 1 year) had reached sexual
maturity and females were gravid. Sexes and varieties were housed separately with ad
libitum access to food, water and nesting space. Birds were trained daily for a week to
sustain locomotion for ~5 min within a Perspex® chamber mounted upon a Tunturi
T60 (Turku, Finland) treadmill. The kinematics of twenty-four of the twenty-eight
leghorns used for the simultaneously collected metabolic measurements described in
(Rose et al., 2015b) are presented here (B♂: N = 9; 1.39 ± 0.03 kg; B♀: N = 5; 1.04 ±
0.03 kg, L♂: N = 5; 1.92 ± 0.13 kg, L♀: N = 5; 1.43 ± 0.06 kg, mean ± s.e.m). All
experiments were approved by the University of Manchester’s ethics committee,
carried out in accordance with the Animals (Scientific procedures) Act (1986) and
performed under a UK Home Office Project Licence held by Dr Codd (40/3549).
Kinematics
The left greater trochanter of the hip of each bird was located by hand and any
overlying feathers were removed and replaced with a reflective marker. Each leghorn
was exercised at a minimum speed of 0.28 m s -1 and at increasing increments of 0.14
(in a randomised order), up to the maximum they could sustain without showing signs
of fatigue. The birds were rested between speed trials. All trials were filmed from a
lateral view (left of each bird) using a video camera (HDR-XR520VE, Sony, Japan,
100 frames s-1).
All video recordings were analysed using Tracker software (Open Source
Physics). Distance was calibrated for each video recording using a known distance
from the front to the back of the respirometry chamber. This allowed for the
alignment of a calibration tool through the line of travel of each bird (always passing
through digit 3), eliminating any error that could be incurred by a bird’s displacement
from it (i.e. the bird’s position on the treadmill/distance from the camera did not affect
our distance calibration). At each speed, the phasing of the sum of the vertical kinetic
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and gravitational potential energies with the horizontal kinetic energy of the body
centre of mass (approximated by the trochanter marker) was determined using spatial
and temporal data. Unlike the males, the female leghorns are either incapable or
unwilling to use grounded running gait mechanics (Rose et al., 2015b). Hence, only
data for speeds at which the birds used walking gait mechanics (out of phase
fluctuation of gravitational potential and horizontal kinetic energy) were used in the
analyses.
The left foot of each bird was tracked across ~10 continuous strides (constant
speed and position) to obtain the times of toe-on and toe–off, which were used to
calculate DF, stride frequency (fstride, Hz), stride length (lstride= U/fstride, m), swing
duration (tswing, s) and stance duration (tstance, s). A single fixed measure of hip height
(hhip) was used per individual (see the following morphological measurements section)
as the characteristic length for normalising their speed and gait kinematic parameters.
U was normalised for size differences as the square root of Froude, here termed
relative speed ( ). Kinematic parameters were normalised based on the
Hof (1996) record of non-dimensional forms of mechanical quantities as: relative
stride length ( = lstride/hhip); relative stride frequency ( ); relative
swing duration ( ); and relative stance duration (
).
Morphological measurements
For each experimental bird, hhip was measured from a video recording (accuracy, ± 1
mm) of a slow walking speed (0.28 m s-1) for a minimum of 7 strides. hhip was taken
(using the same method as Rose et al (2015a,b)) as the distance from the treadmill belt
(where digit one meets the base of the tarsometatarsus) to the hip marker at 90° to the
direction of travel during mid stance, when at its greatest. Back height (hback) was
measured the same way as hhip. Digital vernier callipers (accuracy, ± 0.01 mm) were
used to measure hind limb long bone (femur, tibiotarsus and tarsometatarsus) lengths
(lfem, ltib, ltars) and widths (wfem, wtib, wtars). Total leg length (Σlsegs) was calculated as the
sum of the three element lengths. Note that Σlsegs does not represent the true functional
length of the hindlimb, because the measurements were taken from dried bones
excluding the inter-joint soft tissue. The measurements were taken as the shortest
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distance between the most proximal and distal grooves of each element, which would
further decrease the values of Σlsegs relative to the maximum potential length of the
three leg segments if they were vertically aligned. Therefore, a posture index near the
value of 1.00 at mid stance in the present study is not indicative of a completely
upright limb. The width of the pelvis (wpelv = the distance between the left and right
acetabula) was also measured.
Soft tissue components from 5 experimental individuals of each bird group
were dissected and weighed upon electronic scales (accuracy, ± 0.01 g). Thirteen
major muscles of the right pelvic limb (m.iliotibialis cranialis, m. iliotibialis lateralis,
m. iliofibularis, m. flexor cruris lateralis pars pelvica, m. flexor cruris medialis, m.
iliotrochantericus caudalis, m. femerotibialis medialis, m. pubioischiofemoralis pars
lateralis, m. pubioischiofemoralis pars medialis, m. gastrocnemius pars lateralis, m.
gastrocnemius pars medialis, m. fibularis lateralis and m. tibialis cranialis) were
dissected for a sister study on variety- and sex-specific muscle architectural properties
(Rose et al., 2016a). The masses of these muscles were summed to give a comparable
total pelvic limb muscle mass between chicken groups. The right breast muscles (m.
pectoralis and m. supracoracoideus) and the intestines (small and large combined)
were also weighed. Reproductive mass (developing eggs, ovaries and oviduct) was
measured from female birds only and was assumed negligible in males in terms of
influencing locomotion dynamics. For the bantam females, 4 of the 5 reproductive
masses measured were from individuals whose experimental data were not included in
this present study. These individuals, however, were from the same cohort and
underwent the same training and experimental process as the birds for which
kinematic data are presented here. All anatomical components were compared
between varieties and sexes as a percentage of dead bird body mass.
Statistical analyses
All statistical analyses were conducted in R (v. 3.0.2 GUY 1.2 Snow Leopard build
558) (Team, 2011). The Car package (Fox and Weisberg, 2011) was used for all
analyses of variance (ANOVA) in which variety and sex were included as fixed
factors. Shapiro-Wilk tests were performed on the standardised residuals generated by
all statistical models to ensure the data conformed to a normal distribution. Where
morphological data (Table 1) did not conform to a normal distribution even after log
transformation, a Kruskal Wallis test was conducted to compare the means of the four
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groups: B♂, B♀, L♂, and L♀. Dunn post-hoc tests were used to indicate which groups
differed. The relationships between absolute and relative kinematics variables with U
and were compared between the bird groups using linear models. U and were
included in the models as covariates and all potential interaction terms were
considered before a stepwise backwards deletion of non-significant interaction terms
was conducted to simplify the models. Outputs from the final models are reported.
Best-fit lines were obtained from the coefficients tables of the final statistical models
and were back transformed where data had been log transformed.
RESULTS
Morphological measurements
Body mass (Fig 1A) and total leg length (Σlsegs, Fig 1B) were greater in the standard
than in the bantam variety and greater in males than females (Table 1). Hip height
(hhip, Fig 1C), however, was greater in males than in females in the bantam variety,
but, conversely, greater in females than in males in the standard variety (Table 1).
Posture index (hhip:Σlsegs, Fig 1D) did not differ between the sexes of the bantam
variety. In contrast, the posture index of L♀ was ~27 % greater than that of L♂,
indicative of a more erect limb (Table 1).
Each hind limb segment was a similar proportion of Σlsegs (Table 2) in all of
the leghorn groups excluding B♀, which had a relatively longer lfem, and concomitantly
shorter ltars, resulting in a small, but, nonetheless statistically significant difference
(Table 2). The width of each limb segment (Table 2) was a similar proportion of its
respective segment length in all groups (Table 2). The finding of a more erect posture
in L♀ when compared to the other three groups was further supported by indices
incorporating the height of the back (hback). hhip:hback did not differ between the bird
groups, and Σlsegs:hback was lower in L♀ than in the other three leghorn groups (Table
2). wpelv, relative to Σlsegs (Table 2), did not differ between the sexes, but was ~1 %
greater in the bantams than in the standards (Table 2).
Total pelvic limb muscle mass (the sum of the masses of thirteen pelvic limb
muscles) was a greater % of body mass (Fig 2) in males than in females in both
varieties (Table 1). Total pelvic limb muscle mass was also greater in the bantam than
in the standard variety (Fig 2, Table 1). The observed differences between varieties,
however, were small in comparison to the sexual dimorphisms. The same statistical
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outcomes obtained for the total pelvic limb muscle mass were mirrored by the breast
muscles, m. pectoralis and m. supracoracoideus (Fig 2, Table 1). Intestine mass as a
proportion of body mass (Fig 2) was greater in females than in males (Table 1). The
two varieties, however, shared similar relative intestinal masses. The reproductive
tissue mass as a percentage of body mass was greater in L♀ (11.49 ± 0.56 %) than in
the B♀ (8.40 ± 0.08 %).
Therefore, all four leghorn groups were similar in their hind limb skeletal bone
geometry (a prerequisite of dynamic similarity of locomotion). The sexes, however,
differed markedly in each of the measured anatomical masses when expressed as %
body mass. In contrast, with the exceptions of limb posture and the relative mass of
the female reproductive system, for a given sex, the two varieties of leghorn were
more similar in their anatomical proportions.
Walking kinematics and dynamics
DF, tswing and tstance were negatively correlated, and lstride and fstride were positively
correlated with U. The same correlations were also found for the relationship between
size-normalised kinematics parameters and . For all four groups of leghorns, the
exponents describing the relationships between absolute or size-normalised
parameters and U or were similar, unless otherwise stated below.
Across all speeds, DF (Fig 3A) was greater in females than in males (~ 2 %)
and greater in the bantam than in the standard variety by ~ 2 % (Table 3). At
comparable , DF was, similarly, greater in females than in males in both varieties
and this sex difference was greater in the bantams. In addition, DF was greater in the
bantam than in the standard variety (Fig 3B; Table 3).
fstride (Fig 3C) was greater in females compared to males at any given U (0.11
Hz) (Table 3). Absolute fstride and the rate of increase in fstride with U were significantly
greater in the bantam than in the standard variety. At comparable , , was greater
in females compared to males in the standard variety but, contrastingly, greater in
males compared to females in the bantam variety (Fig 3D; Table 3).
At any given U, lstride was greater in males than in females by a greater amount
in the standard variety (70 mm) than in the bantam variety (20 mm) (Fig 1C; Table 2)
and was associated with a greater difference between the males of the two varieties
than between the females of the two varieties. At any given , (Fig 1D), was
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greater in females than in males in the bantam variety, but, contrastingly, was greater
in males than in females in the standard variety (Table 3).
At each U, tswing (Fig 1G) was greater in males than in females and this
difference was lower in the bantam (0.02 s) than in the standard (0.04 s) variety
(Table 2). In the bantams, swing (Fig 1H), was similar in the two sexes, whilst in the
standard variety, it was significantly greater in males compared to females at a given
.
tstance (Fig 1I) was similar in B♂ and B♀, but was greater in L♂ compared to L♀
by 0.03s at all U (Table 2). Across all , stance (Fig 1J; Table 2) was greater in B♀
than in B♂, yet lower in L♀ than in L♂.
Therefore, none of the sex or variety differences in gait kinematics were
accounted for correcting for body size differences. The two varieties differed in the
mechanisms by which females had elevated DF relative to males. In the bantams,
females had relatively longer stance durations than males (Fig 1J) and the sexes
shared similar swing dynamics (Fig 1H). In the standard variety, females had
relatively shorter swing and stance durations than males, but the sex difference in
swing was much greater than that in stance (Fig 1H and J).
DISCUSSION
This study represents the first detailed comparison of the gait of the sexes in any
species. Leghorn chickens, although all similar in their hind limb segment geometry,
show considerable variation in limb posture and the relative contributions of
anatomical components (skeletal muscle, digestive organs and reproductive tissues) to
total body mass. In association with these morphological differences, and in
agreement with our hypothesis, none of the leghorn groups walked with dynamic
similarity.
Incremental responses of absolute kinematics parameters to increasing U are
generally greater in smaller species (Gatesy and Biewener, 1991). With the exception
of fstride, which increased at a faster rate in bantams than in the standard variety, all
birds in the present study, however, showed similar incremental kinematic responses
to U, despite the size differences associated with sex and variety. Most of the sex
differences in absolute kinematic parameters paralleled inter-species differences,
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associated with body size (Gatesy and Biewener, 1991). In females of the two
varieties, fstride was greater, and lstride, tswing and tstance, smaller, at any given U compared
to that in their conspecific males, which had greater body size (except for tstance in the
bantams, which was similar between the sexes). Similarly, fstride was greater, and lstride,
tswing and tstance shorter at any given U in the bantams compared to the standards. The
only parameter that was not comparable to inter-species patterns associated with body
size for a given absolute speed was DF. Interspecific scaling patterns, would predict
the heavier and longer-legged, animal to have a greater DF than the lighter, shorter-
legged one, at the same U (Gatesy and Biewener, 1991). In contrast, here, females
walked with greater DF than males, and bantams walked with greater DF than
standards.
In agreement with body size dependent inter-species differences in DF
measured at equivalent relative speeds (Alexander and Jayes, 1983; Gatesy and
Biewener, 1991), at any given relative speed, DF here, was still higher in the smaller
bantam relative to the standard variety, and in females relative to males. Deviations
from dynamic similarity of motion with increasing body mass are usually associated
with increasing limb erectness, i.e., an increasing hhip to Σlseg ratio (Biewener, 1987,
1989; Gatesy and Biewener, 1991). Smaller, more crouched, species can achieve
greater lstride relative to their hhip because they can extend the crouched limb, which in
turn, allows a greater DF (Gatesy and Biewener, 1991). In contrast, a more erect limb
is constrained in terms of the range of lstride and DF it can achieve, relative to a given
hhip (Gatesy and Biewener, 1991). The similar pelvic limb skeletal geometry of the
birds in the present study provides a control for the potential effects of limb segment
proportions on walking dynamics and allows investigation into the potential
influences of additional morphological characteristics including limb posture. Despite
L♀ having the most upright limbs, and the lowest relative stride lengths (Fig 1 E),
however, they still produced a greater DF relative to hhip than did the L♂, whose limbs
were more crouched. Furthermore, since sexual dimorphism in limb posture was
exclusive to the standards, limb posture cannot explain the similar sex difference in
DF in the two varieties. The sexual dimorphism in posture in the standard variety only
was reflected in the opposite sex-specific dynamics of , , swing and stance at any
given between the two varieties (i.e the sex differences in gait were variety-
specific, yet ultimately led to greater DF in females than males). The lower in L♀
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than in B♀ and higher in L♀ than in B♀ are consistent with the general consensus
that a more upright limb limits the length of a step relative to hhip (Gatesy and
Biewener, 1991).
By adopting a more upright limb posture, larger animals reduce the forces that
the muscles must exert and that the bones must resist to counteract joint moments,
which would otherwise scale geometrically ( Mb1/3) (Biewener, 1989). Until recently,
this has been considered the principal reason for the scaling of limb posture and gaits
in vertebrates (Biewener, 1989). Why smaller animals do not also have upright limbs
so that they could have relatively more gracile and lighter bones, however, is not
accounted for by this explanation. Explanations proposed to account for a more
crouched limb include that it may improve manoeuvrability (Biewener, 1989) stability
(Gatesy and Biewener, 1991) or minimize the cost of work associated with bouncing
viscera (Daley and Usherwood, 2010). Another potential explanation, however, is that
animals optimise muscle mechanical work and power demands during push-off
(which are scale-dependent) in order to minimise the volume of active muscle for a
given size (Usherwood, 2013). In this case, a crouched limb at mid stance (allowing
longer DF) for small animals may serve to reduce power demands (which are high
because at any given U shorter legs require quicker stances), whilst a more upright
limb suits the work demands of being large (which are high because a
disproportionate amount of body weight must be supported).
The females in the present study may, therefore, benefit from greater DF,
which would decrease the elevated power demands associated with having small
limbs, yet greater body weight to support per unit of muscle mass because of
gravidity. The L♀ in the present study may have adopted kinematic and postural
mechanisms for reducing both the elevated work demands due to gravity (via upright
limbs) and the power demands of being small (via longer DF, achieved without a
crouched posture). It is possible that L♀ may require a more upright limb than B♀
because of their greater relative reproductive tissue mass. In B♀ minimising power via
a greater relative DF (exceeding that in L♀) appears to be more important. In guinea
fowl, Numida meleagris, adding trunk loads equivalent to 23% of body mass did not
affect tswing but led to a 4% increase in tstance (Marsh et al., 2006). In several additional
avian species, however, no changes in gait kinematics were associated with the
application of trunk loads (McGowan et al., 2006; Tickle et al., 2010; Tickle et al.,
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2013). These experiments, however, involve unnatural loads applied in backpacks and
may not represent a true gravid loading condition. The hypothesis that the kinematics
of leghorn hens are influenced by muscle mechanical demands associated with
gravidity is further supported by the finding than DF increases with the onset of egg
laying during sexual maturation in leghorn hens (Rose et al., 2016b). Equally, males
may benefit from lower DF via the minimization of work demands associated with
changes in fore-aft acceleration and deceleration, because of being larger.
The hypothesis of Usherwood (2013), that animals adopt kinematic and
postural mechanisms to minimise active muscle volume (according to work and
power demands) in order to minimize metabolic costs is supported by the present
findings together with previously published data on locomotor energy metabolism
collected simultaneously from the same birds (Rose et al., 2015a,b). The metabolic
cost of transport in gravid female leghorns is in fact lower than allometric predictions
based on body mass (Vankampen, 1976; Rose et al., 2015b) and also lower than that
of male leghorns (Rose et al., 2015b), which can be linked to their comparatively
greater DF. A lower metabolic cost of transport in L♀ than in B♀ (Rose et al., 2015b)
can also be linked to more upright limbs. Additionally, greater relative DF and more
upright limb posture may contribute to a lower than expected metabolic cost of
transport in B♂ for their body mass and the lack of scaling in the metabolic cost of
transport between males of the two varieties (Rose et al., 2015a).
Alternatively/additionally, the greater DF in females relative to males may be
a mechanism for reducing peak muscle forces in supporting body weight, which may
again be particularly important when carrying proportionally more weight (due to
greater digestive/reproductive tissue volume) with proportionally less muscle volume.
Furthermore, chickens artificially selected for egg production are well known to suffer
from osteoporosis associated with the utilisation of calcium from limb bone medullary
in order to form egg-shells (Dacke et al., 1993; Whitehead, 2004). A greater
proportion of ground contact throughout the stride to reduce peak forces exerted on
the bones may reduce the risk of bone fracture. This argument may be particularly
pertinent to L♀ due to the fact that the pelvic limb skeletal element diameters of the
two varieties conformed to geometric, and not elastic (positive allometry), scaling as
is found between species (Doube et al., 2012). The bones of L♀ are, therefore, not
expected to be any more robust than those of B♀ to assist with supporting
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proportionally more weight of the reproductive system. The same reasoning may also
explain the upright limbs of L♀.
It is also possible that additional sexual dimorphisms, perhaps in muscle
physiology or morphology, are linked to the sex differences in dynamics. For
example, simply the distribution of mass across the limb segments may be
responsible. In a recent study in which the swing phase kinematics of different
charadriiform birds were compared, Northern lapwings (Vanellus vanellus) and
Eurasian oystercatchers (Haematopus), which share similar hind limb long bone
proportions, shared similar tswing at any given speed despite oystercatchers having
longer and heavier limbs overall (Kilbourne et al., 2016). In comparison to these two
species, pied avocets (Recurvirostra avosetta) moved with longer swing durations at
higher speeds linked to a more distal concentration of hind limb mass (Kilbourne et
al., 2016). The greater relative pelvic limb muscle mass in males, relative to females
(Mitchell et al., 1931; Rose et al., 2016a), may similarly increase limb moment of
inertia and prolong the swing phase of the limb, increasing its contribution to the
stride period.
In summary, this study represents the first detailed comparison of male and
female gait in a bird. Clear departures from dynamic similarity of motion were
evident between the sexes in standard and bantam varieties of leghorn chicken.
Females walked with greater DF than males at any given relative speed, but this sex
difference was achieved through alternative kinematic mechanisms in each variety
and linked to variety differences in sex-specific posture. L♀ carry a greater relative
reproductive mass than B♀ and potentially represent the first documented example of
an animal adopting mechanisms for minimising the demands of both work (via an
upright limb, relative to B♀) and power (via a longer DF than their heavier, more
crouched male conspecifics).
List of abbreviations
B♀ female bantams
B♂ male bantams
DF duty factor
fstride stride frequency
Fr Froude number
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normalised stride frequency
lfem femur length
lstride stride length
hhip hip height
hhip: Σlsegs posture index
L♀ female standards
L♂ male standards
normalised stride length
ltib tibiotarsus length
ltars tarsometatarsus length
tstance stance duration
stance normalised stance duration
tswing swing duration
swing normalised swing duration
U speed
relative speed
wfem femur width
wtib tibiotarsus width
wtars tarsometatarsus width
Σlsegs sum of the hind limb long bone lengths
Competing interests
The authors have no competing interests
Author’s contributions
R.L.N, J.R.C and K.A.R designed the study and contributed to the manuscript. K.A.R
conducted the experiments and statistical analyses with advice from R.L.N and J.R.C.
Funding
This research was funded by the BBSRC (G01138/1 and 10021116/1 to J.R.C).
K.A.R was supported by a NERC DTA stipend and CASE partnership with the
Manchester Museum.
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Figure Legends
Figure 1. Morphological measurements for the variety and sex combinations of
leghorn chicken. (a) Body mass. (b) Total leg length (sum of the three skeletal
element lengths). (c) Hip height. (d) Posture index (hip height: total leg length). Bars
represent means ± s.e.m for standard males (grey), standard females (purple), bantam
males (blue) and bantam females (red). Significant variety, sex and variety x sex
interaction terms are denoted by V, S and I, respectively. Significance levels of 0.05,
0.01 and 0.001 are denoted by *, ** and ***, respectively. Results of the two way
ANOVAs conducted to test for variety and sex differences are in Table 1. These
morphological differences have been reported previously in (Rose et al., 2015b) for a
different sample size.
Figure 2. Anatomical components as a % of body mass for the variety and sex
combinations of leghorn chicken. Bars represent means ± s.e.m for standard males
(grey), standard females (purple), bantam males (blue) and bantam females (red).
Limb muscle mass was calculated as the sum of thirteen major pelvic limb muscles on
the right limb. M. pectoralis and M. supracoracoideus expressed as a % of body mass
are for the right side of the body only. Reproductive mass was assumed negligible in
the males in terms of influencing gait. Significant variety and sex effects are denoted
by V and S, respectively. Significance levels of 0.05, 0.01 and 0.001 are denoted by
*, ** and ***, respectively. Results of the one- and two-way ANOVAs conducted to
test for variety and sex differences are in Table 1.
Figure 3. Absolute gait kinematics parameters versus speed (left column) and
relative gait kinematics parameters versus relative speed (right column). Duty
factor (a-b), stride length (c-d), stride frequency (e-f), swing duration (g-h) and stance
duration (i-j). Each data point (standard males = grey circles, standard females =
purple crosses, bantam males = blue circles and bantam females = red crosses)
represents a single trial for an individual bird. Best-fit line equations and the results of
the linear models conducted to test for variety and sex differences are in Table 3.
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Table 1. Results of the one- and two-way ANOVAs that tested for variety and sex differences in morphological measurements/indices.
Measurement/index ANOVA (final model)Body mass(kg)
variety: F1,20= 47.34, P<0.001,sex: F1,20=33.96, P<0.001R2= 0.76
Leg length(mm)
variety: F1,20=125.26, P<0.001,sex: F1,20=84.44, P<0.001R2= 0.89
Hip height(mm)
variety: F1,19=95.44 P<0.001,sex: F1,19=0.29, P=0.594variety x sex: F1,19=29.55, P<0.001,R2= 0.85
Posture index variety: F1,19=14.42, P=0.001,sex: F1,19=19.44, P<0.001variety x sex: F1,19=42.30, P<0.001,R2=0.75
13 pelvic limb muscles(%body mas)
variety: F1,17=9.10, P=0.008,sex: F1,17=161.53, P<0.001, R2=0.90
M. pectoralis(% body mass)
variety: F1,17=18.50, P<0.001sex: F1,17=31.00, P<0.001, R2=0.71
M. supracoracoideus(%body mass)
variety: F1,17=8.35, P=0.010sex: F1,17=29.01, P<0.001, R2=0.65
Intestines a
(%body mass)variety: F1,16=0.71, P=0.411,sex: F1,16=48.09, P<0.001, R2=0.73
Reproductive(%body mass) b
variety: F1,8= 8.74, P=0.018,R2 = 0.46
a N=4 for standard malesb Females only as reproductive mass was assumed negligible in malesBody mass, leg length, hip height and posture index were measured from the full sample of experimental birds Soft tissue masses (% body mass) were calculated for 5 individuals of each bird groupBreast muscle %body masses are for the right side of the body onlyThe adjusted R2 values of the final statistical models are reported
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Table 2. Mean (± s.e.m) morphometric indices and results of the statistical tests conducted to investigate whether the indices differed between varieties and sexes.
Index B♂ B♀ L♂ L♀ Statistical resultslfem:Σlsegs 0.28 0.29 0.28 0.28 Kruskal Wallis: X2= 19.6, df=3, P=<0.001
Dunn test: B♂ v B♀: Z=3.71, P<0.001, B♂ v L♂: Z=-0.61, P=0.272, B♂ v L♀: Z=0.00, P=0.500, B♀ v L♂: Z=-3.89, P<0.001, B♀ v L♀: Z=-3.35, P<0.001, L♂ v L♀: Z=0.55, P=0.292
ltib:Σlsegs 0.42 0.42 0.42 0.42 Kruskal Wallis: X2= 0.13, df=3, P=0.988ltars:Σlsegs 0.30 0.29 0.30 0.30 Kruskal Wallis: X2= 12.47, P=0.006
Dunn test B♂ v B♀: Z=-2.48, P=0.007, B♂ v L♂: Z=0.90, P=0.18 B♂ v L♀: Z=0.90, P=0.18, B♀ v L♂: Z=3.05, P=0.001, B♀ v L♀: Z=3.05, P=0.001, L♂ v L♀: Z=0.00, P=0.500
wfem:lfem 0.11 0.11 0.11 0.11 Kruskal Wallis: X2= 0.46, df=3, P=0.929wtib:ltib 0.07 0.06 0.07 0.07 Kruskal Wallis: X2= 7.20, df=3, P=0.066wtars:ltars 0.10 0.10 0.10 0.10 Kruskal Wallis: X2= 0.36, df=3, P=0.948hhip:hback 0.78 ±
0.010.77 ± 0.02
0.76 ± 0.00
0.77 ± 0.02
variety: F1,20=0.45, P=0.512, sex: F1,20=0.00, P=0.948, R2=0.00
Σlsegs:hback 1.01 ± 0.03
1.02 ± 0.02
1.03 ± 0.01
0.76 ± 0.02
variety: F1,19=20.58, P<0.001, sex: F1,19=22.16, P<0.001, variety x sex: F1,19=37.91, P<0.001, R2=0.78
wpelv:Σlsegs 0.17 (N=6)
0.18 0.16 0.17 variety: F1,18=11.368, P=0.003, sex: F1,18=0.347, P=0.079, R2=0.39
The adjusted R2 values of the final models are reported.Only the results of the final two-way ANOVAs are reportedStandard errors are not presented where they were 0.00 to 2 decimal placesThe sample size is indicated in brackets if lower than the total sample size of the leghorn group
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Table 3. Results of the linear models that tested for sex differences in absolute/normalised kinematics with speed.
The adjusted R2 values of the final statistical models are reporte
Parameter Final model Lines of best fitDF U (F1,111=315.80, P<0.001),
variety (F1,111=7.38, P=0.008),sex (F1,111=27.79, P<0.001),R2= 0.79
B♂ : = -0.16U+0.79B♀: = -0.16U+0.81L♂: = -0.16U + 0.77L♀: = -0.16U+0.79
DF (F1,110=276.78, P<0.001),variety (F1,110=30.71, P<0.001),sex (F1,110=25.30, P<0.001),variety x sex (F1,110=5.58, P=0.020),R2= 0.77
B♂ : = -0.23 + 0.79
B♀: = -0.23 + 0.82
L♂: = -0.23 + 0.77
L♀: = -0.23 + 0.78fstride U (F1,110=706.18, P<0.001),
variety (F1,110=204.13, P<0.001),sex (F1,110=24.64, P<0.001),U x variety (F1,110=16.74, P=<0.001),R2= 0.87
B♂ : = 1.76U+ 0.69B♀: = 1.76U+ 0.80L♂: = 1.24U+ 0.61L♀: = 1.24U+ 0.72
(F1,110=615.06, P<0.001),variety (F1,110=1.32, P=0.253),sex (F1,110=26.84, P<0.001),variety x sex (F1,110=80.66, P<0.001),R2= 0.87
B♂ : = 0.30 + 0.12
B♀: = 0.30 + 0.10
L♂: = 0.30 + 0.08
L♀: = 0.30 + 0.13log lstride logU (F1,110=662.71, P<0.001),
variety (F1,110=222.07, P<0.001),sex (F1,110=40.77, P<0.001),variety x sex (F1,110=10.93, P=0.001),R2= 0.92
B♂ : = 0.43U0.46
B♀: = 0.41U0.46
L♂: = 0.56U0.46
L♀: = 0.49U0.46
log log (F1,110=663.00, P<0.001),variety (F1,110=0.03, P=0.862),sex (F1,110=52.48, P<0.001),variety x sex (F1,110=151.57 P<0.001),R2= 0.88
B♂ : = 2.50 0.23
B♀: = 2.78 0.23
L♂: = 2.95 0.23
L♀: = 2.30 0.23
log tswing logU (F1,110=94.88, P<0.001),variety (F1,110=225.41, P<0.001),sex (F1,110=71.69, P<0.001),variety x sex (F1,110=4.51, P=0.036),R2= 0.73
B♂ : = 0.16U-0.22
B♀: = 0.14U-0.22
L♂: = 0.22U-0.22
L♀: = 0.18U-0.22
log log (F1,110=97.77, P<0.001),variety (F1,110=40.02, P<0.001),sex (F1,110=77.88, P<0.001),variety x sex (F1,110=57.83, P<0.001),R2= 0.69
B♂ : = 1.04 -0.11
B♀: = 1.04 -0.11
L♂: = 1.31 -0.11
L♀: = 1.00 -0.11
log tstance logU (F1,110=1431.42, P<0.001),variety (F1,110=214.12, P=0.079),sex (F1,110=22.35, P<0.001),variety x sex (F1,110=13.76, P<0.001),R2= 0.93
B♂ := 0.28U-0.64
B♀: = 0.28U-0.64
L♂: = 0.36U-0.64
L♀: = 0.33U-0.64
log log (F1,110=1057.41, P<0.001),variety (F1,110=1.85, P=0.177),sex (F1,110=17.74, P<0.001),variety x sex (F1,110=126.77, P<0.001),R2= 0.92
B♂ : = 1.60 -0.32
B♀: = 1.85 -0.32
L♂: = 1.85 -0.32
L♀: = 0.47 -0.32
720721722723
725
726
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