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Apparent density of the primate calcaneo-cuboid joint and its association with locomotor mode foot posture and the Уmidtarsal breakФ.

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 142:180–193 (2010)
Apparent Density of the Primate Calcaneo-Cuboid Joint
and Its Association With Locomotor Mode, Foot
Posture, and the ‘‘Midtarsal Break’’
Matthew G. Nowak,1* Kristian J. Carlson,2,3 and Biren A. Patel4
1
Department of Anthropology, Southern Illinois University, Carbondale, IL 62901-4502
Institute for Human Evolution, University of the Witwatersrand, WITS 2050, Johannesburg, South Africa
3
Department of Anthropology, Indiana University, Bloomington, IN 47405-7100
4
Department of Anatomical Sciences, Stony Brook University, Stony Brook, NY 11794-8081
2
KEY WORDS
longitudinal arch; quadrupedal; suspensory; bipedal; plantigrade
ABSTRACT
Primates use a range of locomotor
modes during which they incorporate various foot postures. Humans are unique compared with other primates
in that humans lack a mobile fore- and midfoot. Rigidity
in the human foot is often attributed to increased propulsive and stability requirements during bipedalism.
Conversely, fore- and midfoot mobility in nonhuman primates facilitates locomotion in arboreal settings. Here,
we evaluated apparent density (AD) in the subchondral
bone of human, ape, and monkey calcanei exhibiting different types of foot loading. We used computed tomography osteoabsorptiometry and maximum intensity projection (MIP) maps to visualize AD in subchondral bone at
the cuboid articular surface of calcanei. MIPs represent
3D volumes (of subchondral bone) condensed into 2D
images by extracting AD maxima from columns of voxels
comprising the volumes. False-color maps are assigned
to MIPs by binning pixels in the 2D images according to
brightness values. We compared quantities and distributions of AD pixels in the highest bin to test predictions
relating AD patterns to habitual locomotor modes and
foot posture categories of humans and several nonhuman
primates. Nonhuman primates exhibit dorsally positioned high AD concentrations, where maximum compressive loading between the calcaneus and cuboid likely
occurs during ‘‘midtarsal break’’ of support. Humans exhibit less widespread areas of high AD, which could
reflect reduced fore- and midfoot mobility. Analysis of
the internal morphology of the tarsus, such as subchondral bone AD, potentially offers new insights for evaluating primate foot function during locomotion. Am J Phys
Anthropol 142:180–193, 2010. V 2009 Wiley-Liss, Inc.
Diagnostic functional morphology of a biped foot provides a critical tool for interpreting locomotor and postural capacities of bipedal and nonbipedal fossil forms
(Morton, 1922, 1924a,b; Weidenreich, 1923; Elftman and
Manter, 1935a,b; Day and Napier, 1964; Day and Wood,
1968; Bojsen-Møller, 1979; Oxnard and Lisowski, 1980;
Gomberg, 1981; Stern and Susman, 1983; Susman, 1983;
Deloison, 1985; Lamy, 1986; Langdon, 1986; Latimer and
Lovejoy, 1989, 1990a,b; Lewis, 1989; Clarke and Tobias,
1995; Kidd et al., 1996; Kidd, 1999; Aiello and Dean,
2002; Harcourt-Smith, 2002; Berillon, 2003; HarcourtSmith and Aiello, 2004; Wang and Crompton, 2004; Gebo
and Schwartz, 2006; Klenerman and Wood, 2006;
DeSilva, 2009, in press; Griffin and Richmond, in press).
Relative to all other primates, the modern human foot is
functionally and morphologically distinct (Lewis, 1980,
1981, 1989; Langdon, 1986; Gebo, 1992, 1993b; Aiello
and Dean, 2002; Klenerman and Wood, 2006). The lack
of a mobile fore- and midfoot and the presence of a longitudinal arch in humans, both emphasizing propulsion
and stability at the expense of grasping ability, are traits
commonly attributed to the evolution of bipedalism in
humans. Nonhuman anthropoid primates are an ideal
group against which the uniqueness of the human foot
can be evaluated because of the diversity of locomotor
and postural modes (Hunt et al., 1996) as well as pedal
contact types (e.g., digitigrade [DG], semiplantigrade
[SP], and plantigrade [P]) that nonhuman primates exhibit while negotiating highly variable arboreal and terrestrial environments (Meldrum, 1991, 1993; Gebo, 1992,
1993a,b; Schmitt and Larson, 1995; Vereecke et al.,
2003).
Many comparative studies have focused on internal
morphological properties of human, nonhuman primate,
and nonprimate mammalian bones in order to interpret
loading history among animals with different locomotor
and postural behaviors (Eckstein et al., 1992, 1993,
1994, 1995; Müller-Gerbl et al., 1992; Skedros et al.,
1994a,b, 1997, 2001, 2004, 2007; Biewener et al., 1996;
Swartz et al., 1998; Ahluwalia, 2000; Fajardo and
Müller, 2001; MacLatchy and Müller, 2002; Ryan and
van Rietbergen, 2005; Carlson and Patel, 2006; Maga et
al., 2006; Patel and Carlson, 2007, 2008; Polk et al.,
2008, 2009). The material properties of mammalian calcanei, in particular, have been shown to correlate with
principal locomotor stresses (both compressive and tensile) (von Meyer, 1867; Thompson, 1917; Ward and Suss-
C 2009
V
WILEY-LISS, INC.
C
Grant sponsor: National Science Foundation; Grant number:
BCS-0524988; Grant sponsor: L.S.B. Leakey Foundation.
*Correspondence to: Matthew G. Nowak, Department of Anthropology, Southern Illinois University, Carbondale, IL 62901-4502.
E-mail: mnowak@siu.edu
Received 28 August 2008; accepted 4 September 2009
DOI 10.1002/ajpa.21210
Published online 16 November 2009 in Wiley InterScience
(www.interscience.wiley.com).
PRIMATE CALCANEO-CUBOID JOINT
man, 1979; Bacon et al., 1984; DeRousseau, 1988; Jensen
et al., 1991; Skedros et al., 1994a,b, 1997, 2001, 2004,
2007; Fernandez Camacho et al., 1996; Gefen and Seliktar, 2004; Maga et al., 2006); however, no study has
quantified how loading history is related to joint subchondral bone structure in the calcaneus. Recently, the
method of computed tomography osteoabsorptiometry
(CT-OAM) has been used to infer joint loading history in
humans, apes, and monkeys via quantification of radiodensities in subchondral cortical bone underlying the
articular surface of the proximal tibia (Ahluwalia, 2000)
and distal radius (Carlson and Patel, 2006; Patel and
Carlson, 2007, 2008). Using these same methods, the
goal of this study was to investigate subchondral bone
morphology in the primate calcaneocuboid joint in order
to evaluate several predictions relating internal morphological specializations to patterns in primate midfoot
function and loading regimes.
Habitual locomotor behaviors (e.g., bipedalism, suspensory, and quadrupedalism) significantly influence pedal
anatomy, because these different locomotor modes incorporate different compressive loading regimes. In general,
primate hind limb joints can be subjected to variable
degrees of compressive loading during locomotion
depending on 1) body mass support and 2) muscle–tendon complexes. Relative to forelimb joints, hind limb
joints of both quadrupeds and bipeds are likely subjected
to relatively higher compressive forces because the hind
limbs habitually support either the majority of body
mass (e.g., quadrupedal primates) or all of the body
mass (e.g., bipedal humans) during locomotion (e.g.,
Demes et al., 1994), plus compressive loading due to
muscle–tendon complexes crossing the joints. In contrast, suspensory primates (e.g., Hylobates and Pongo)
theoretically load their hind limbs with relatively lower
compressive forces because hind limb involvement in terrestrial or above-branch support of body mass comprises
a comparatively smaller amount of their locomotor repertoire (Fleagle, 1976, 1980; Thorpe and Crompton, 2006).
Thus, for suspensory primates, compressive forces of
muscle–tendon complexes likely figure prominently in
the hind limb compressive loading regime.
During bipedalism and quadrupedalism, where compressive forces in hind limb joints should be high, primate feet exhibit a range of contact points at the beginning of stance phase. According to Schmitt and Larson
(1995), DG primates initiate hind limb contact through
their metatarsal heads following swing phase. SP primates initiate hind limb contact at touchdown using a comparatively greater extent of the plantar surface than DG
primates, but, similar to DG primates, they still avoid
heel contact (Fig. 1) (Schmitt and Larson, 1995). Plantigrady, or heel contact, can be subdivided into ‘‘midfoot/
heel’’ plantigrady (MFP) and ‘‘heel-strike’’ plantigrady
(HSP) (Schmitt and Larson, 1995). Primates utilizing
MFP (e.g., Ateles and Hylobates) display heel contact simultaneous or subsequent to contact of the fore/midfoot
(Schmitt and Larson, 1995). HSP primates, such as great
apes and humans, display heel contact at the initiation
of stance phase (Fig. 1) (Schmitt and Larson, 1995).
Great ape HSP differs from the human condition, however, in that the former exhibit simultaneous heel and
lateral midfoot contact at touchdown (e.g. ‘‘inverted heelstrike’’ plantigrady [IHSP]) (Vereecke et al., 2003).
Human HSP is unique, as foot contact is made only with
the heel (e.g., ‘‘full-contact heel-strike’’ plantigrady
[FCP]) (Vereecke et al., 2003).
181
In addition to the type of foot postures employed at
initial contact, the arthrokinematics of primate feet differ after touchdown, through midsupport and into lift-off
(Kidd et al., 1996). In DG/SP primates, the heel is elevated throughout the majority of stance phase, and midfoot extension is accentuated. In particular, Meldrum
(1991) noted that heel elevation in the cercopithecine
foot initially is produced by extension of the midtarsal
joint (Fig. 1), termed midtarsal break, which has the
ability to extend to 408 or more (see also Bojsen-Møller,
1979, but see DeSilva, in press). Following midtarsal
break, the metatarsophalangeal joints of cercopithecines
are extended at midsupport and remain extended into
lift-off (Meldrum, 1991). In IHSP primates, and to a
lesser extent in MFP primates, heel elevation, on the
other hand, does not occur until after midsupport, and
similar to DG/SP primates there is a characteristic midtarsal break (Fig. 1) (Elftman and Manter, 1935a; Bojsen-Møller, 1979; Susman, 1983; Gebo, 1992; Schmitt
and Larson, 1995; Vereecke et al., 2003). Humans (FCP)
are unique compared with other primates because there
does not appear to be a period of accentuated movement
in the sagittal plane (i.e., extension and flexion) at the
midtarsal region during stance phase (Elftman and Manter, 1935a; Bojsen-Møller, 1979; Susman, 1983; Gebo,
1992; DeSilva, in press). In particular, as the heel is
lifted off of the substrate, the human midfoot region
remains relatively rigid and weight is transferred medially to the ball of the foot (Elftman and Manter, 1935b;
Vereecke et al., 2003; Pataky et al., 2008).
The transverse tarsal joint (TTJ) complex, consisting
of the talocalcaneonavicular and calcaneo-cuboid joints
(CCJs), is of primary interest when comparing how primates use their foot during locomotion. This joint complex facilitates mobility within the nonhuman primate
fore- and midfoot (i.e., eversion/inversion, extension/flexion, abduction/adduction), which improves grasping ability of pedal digits on a range of substrate orientations
(Elftman and Manter, 1935a,b; Bojsen-Møller, 1979; Susman, 1983; Lewis, 1989; Meldrum, 1991; Gebo, 1993b).
Early work advocated the TTJ as the principal flexor
region of the nonhuman primate foot during the characteristic midtarsal break (Elftman and Manter, 1935a;
Bojsen-Møller, 1979; Susman, 1983; Meldrum, 1991;
Gebo, 1992). Recent analyses, however, proposed that
extension/flexion at the cuboid-metatarsal (IV and V)
joint (CMJ) may be comparatively greater than at the
CCJ, and that extension at the CMJ may expand the
range of motion during midtarsal break beyond that
which can be achieved at the TTJ complex (Vereecke et
al., 2003; D’Août et al., 2004; DeSilva and MacLatchy,
2008; DeSilva, in press). Regardless of the extent to
which the CMJ contributes to midtarsal break, extension
of the CCJ during hind limb propulsive locomotion ultimately could transfer compressive loads through this
joint complex. Presumably, elevating the heel during
such compressive loading would direct substantial loads
to the dorsal region of the CCJ, because the joint would
be held in a (hyper-) extended position (Fig. 1).
Relative to other primates, the human TTJ has unique
modifications that enhance stability of the longitudinal
arch during bipedal locomotion (Weidenreich, 1923; Elftman and Manter, 1935a; Lewis, 1980, 1981, 1989; Gebo,
1992; Aiello and Dean, 2002). Most strikingly, the distal
end of the human calcaneus has become elevated relative to the substrate (Fig. 1) (Elftman and Manter,
1935a; Lewis, 1981; Gebo, 1992). This distal elevation
American Journal of Physical Anthropology
182
M.G. NOWAK ET AL.
Fig. 1. Left feet in lateral view drawn to the same proximal-distal length. (A) Lophocebus albigena (DG/SP) showing an elevated
heel that persists throughout the gait cycle. (B) Pan troglodytes (IHSP) showing heel contact during middle stance phase (i.e., at
peak vertical force). (C) Pan troglodytes (IHSP) showing an elevated heel during middle to late stance phase. (D) Homo sapiens
(FCP) showing heel contact during middle stance (i.e., at peak vertical force). The calcaneo-cuboid joint (CCJ) is depicted with an
arrow at the plantar border of the joint articulation. Note the lowered arch in the nonhuman primates (A–C), compared with the
elevated arch and CCJ in humans (D). Additionally, note that during heel elevation in both Lophocebus (A) and Pan (C) compressive forces are directed at the dorsal portion of the CCJ. The figures were drawn by Chrystal Nause. Modified from the works of
Meldrum (1991) and Gebo (1992).
completely alters the human TTJ by transforming the
CCJ into the fundamental supporting structure of the
lateral longitudinal arch (Lewis, 1981; Gebo, 1992; Aiello
and Dean, 2002). The asymmetric human CCJ has a
medial concavity on the cuboid surface of the calcaneus,
which receives a plantar-medial ‘‘beak-like’’ projection of
the calcaneal facet of the cuboid (Bojsen-Møller, 1979;
Lewis, 1989). This configuration facilitates external rotation in conjunction with a lateral swing or displacement
of the calcaneus during stance phase. Combining rotation and lateral displacement pushes the CCJ into a
tight close-packed position enhancing propulsion and
providing stability during toe-off (Bojsen-Møller, 1979;
Susman, 1983; Lewis, 1989). The longitudinal arch,
while promoting stability and propulsive capabilities in
the human foot, effectively hinders extension and flexion
American Journal of Physical Anthropology
at the TTJ such that the midtarsal break characterizing
nonhuman primates does not occur in humans (Elftman
and Manter, 1935a,b; Bojsen-Møller, 1979; Susman,
1983).
Uniqueness of the human TTJ is also accompanied by
soft tissue differences (i.e., the spring ligament, the long
plantar ligament, the short plantar ligament, and the
plantar aponeurosis) (Lewis, 1980, 1989; Gomberg, 1981;
Sarmiento, 1983; Langdon, 1990). The presence of a
well-developed plantar aponeurosis in humans, which
originates on the calcaneal tuber, assists in sustaining
the longitudinal arch (Hicks, 1954; Wright and Rennels,
1964; Bojsen-Møller and Flagstad, 1976; Bojsen-Møller,
1979; Gomberg, 1981; Kim and Voloshin, 1995; Kitaoka
et al., 1997; Pataky et al., 2008; Caravaggi et al., 2009).
Hicks (1954) described the human plantar aponeurosis
183
PRIMATE CALCANEO-CUBOID JOINT
TABLE 1. Comparative sample
Genus
Ateles
Cebus
Chlorocebus
Gorilla
Homo
Hylobates
Nasalis
Mandrillus
Pan
Papio
Pongo
Presbytis
Total
Species
d
spp.
apella
aethiops
gorilla
sapiens
spp.e
larvatus
sphinx
troglodytes
spp.f
pygmaeus
spp.g
n
Locomotor groupa
Foot postureb
6
6
5
8
9
10
3
2
8
5
3
5
70
Quadrupedal
Quadrupedal
Quadrupedal
Quadrupedal
Bipedal
Suspensory
Quadrupedal
Quadrupedal
Quadrupedal
Quadrupedal
Suspensory
Quadrupedal
MFP
DG/SP
DG/SP
IHSP
FCP
MFP
DG/SP
DG/SP
IHSP
DG/SP
IHSP
DG/SP
Sourcec
AMNH,
AMNH
AMNH
AMNH
AMNH,
AMNH,
AMNH
AMNH
AMNH,
AMNH,
AS
AMNH,
AS
AS
AS
AS, SUS
AS, SUS
SBA
a
The locomotor groups used within this study follow broad categories outlined by Fleagle (1999).
Foot placement grouping used in this study follows that used in the works of Schmitt and Larson (1995) and Vereecke et al.
(2003). DG/SP, digitigrade/semiplantigrade; MFP, midfoot heel plantigrade; IHSP, inverted heel strike plantigrade; FCP, full contact
plantigrade.
c
The sample was derived from the following institutions: AS, Adolph Schultz Collection, Anthropologisches Institut and Museum,
Universität Zürich, Switzerland; AMNH, American Museum of Natural History, New York, NY; SBA, Stony Brook University Anatomy Museum, Stony Brook, NY; SUS, Private collection of Dr. Randall Susman, Stony Brook, NY.
d
Includes A. geoffroyi, A. belzebuth, A. fusciceps, and an unknown species of Ateles.
e
Includes H. hoolock and H. lar.
f
Includes P. ursinus and an unknown species of Papio.
g
Includes Pr. obscura and an unknown species of Presbytis.
b
as a ‘‘windlass,’’ suggesting that passive toe dorsiflexion
tightens the plantar aponeurosis around the metatarsal
heads, which consequently heightens the longitudinal
arch, further enforcing its stability and enhancing foot
propulsion (Bojsen-Møller, 1979; Ker et al., 1987; Erdemir et al., 2004; Erdemir and Piazza, 2004; Cheng et al.,
2008a,b; Pataky et al., 2008; Caravaggi et al., 2009). The
plantar aponeurosis of most monkeys (excluding atelines
and Cebus) originates from the plantaris tendon and
serves to plantar flex the foot (Sarmiento, 1983; Langdon, 1990). Apes, on the other hand, have a separate origin of the plantar aponeurosis from the calcaneus similar to humans, although it is not as well-developed in
apes as in humans (Gomberg, 1981; Sarmiento, 1983;
Vereecke et al., 2005). Relative to humans, a separate origin (e.g., monkeys) or an underdeveloped plantar aponeurosis (e.g., apes) could facilitate greater extension
capability of the midfoot.
In this study, we assess two separate hypotheses.
First, quantitative variation in apparent density (AD)
distributions of the anthropoid primate CCJ reflects how
a primate uses the hind limb and foot during habitual
locomotion. Second, spatial variation in AD distributions
of the anthropoid primate CCJ reflects how a primate
positions its foot during locomotion. To assess the first
hypothesis, we predict the following: 1) bipedal humans
(FCP) will have the largest percentage of high AD in the
CCJ because all body mass support goes through their
hind limbs; 2) quadrupedal primates will exhibit an intermediate percentage of high AD in the CCJ because
they habitually support body mass with all four limbs;
and 3) suspensory primates will exhibit the smallest
areas of high AD in the CCJ because of a restricted loading regime that is predominantly generated by muscle–
tendon complexes. To assess the second hypothesis, we
predict the following: 1) humans will lack definable differences between dorsal and plantar AD distributions in
the CCJ because of bony and soft-tissue modifications
that reduce extension/flexion capabilities in the TTJ; 2)
nonhuman primates will have dorsally positioned areas
of high AD in the CCJ as a result of dorsally localized
habitual compressive loading between the calcaneus and
the cuboid during midtarsal extension; 3) DG/SP primates will have the largest percentages of high AD in the
dorsal portion of the CCJ because they habitually elevate the heel throughout support phase; and 4) MFP
and IHSP groups will have the smallest percentages of
high AD in the dorsal portion of the CCJ because they
flex their midfoot only subsequent to initial heel contact.
MATERIALS AND METHODS
Calcanei from 70 individuals representing 12 primate
genera were selected for this study (Table 1). All nonhuman primates are adult, wild-caught specimens. The
human sample is comprised of nonarchaeological adults.
Based on provenience information in museum records,
we cannot be certain that all humans in the sample
were unshod during life. [Four of the human specimens
are from the Adolph Schultz collection of the Anthropologisches Institut und Museum, Universität Zürich. These
specimens are listed as ‘‘African’’ in the collection, but it
is unlikely that they originated from Africa. Rather,
these specimens were likely obtained by Adolph Schultz
as African-American cadavers, and thus, it seems reasonably unlikely that they would have been unshod during life (P. Schmid, personal communication, 2009). The
remaining five human specimens are from the collection
housed in the Anthropology Department of the American
Museum of Natural History. Of these, one male is an
aborigine from southern Australia, one male is from the
Baining tribe of New Britain, Papua New Guinea, one
female is from the Andaman Islands, and two other
males are from South Africa (a ‘‘Hottentot’’ from Campbell, Cape Colony, and a Korana tribe member from
Bucklands, Douglas). It is unclear whether all five individuals came from unshod populations.] All specimens
were visually inspected and free from obvious pathological conditions in the postcranial skeleton. We attempted
to select specimens with absent or minimal postmortem
American Journal of Physical Anthropology
184
M.G. NOWAK ET AL.
damage whenever possible (e.g., abrasion of articular
surfaces). Specimens with excessive grease were avoided
because this can distort the radiodensities of bone (Ruff
and Leo, 1986). Additional details of sample selection criteria are available elsewhere (Carlson and Patel, 2006). Taxa
were partitioned into three locomotor groups—quadrupedal, suspensory, and bipedal—according to published attributions of habitual locomotor modes (Fleagle, 1999) (Table
1). Taxa also were grouped according to foot posture: 1)
DG/SP, 2) MFP, 3) IHSP, and 4) FCP, following Schmitt
and Larson (1995) and Vereecke et al. (2003) (Table 1).
CT-OAM was used to visualize the patterns of high
AD in the subchondral cortical plate at the distal calcaneus following a published protocol (Carlson and Patel,
2006; Patel and Carlson, 2007, 2008). Quantitative computed tomography has recently been shown to be an
accurate and powerful tool in the measurement of subchondral bone mineral density in three-dimensional (3D)
models because modality-derived subchondral densities
were strongly correlated with percent mineralization and
ash density in the equine distal third metacarpal (Drum
et al., 2009). In brief, serial CT scans of the calcaneus
were obtained in parasagittal planes using the minimum
slice thickness permitted by the CT scanner (typically
0.625 mm). Serial scans were saved as DICOM image
stacks, which were imported into ImageJ software for
subsequent analysis (http://rsb.info.nih.gov/ij). The first
step involved obtaining a volume of interest (VOI) by
cropping the stack of serial images. With the mediolateral dimension of an articular surface in mind, images in
a stack that did not include the articular surface were
excluded. With depth relative to an articular surface in
mind, a best-fit approach for width of the cropping box
used the minimum dimension required to include all
subchondral trabecular bone. With the dorsal-plantar
dimension of an articular surface in mind, a best-fit
approach for height of the cropping box used the minimum dimension required to include dorsal-most and
plantar-most regions of the articular surface.
The purpose of cropping the stack was to exclude parts
of the nonarticular surface from unduly influencing subsequent steps. If nonarticular areas are included in the
cropped stack, and they have higher ADs than subchondral bone in the articular surface of interest, then the
nonarticular areas would set upper limits for AD, injecting bias into comparisons of articular surfaces. Thus, relative radiodensities of articular and nonarticular areas
should be verified on an analysis-by-analysis basis [e.g.,
see fig. 1 in Carlson and Patel (2006) for visual comparisons in the distal radius of primates]. Certain joint surfaces (e.g., ones with complexly shaped or highly curved
surfaces) may not be suitable for this type of analysis if
nonarticular areas of high radiodensity cannot be
adequately excluded through cropping. In the case of the
calcaneal articular surface for the cuboid, it was possible
to remove nearly all nonarticular areas during the cropping process. Moreover, nonarticular areas that could
not be excluded from a specimen had relatively equivalent or lower radiodensity compared with articular areas
in the same specimen for 68 of the 70 (97%) specimens.
Subsequent to cropping, images of the subchondral
cortical bone were restacked and rotated 908 to visualize
the articular surface. Two-dimensional (2D) maps of the
3D VOIs (i.e., subchondral cortical bone) were created
using maximum intensity projection (MIP) maps and by
binning brightness values into eight categories (Fig. 2).
Essentially, each pixel in a 2D map represents the maxiAmerican Journal of Physical Anthropology
mum brightness value extracted from a column of pixels
corresponding to the z-dimension of the stack (i.e., its
depth). After inverting an image, each of the eight colors
represents a range of 32 gray values, except the lowest
bin which represents 31 gray values. The lowest bin
(white) corresponds to the lowest brightness values and
the highest bin (black) corresponds to the highest brightness values (i.e., radiodensity) in a specific MIP. When
using a standard reconstruction algorithm (e.g., a soft
tissue filter) to produce DICOM images from raw CT
data, as was done here, brightness values have a linear
relationship with attenuation coefficients and can be
transformed to a Hounsfield scale.
After the creation of a MIP, it was projected onto a 3D
virtual reconstruction of a calcaneus in order to identify
boundaries of the articular surface (Fig. 2). Nonarticular
areas in a MIP are erased, thus excluding these pixels
from analyses. Images were standardized in orientation
such that the sustentacular shelf of the 3D virtual reconstruction formed a 908 angle to a vertical axis (Fig. 2)
(Langdon, 1986). Size and distribution of high AD areas
in MIPs (i.e., black pixels) were quantified by pixel
counting. Only pixels in the highest radiodensity category are analyzed in detail because pixels in the lower
bins can be influenced to varying degrees by image artifacts (i.e., partial volume averaging and ‘‘streaking’’).
When nonarticular areas in a MIP significantly exceed
articular areas in terms of radiodensity, it is possible
that the highest bin (i.e., black pixels) will be empty after erasing the former. This was the case for only 2 of 70
(3%) specimens in the sample. Spatial distribution of
high pixel concentrations on the articular surfaces (i.e.,
dorsal and ventral) also were compared among foot posture groups using the MIPs (Fig. 2). Using ImageJ software, each articular surface was divided into a dorsal
and plantar region by fitting a horizontal line through
the midpoint between the dorsal-most and plantar-most
edges of the articular surface (Fig. 2).
As underlying absolute tissue and AD maxima may
vary amongst specimens according to a variety of factors
such as health, genetics, sex, and hormones (Martin
et al., 1998; Lieberman et al., 2001; Currey, 2002; Pearson and Lieberman, 2004; Skedros et al., 2004, 2007;
Ruff et al., 2006), comparisons of densities across specimens scanned separately are relative, unless a calibration object is scanned with the bones. Calibrating
images, unfortunately, was not feasible in this study. We
attempted to control for body size differences in the sample, as well as differences in absolute size of articular
surfaces, by considering the high AD area (i.e., black pixels) relative to total articular surface area (i.e., total
number of pixels in the articular surface), or to regional
articular surface area (i.e., total number of pixels in the
dorsal or plantar portions of the CCJ) in cases of more
localized comparisons. Similar percentages of black pixels in two specimens imply similarly accentuated (i.e.,
large percentages) or reduced (i.e., small percentages)
maximal compressive loading in the specimens. As these
are relative rather than absolute measures of AD, spatial distribution of black pixels in the articular surface
indicates the presumed location of the highest compressive loading for a given specimen without assigning
absolute magnitudes to the loadings. Thus, high percentages of black pixels concentrated in a contiguous area
suggest extensive maximal loading locally in a mobile
joint, whereas low percentages of black pixels dispersed
over the entire articular surface suggest uniformly lower
or distributed maximal loading.
PRIMATE CALCANEO-CUBOID JOINT
185
Fig. 2. Maximum intensity projection (MIP) maps of the calcaneo-cuboid joint (CCJ) surface. Images depict taxa from the different locomotor groupings and foot posture categories. All calcanei are scaled to the same size. Note that all taxa show concentrations
of high apparent density (AD) in the dorsal region of the CCJ. Quadrupeds have the most extensive areas of high AD, followed by
suspensory and bipedal taxa, respectively. Also illustrated are the articular surface partitions used in the analyses of dorsal and
ventral regions. See text for details on orientation and partitioning criteria.
Significant differences in high AD between locomotor
and foot posture groups were assessed using analysis of
variance (ANOVA). A Levene test was used to assess the
homogeneity of group variances among locomotor modes
and foot posture categories (Levene, 1960). When a positive Levene test was observed, indicating group variances were heterogeneous (P \ 0.05), a series of one-way
ANOVAs in conjunction with Tamhane’s T2 post-hoc
tests were used (Tamhane, 1977, 1979). When a negative
Levene test was observed, group variances were not significantly different (i.e., homogeneous), and a series of
one-way ANOVAs was used in conjunction with the Bonferroni post-hoc test. Within-group differences of dorsal/
plantar high AD for each foot posture group were
assessed using Student’s t-tests. To characterize the relationship between high AD area (i.e., number of black
pixels) and the size of the articular surface (i.e., number
of total pixels), reduced major axis (RMA) regression
analysis was performed. Using RMA regression was
more appropriate than using ordinary least squares
(OLS) regression for indicating the presence of isometry
or allometry in the relationship because of the variables
of interest and the particular question about their relationship (Smith, 2009). Statistical significance was set at
P \ 0.05 for all statistical testing. All ANOVAs, Levene
tests, Tamhane’s T2 tests, and Student’s t-tests were
performed using SPSS 11.0.4 for MAC OS X (SPSS,
Chicago, IL), whereas RMA regression analyses were
performed using (S)MATR (Falster et al., 2003).
RESULTS
Quantitative variation in high AD by locomotor
mode and foot posture
Percentages of high AD area (i.e., black pixels) relative
to total articular surface area (i.e., total pixels) are
reported for each locomotor group (Table 2) and illustrated in Figure 3. Locomotor groups differ significantly
(F 5 10.817; df 5 2, 69; P \ 0.001; Table 3). Quadrupedal primates have significantly larger high AD areas
than suspensory (P 5 0.001) and bipedal primates (P \
0.001), whereas suspensory primates exceed bipedal primates in percentage of high AD area, but not signifiAmerican Journal of Physical Anthropology
186
M.G. NOWAK ET AL.
TABLE 2. Summary of % high AD by locomotor group
TABLE 3. Tamhane’s T2 post-hoc analysis of % high AD by
locomotor groupa,b
a
% High apparent density
Locomotor group
n
Means 6 SD
Range
Bipedal
Suspensory
Quadrupedal
9
13
48
5.0 6 5.3
9.5 6 5.8
18.1 6 10.1
\0.1–16.2
1.7–24.5
0.2–47.0
a
Values represent high apparent density area (i.e., black pixels)
taken as a percentage of total area in the articular surface (in
pixels).
cantly (P 5 0.207). The same analyses were also conducted on combined bins 1 and 2 (i.e., summing black
and red pixels). The results (not reported) were virtually
identical, suggesting that these maximal density differences between locomotor groups are robust.
The percentages of high AD area (i.e., black pixels) relative to total articular surface area (i.e., total pixels) for
each foot posture group are presented in Table 4 and
illustrated in Figure 4. Group differences are significant
(F 5 11.894; df 5 3, 69; P \ 0.001; Table 5). IHSP and
DG/SP primates exhibit significantly greater percentages
of high AD than MFP and FCP primates (P \ 0.05);
IHSP primates exceed DG/SP primates, but the difference is not significant (P 5 0.652). The MFP primates
exceed FCP primates, but this difference also is not significant (P 5 0.571).
Both quadrupedal and bipedal primates exhibit a significant predictive relationship between logged high AD
area (i.e., total black pixels) and logged articular surface
size (i.e., total pixels), whereas no significant relationship was observed among suspensory primates (Table 6).
Quadrupeds and bipeds exhibit positive allometry in
high AD area. The DG/SP, MFP, and FCP foot posture
groups also exhibit positive allometry in high AD area,
whereas IHSP primates show no significant relationship
(Table 6).
P
Quadrupedal 3 Suspensory
Quadrupedal 3 Bipedal
Suspensory 3 Bipedal
0.001
\0.001
0.207
*
**
ns
ANOVA results: F 5 10.817; df 5 2, 69; P \ 0.001.
Unequal variances assumed: Levene statistic 5 3.467; df 5 2,
67; P \ 0.037.
* Significance at P \ 0.01.
** Significance at P \ 0.001.
ns, not significant.
a
b
Spatial variation of high AD by foot posture
The results of mean within-foot-posture-group dorsal/
plantar differences are provided in Table 4 and illustrated in Figure 5. The percentages of high AD area in
the dorsal region of the CCJ significantly exceed percentages in the plantar region for all nonhuman primate
foot posture groups (P \ 0.001; Figs. 2 and 5; Table 7).
In contrast, the human CCJ shows no dorsal-plantar regional differences in percentages of high AD (P 5 0.071;
Figs. 2 and 5; Table 7).
Percentages of high AD area in the dorsal region (i.e.,
black pixels) relative to total dorsal articular surface
area (i.e., total pixels) for each foot posture group are
presented in Table 4 and illustrated in Figure 6. Primates using different foot contact types differ significantly
from one another in the percentage of high AD in the
dorsal region of the CCJ (F 5 9.786; df 5 3, 69; P \
0.001). The DG/SP and IHSP primates exhibit significantly larger percentages of high AD than MFP and
FCP primates (P \ 0.05), whereas IHSP primates exceed
DG/SP primates and this difference is not significant
(P 5 0.754). The MFP primates exceed FCP primates,
but this difference also is not significant (P 5 0.442)
(Table 5).
The percentages of high AD area in the plantar region
(i.e., black pixels) relative to total plantar articular surface area (i.e., total pixels) for each foot posture group
are presented in Table 4 and illustrated in Figure 7. Primates using different foot contact types differ significantly from one another in the percentage of high AD in
the plantar region of the CCJ (F 5 4.589; df 5 3, 69; P
5 0.006). This result, however, may be driven in part by
a disproportionately large difference between MFP and
IHSP nonhuman primates (P 5 0.010), because all other
pairwise comparisons are not significantly different
(Table 5).
DISCUSSION
Fig. 3. Box-and-whisker plot of between locomotor group differences in high apparent density for the cuboid articular surface of the calcaneus. Values represent high apparent density
area (i.e., black pixels) taken as a percentage of total articular
surface area (in pixels). Horizontal lines within each box illustrate the median value. Boxes contain the interquartile range
(50% of values) of the sample distribution, and whiskers encompass the upper and lower extreme values, excluding outliers.
Filled circles beyond whiskers indicate outliers. See text and
Table 3 for statistical results.
American Journal of Physical Anthropology
The goal of this study was to identify differences in
CCJ loading in anthropoid primates by evaluating radiodensity distributions across taxa characterized by various habitual locomotor modes and foot posture categories. Both quantitative and spatial variation was
observed in high AD areas of the subchondral cortical
bone in the primate CCJ. These patterns are suggestive
evidence for a functional signal that partly reflects
joint loading history in this region of the primate foot
(Fig. 2).
187
PRIMATE CALCANEO-CUBOID JOINT
TABLE 4. Summary of % high AD area by foot posture group
% Total high ADa
Foot posture group
n
Means 6 SD
Range
DG/SP
MFP
IHSP
FCP
26
16
19
9
17.1
8.6
22.0
5.0
6
6
6
6
8.1–35.0
0.2–24.5
3.9–47.0
\0.1–16.2
6.3
5.6
12.8
5.3
% Dorsal high ADb
Means 6 SD
Range
6
6
6
6
10.1–51.5
0.2–41.3
\0.1–74.4
\0.1–26.1
27.0
14.6
33.8
7.8
11.5
9.4
20.9
9.1
% Plantar high ADc
Means 6 SD
Range
6
6
6
6
\0.1–15.8
\0.1–2.6
\0.1–20.6
\0.1–4.7
2.4
0.2
4.9
1.0
4.2
0.7
5.5
1.8
a
Values represent high AD area (i.e., black pixels) taken as a percentage of total area in the articular surface (in pixels).
Values represent dorsal high AD area (i.e., black pixels) taken as a percentage of total area in the dorsal region of the calcaneocuboid articular surface (in pixels).
c
Values represent plantar high AD area (i.e., black pixels) taken as a percentage of total area in the plantar region of the calcaneocuboid articular surface (in pixels).
b
Quantitative variation in high AD amongst
primates
As predicted, quadrupedal primates exhibit more expansive areas of high AD compared to suspensory primates (Fig. 3). Presumably this is the result of larger peak
compressive forces that in turn may be a result of the
additive effects of body mass support and muscle–tendon
complexes transmitted through the quadruped CCJ. Suspensory primates (i.e., Hylobates and Pongo), on the
other hand, exhibit reduced areas of high AD, potentially
reflecting what could be reduced compressive loading
through the CCJ because of the lessened role of their
hind limbs in providing terrestrial and above-branch
body mass support in their habitual locomotor repertoires (e.g., torso-orthograde suspensory activities).
These findings recall a similar dichotomy in high AD
areas of subchondral bone and habitual activity patterns
that was observed in the distal radius of quadrupedal
(i.e., anteaters, cercopithecoids, and African apes) and
suspensory (i.e., Asian apes and sloths) mammals
(Carlson and Patel, 2006; Patel and Carlson, 2008).
Although specimens in any given taxon showed
broadly similar patterns in the quantitative or spatial
distributions of high AD, and it would be interesting to
consider, it is premature to assess intraspecific variability with the present sample. In a larger sample, perhaps
focusing on a fewer number of taxa, it would be worthwhile to investigate the influences of variability through
the analysis of factors such as dietary constraints/habits,
hormone levels, habitat differences, age-/sex-biased behavioral differences, and ontogenetic variation (Martin
et al., 1998; Lieberman et al., 2001; Currey, 2002; Pearson and Lieberman, 2004; Skedros et al., 2004, 2007;
Ruff et al., 2006). All of these factors are known to influence bone remodeling, and thus, they could play a complementary role to functional loading as determinants of
AD patterns in subchondral bone of articular surfaces.
Body size also could be a determining factor (e.g., Rafferty, 1996; Swartz et al., 1998; MacLatchy and Müller,
2002); however, a general body size trend is not apparent
amongst primates because suspensory orangutans have
much lower percentages of total high AD (mean: 10.0%)
compared with several quadrupeds of smaller body sizes
(e.g., Nasalis, mean: 18.9%; Mandrillus, mean: 19.3%;
and Papio, mean: 25.6%). Amongst certain locomotor
groups, such as quadrupeds and bipeds, there is evidence for positive allometry in high AD area of the CCJ.
Moreover, it is interesting that the joints in the limb
that serve as a primary compressive load-bearing structure show positive allometry in high AD area for the
small sample of joints investigated so far. Quadrupeds
exhibit positive allometry in joints of both the forelimb
TABLE 5. Tamhane’s T2 post-hoc analyses of % high
AD by foot posture
% Total
high ADa,b
P
DG/SP 3 MFP
DG/SP 3 IHSP
DG/SP 3 FCP
MFP 3 IHSP
MFP 3 FCP
IHSP 3 FCP
Fig. 4. Box-and-whisker plot of foot posture group differences in high apparent density for the cuboid articular surface of
the calcaneus. Values represent high apparent density area in
the total articular surface (i.e., black pixels) taken as a percentage of total articular surface area (in pixels). Horizontal lines
within each box illustrate the median of the distribution. Boxes
envelop the interquartile range (50% of values) of the sample
distribution, and whiskers encompass the upper and lower
extreme values, excluding outliers. Filled circles beyond
whiskers indicate outliers. See text and Table 5 for statistical
results.
\0.001
0.652
\0.001
0.003
0.571
\0.001
*
ns
*
**
ns
*
% Dorsal
high ADc,d
P
0.003
0.754
\0.001
0.008
0.442
0.001
**
ns
*
**
ns
*
% Plantar
high ADe,f
P
0.091
0.495
0.651
0.010
0.849
0.053
ns
ns
ns
**
ns
ns
ANOVA results: F 5 11.894; df 5 3, 69; P \ 0.001.
Unequal variances assumed: Levene statistic 5 9.067; df 5 3,
66; P \ 0.001.
c
ANOVA results: F 5 9.786; df 5 3, 69; P \ 0.001.
d
Unequal variances assumed: Levene statistic 5 7.955; df 5 3,
66; P \ 0.001.
e
ANOVA results: F 5 4.589; df 5 3, 69; P 5 0.006.
f
Unequal variances assumed: Levene statistic 5 7.685; df 5 3,
66; P \ 0.001.
* Significance at P \ 0.001;
** Significance at P \ 0.01; ns, not significant.
a
b
American Journal of Physical Anthropology
188
M.G. NOWAK ET AL.
TABLE 6. RMA regression results for logged high AD pixels regressed on logged total pixels in the calcaneo-cuboid joint
Group
Locomotor mode
Quadrupedal
Suspensory
Bipedal
Foot posture
DG/SP
MFP
IHSP
FCP
Slope
95% CI
Intercept
R2
P
F*
P*
2.997
2.110
12.555
2.305–3.898
1.187–3.750
7.074–22.283
210.165
26.17
254.226
0.253
0.162
0.541
\0.001
0.172
0.024
102.139
–
592.987
\0.001
–
\0.001
1.385
3.286
3.336
12.555
1.005–1.910
2.042–5.289
2.056–5.413
7.074–22.283
22.586
211.693
211.706
254.226
0.426
0.257
0.164
0.541
\0.001
0.045
0.107
0.024
4.41
41.885
–
592.987
0.047
\0.001
–
\0.001
95% CI indicates the 95% confidence intervals of the slope presented in column 2.
* Statistical results comparing the RMA slopes in column 2 with a theoretical slope of isometry (i.e., 1). Suspensory and IHSP
groups were not used in this comparison, as there was no significant relationship for the RMA regression of logged maximum pixels
regressed on logged total pixels.
[i.e., distal radius (Carlson and Patel, 2006)] and the
hind limb (i.e., CCJ joint), whereas bipeds exhibit positive allometry in the hind limb only (i.e., CCJ joint). Suspensory primates, on the other hand, do not exhibit positive allometry in either of the joints of the forelimb [i.e.,
distal radius (Carlson and Patel, 2006)] or hind limb
(i.e., CCJ) that have been examined so far. Thus, it
seems that larger quadrupedal and bipedal primates
subject increasingly more of their weight-bearing joint
surface to maximal compressive loading. This could
be one potential mechanism for limiting absolute
magnitudes of compressive forces in joints of larger-bodied individuals, possibly to spare damage to articular
cartilage.
Fig. 5. Mean foot posture group differences of high apparent
density for dorsal and plantar regions in the cuboid articular
surface of the calcaneus. Values represent high apparent density area (i.e., black pixels) in each region (i.e., dorsal or plantar), taken as a percentage of total area in that region (in pixels). Black bars represent dorsal region. Gray bars represent
plantar region. Note that all foot posture groups have greater
percentages of high AD in the dorsal region of the calcaneocuboid joint surface than in the plantar region. See text and
Table 7 for statistical results.
American Journal of Physical Anthropology
Spatial variation in high AD amongst primates
As predicted, nonhuman primates exhibit significantly
greater percentages of high AD in the dorsal region of
the CCJ compared with the plantar region (Figs. 2 and
5). The relative absence of plantar foci is consistent with
the idea that nonhuman primates may not regularly
load their CCJ while the joint is in flexion (i.e., plantardirected compressive loading). Conversely, dorsally positioned foci are consistent with compressive loading
through the CCJ during a close-packed position (i.e.,
hyperextension) (Fig. 1). The consistency of this trend
amongst nonhuman primates corroborates the broad
similarity that others have attributed to the function of
the nonhuman primate CCJ, as well as a functional signal associated with midfoot extension at the TTJ
(Elftman and Manter, 1935a,b; Bojsen-Møller, 1979;
Langdon, 1986; Lewis, 1989; Meldrum, 1991; Gebo,
1992). Although recent analyses (Vereecke et al., 2003;
D’Août et al., 2004; DeSilva and MacLatchy, 2008;
DeSilva, in press) suggest that the midtarsal break
actually recruits the CMJ rather than the CCJ, results
of this study suggest that some (hyper-) extension may
arise in the CCJ (see also DeSilva, in press). Comparing
relative contributions to midtarsal break of these two
joints is beyond the scope of this study, although clearly
this warrants further investigation. Even if extension at
the CMJ ultimately is proven to be more substantial
than at the CCJ (Vereecke et al., 2003; DeSilva and
MacLatchy, 2008; Griffin et al., 2008; DeSilva, in press),
simultaneous or successive extension at both joints could
promote additional (and essential) mobility in the midfoot as weight is shifted forward on the foot during
stance phase. Enhancing the mobility of the midfoot
would be advantageous, particularly during arboreal
locomotion, because it could provide a mechanism for
maintaining a longer period of contact with the substrate
(Meldrum, 1991). This, in turn, could reduce vertical
peak forces, while maintaining stability, which would be
more beneficial than that allowed by a more rigid foot.
TABLE 7. Within-group comparisons of dorsal and plantar %
high AD area by foot posture
Foot posture group
n
Comparison
df
t
DG/SP
MFP
IHSP
FCP
26
16
19
9
D[V
D[V
D[V
D[V
25
15
18
8
9.238
6.065
7.152
2.079
* Significance at P \ 0.001; ns, not significant.
P
\0.001
\0.001
\0.001
0.071
*
*
*
ns
PRIMATE CALCANEO-CUBOID JOINT
189
well. Similarity in AD patterns between these foot posture
groups, however, is not consistent with this scenario.
Extension capability of the midfoot over the duration of
stance phase may be relevant to this discrepancy. Vereecke et al. (2003) observed that although bonobos (during
quadrupedal locomotion) incur the highest vertical peak
reaction forces during the initial contact of the heel, they
also experience relatively large reaction forces at the lateral midfoot when the heel is elevated in middle-to-late
stance phase (Fig. 1).
Uniqueness of the human CCJ?
Fig. 6. Box-and-whisker plot of foot posture group differences
of high apparent density in the dorsal region of the cuboid articular surface of the calcaneus. Values represent high apparent density area in the dorsal region (black pixels) taken as a percentage
of total dorsal articular surface area (in pixels). Horizontal lines
within each box illustrate the median of the distribution. Boxes
envelop the interquartile range (50% of values) of the sample distribution, and whiskers encompass the upper and lower extreme
values, excluding outliers. Filled circles beyond whiskers indicate
outliers. See text and Table 5 for statistical results.
Additionally, midfoot flexibility also may enhance propulsion at push-off (Vereecke and Aerts, 2008). In particular, Vereecke and Aerts (2008) noted that during bipedalism, the flexible foot of Hylobates lar functioned as a
‘‘reversed arch’’ that generated elastic recoil potential via
the plantarflexor tendons.
Variation in presumed joint loading in the primate foot
appears to partially reflect the use of different habitual
foot postures. As predicted, DG/SP primates exhibit dorsally expanded areas of high AD compared with MFP
primates, but not compared with IHSP primates. Large
areas of high AD in the dorsal portion of the CCJ of DG/
SP primates presumably reflect more expansive maximal
compressive loading through the CCJ as a result of habitual heel elevation and concomitant joint (hyper-)
extension (Fig. 6). Reduction of the dorsal area of high
AD in the articular surface of MFP primates (i.e., Ateles
and Hylobates) compared with both DG/SP and IHSP
(Fig. 6) primates could be partly attributable to more
suspensory locomotion in the former (e.g., Fleagle, 1976,
1980; Cant, 1986; Youlatos, 2002), which may reduce
overall compressive loading in the midfoot if hind limbs
experience a reduced frequency and/or magnitude of
compressive force (i.e., body mass support) during suspensory behaviors.
Contrary to our predictions, the IHSP group does not
have a lower percentage of dorsal high AD than the DG/
SP group (Fig. 6), even though different regions of the foot
initially contact the substrate in these groups (i.e., elevated heel vs. heel contact, respectively). While DG/SP
primates experience substrate reaction forces at and
shortly after touchdown, a proportionately larger compressive joint reaction force should be transferred through
the CCJ compared with the condition in IHSP primates
because the heel is elevated in the former, thereby reducing foot contact area for distributing the reaction force. In
contrast, the peak compressive force at and shortly after
touchdown in IHSP primates should be distributed not
only through the CCJ but through the calcaneal tuber as
Contrary to our prediction, humans on average exhibit
the most reduced areas of high AD compared with other
primates (Fig. 2). However, as predicted, humans do not
display significant differences in high AD percentages
between dorsal and plantar regions of the CCJ (Fig. 5).
Both HSP foot posture groups have an anatomically similar plantar aponeurosis compared with most other monkeys, although it is described as less well developed in
IHSP primates than FCP primates (Gomberg, 1981; Sarmiento, 1983; Vereecke et al., 2005). Because of this similarity, it is potentially interesting to consider the contribution of the plantar aponeurosis in the distribution of
compressive forces in the foot. The fact that humans
(FCP foot posture group) more closely resemble apes
(IHSP foot posture group) in the dorsal/plantar ratios of
maximal density (i.e., black pixel % ratios) than other
foot posture groups suggests that the plantar aponeurosis may modulate force distribution in the foot, at least
to some degree depending on its state of development.
Taken together, and compared with all primates
sampled, the unique human AD pattern suggests that
maximal compressive force transmission through the distal calcaneus of humans is more evenly dispersed over
the entire articular surface (i.e., not dorsally concentrated) and that the majority of the surface in bipeds
experiences relatively low overall compressive forces.
Fig. 7. Box-and-whisker plot of foot posture group differences
of high apparent density in the plantar region of the cuboid articular surface of the calcaneus. Values represent high apparent
density area in the plantar region (black pixels) taken as a percentage of total plantar articular surface area (in pixels). Horizontal lines within each box illustrate the median of the distribution.
Boxes envelop the interquartile range (50% of values) of the sample distribution, and whiskers encompass the upper and lower
extreme values, excluding outliers. Filled circles beyond whiskers
indicate outliers. See text and Table 5 for statistical results.
American Journal of Physical Anthropology
190
M.G. NOWAK ET AL.
This uniqueness may be related to the hard and soft
tissue specializations in the human foot (i.e., a closepacking CCJ and well-developed plantar aponeurosis).
The human AD pattern in the CCJ is consistent with
the idea that the asymmetrically shaped CCJ and the
well-developed plantar aponeurosis act to stabilize the
longitudinal arch (Hicks, 1954; Wright and Rennels,
1964; Bojsen-Møller and Flagstad, 1976; Bojsen-Møller,
1979; Gomberg, 1981; Kim and Voloshin, 1995; Kitaoka
et al., 1997; Pataky et al., 2008; Caravaggi et al., 2009).
During early stance phase, the asymmetrically shaped
human CCJ is forced into a close-packed position following the ‘‘lateral swing’’ of the calcaneus, which in turn
tightens or ‘‘preloads’’ the plantar aponeurosis (Weidenreich, 1923; Elftman and Manter, 1935a,b; Bojsen-Møller,
1979; Lewis, 1989; Pataky et al., 2008; Caravaggi et al.,
2009). As the foot endures loading because of gravitational forces during midstance (e.g., body weight), and
compressive loads ‘‘open’’ the arch plantarly (Gefen et
al., 2000), tension in the plantar aponeurosis increases
(Gefen, 2003), counteracting midfoot extension. Peak
tensile strains in the plantar aponeurosis occur during
the later portion of stance phase and are directly correlated with a cranially oriented pull of the Achilles tendon and passive dorsiflexion of the toes that initiates the
windlass mechanism and heightens the arch (Hicks,
1954; Bojsen-Møller, 1979; Bojsen-Møller and Lamoreux,
1979; Thordarson et al., 1995; Kappel-Bargas et al.,
1998; Carlson et al., 2000; Giddings et al., 2000; Gefen,
2002, 2003; Erdemir et al., 2004; Erdemir and Piazza,
2004; Cheng et al., 2008a,b; Caravaggi et al., 2009).
Recently, Griffin et al. (2008; Griffin and Richmond, in
press) have noted that the human first metatarsophalangeal joint is capable of greater dorsiflexion than the
same joint in quadrupedal bonobos. Increased dorsiflexion in the human first metatarsophalangeal joint coupled
with a strong plantar aponeurosis may enhance the mechanical effectiveness of the windlass mechanism,
thereby further buttressing the longitudinal arch of
humans compared to nonhuman primates. Structural
competency of the longitudinal arch is therefore critical
in humans. Indeed, clinical work has outlined numerous
risk factors associated with the surgical release of the
plantar aponeurosis, including a decrease in arch height
(Kim and Voloshin, 1995; Kitaoka et al., 1997; Sharkey
et al., 1998) and altered stress distributions in hard (i.e.,
calcaneocuboid joint and metatarsals) and soft (i.e.,
spring ligament, short plantar ligament, long plantar ligament, flexor digitorum longus, and flexor hallucis longus) tissues (Murphy et al., 1998; Gefen, 2002; Crary
et al., 2003; Erdemir and Piazza, 2004). A well-developed
human plantar aponeurosis contributes to propulsion by
rapidly transmitting forces from the hind foot to the
forefoot via elastic recoil of the ‘‘preloading’’ and peakloading phases (Hicks, 1954; Wright and Rennels, 1964;
Bojsen-Møller, 1979; Ker et al., 1987; Simkin and
Leichter, 1990; Erdemir et al., 2004; Erdemir and
Piazza, 2004; Pataky et al., 2008; Caravaggi et al.,
2009). Accordingly, the plantar aponeurosis of humans
appears to attenuate extensive dorsal loading in the CCJ
by limiting (hyper-) extension in the joint, unlike the
condition in nonhuman primates.
rupedal, suspensory, and bipedal primates (i.e., high,
low, and minimal percentages of high AD, respectively).
This can be interpreted as expanded areas of presumed
maximal compressive force transmission through the
CCJ of quadrupedal primates compared with the latter
groups. Intermediate percentages of high AD in suspensory primates may be related to an overall reduction in
hind limb involvement in terrestrial and above-branch
body mass support, and thus, a likely reduction in compressive loading in the hind limbs. Bipedal humans, on
the other hand, rather than exhibiting high compressive
loading in their CCJ, exhibit surprisingly low percentages of high AD. Potentially high compressive loads in
the human CCJ may be mediated by the presence of a
unique longitudinal arch.
Comparisons between primates adopting different habitual foot postures identified several significant differences between groups, which seem to be tied to foot orientation during support phase of a stride. Consistent
with the notion of a midtarsal break, all nonhuman primates have more extensive areas of high AD in the dorsal aspect of the CCJ compared with the plantar aspect,
which suggests that the CCJ experiences maximal compressive loading while (hyper-) extended. A lack of differentiation between MFP and FCP primates is proposed to
be a result of greater reliance on suspensory locomotion
(i.e., less use of hind limbs for above-branch body mass
support) by MFP primates. FCP primates (humans) exhibit a CCJ with unique features compared with all
other nonhuman primates. These support the notion
that humans have evolved a foot with greater stabilizing
and propulsive capabilities, while sacrificing midfoot mobility. Development of unique bony (i.e., a CCJ capable
of close-packing) and soft tissue (i.e., plantar aponeurosis) support mechanisms are proposed to be the likely
candidates responsible for the distinctive AD patterns in
the human CCJ.
ACKNOWLEDGMENTS
The authors acknowledge Universität Zürich-Irchel for
permission to use specimens in their comparative collection. The authors are grateful to Michael Krupa and the
Universitätsspital, Zürich, Switzerland, for their assistance and permission to acquire CT data. The authors
thank Stony Brook University Hospital for granting
access to their CT facilities, especially Justin Georgi for
his assistance with scanning. Randall Susman aided this
work by providing several of the comparative specimens
used in this analysis. The authors are also grateful to
Eileen Westwig, Gisselle Garcia, and the Departments of
Mammology and Anthropology at the American Museum
of Natural History, New York, for assistance with the
collections and permitting specimen loans. The authors
thank Peter Schmid, for providing information on specimens in the Schultz collection at the Universität ZürichIrchel, and Chrystal Nause (Southern Illinois University,
Carbondale), for her drawings of the primate feet (Fig.
1). Finally, the authors are extremely grateful for the
valuable comments and suggestions provided by Chris
Ruff, an associate editor, and anonymous reviewers.
CONCLUSIONS
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