Relative strength of the tibia and fibula and locomotor behavior in
Department of Biological Anthropology and Anatomy, Duke University, 05 Bio. Sci. Bldg. Science Drive, Box 90383, Durham, NC 27708-0383, USA
Received 28 August 2006; accepted 9 May 2007
The fibula has rarely been considered in comparative morphological studies, probably due to its relatively minor role in carrying mechanical
loads. However, some differences in morphology (and inferred function) of the fibula between humans and apes, and within apes, have been
noted and related to differences in positional behavior. Therefore, the study of tibiofibular relations may be useful in characterizing such dif-
ferences. This study examines cross-sectional geometric (CSG) properties (cortical area and polar section modulus, Zp) of the tibia and fibula
at mid-diaphysis across a sample (n ¼87) of humans, chimpanzees, gorillas, orangutans, and gibbons. The fibula is compared against the tibia in
the different taxa. The results indicate that the robusticity of the fibula relative to that of the tibia can be explained in terms of differences in
positional behavior. In particular, hominoids that are more arboreal (i.e., gibbons, orangutans, and chimpanzees) possess a relatively more robust
fibula than do hominoids that are more terrestrial (i.e., gorillas and humans). The difference appears to be a consequence of the more mobile
fibula and more adducted position of the hindlimb necessary in an arboreal environment. Apart from providing the first CSG data on the fibula,
these results may be helpful in reconstructing the locomotor behavior of fossil hominoids.
? 2007 Elsevier Ltd. All rights reserved.
Keywords: Cross-sectional geometry; Hominoid locomotion; Tibia; Fibula
Although quadrupedalism is the most common mode of lo-
comotion among primates, there is a great diversity of locomo-
tor habits in this group. In addition, primates have been shown
to differ from nonprimate mammals in that they rely more on
their hindlimbs for both support and propulsion (Kimura et al.,
1979; Kimura, 1985, 1992; Demes et al., 1991, 1994; Demes
and Jungers, 1993; Schmitt and Lemelin, 2002; Schmitt and
The firsts attempts to interpret locomotor function from pat-
terns of structural strength in the diaphyses of primate hindlimb
bones were made at the end of the 1970s and the beginning of
the 1980s (Jungers and Minns, 1979; Burr et al., 1981, 1982).
In one of the first large-scale studies of the cross-sectional
geometry (CSG) of hindlimb long bones, Ruff and Hayes
(1983) investigated differences in structure of the femur and
tibia in archaeological and modern human samples, and be-
tween humans and nonhuman primates. The latter authors
stressed the importance of studies of hindlimb cross-sectional
properties in elucidating differences in loadings produced by
different locomotor behaviors within primates.
Recent experimental research suggests that mechanically
induced hypertrophy of the skeleton might be systemic rather
than localized in response to loading (Lieberman, 1996; Dev-
lin and Lieberman, 2007). It has also been found that geomet-
ric properties of the diaphysis do not correspond strictly with
actual patterns of in vivo strains, partially as a result of the
shift of the neutral axis during loading (Lieberman et al.,
2004). Despite evidence of complexity of cortical-bone re-
modeling, experimental research continues to support the exis-
tence of a relationship between cortical-bone morphology and
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Journal of Human Evolution 53 (2007) 647e655
mechanical loading (Robling et al., 2000; Daly et al., 2004;
Warden et al., 2005; for a review, see Ruff et al., 2006). How-
ever, given that there are probably genetic controls to basic
bone form and bone response to mechanical loading (Lovejoy
et al., 2003; Devlin and Lieberman, 2007), it is advisable to
compare bones from similar skeletal locations in species
with similar mechanical designs. Within such comparisons,
cross-sectional geometric parameters are still the best avail-
able estimates of in vivo mechanical competence (Ruff
et al., 2006).
Numerous CSG studies have been performed on the hin-
dlimb bones of primates (Schaffler et al., 1985; Ruff, 1987,
1989, 2002; Burr et al., 1989; Runestad, 1997; Polk et al.,
2000; Kimura, 2002, 2003; Marchi and Borgognini-Tarli,
2004; Carlson, 2005; Marchi, 2005). In spite of the great
amount of material studied, attention has almost always
been devoted exclusively to the femur and tibia. However, var-
iation in fibular form and function among different groups of
mammals has been documented (Walmsley, 1918; Carleton,
1941; Barnett and Napier, 1953). Although anthropoids gener-
ally have a mobile fibula (Barnett and Napier, 1953), the ro-
busticity of this bone relative to the tibia varies. Ruff (2003)
calculated the ratio of fibular to tibial circumference for a num-
ber of primate species based on data reported by Schultz
(1953). He found that this ratio varies from 0.446 to 0.500
among cercopithecoids, and from 0.520 to 0.624 among hom-
inoids. On the basis of these data, it can be concluded that
hominoids have a relatively more robust fibula than do cerco-
pithecoids, and this difference may be related to the fibula’s
role in bearing mechanical loads in the hindlimb; indirect ev-
idence suggests that the degree to which the fibula bears loads
varies among primates. For example, Ruff (2003) found that
tibial cross-sectional diaphyseal dimensions are particularly
poor predictors of body mass in primates except within cerco-
pithecoids, and he suggested that this result is due to variation
in the weight-bearing role of the fibula within anthropoids,
which would affect relative tibial strength. Studies conducted
on human samples (Lambert, 1971; Takebe et al., 1984; Goh
et al., 1992; Wang et al., 1996; Funk et al., 2004) indicate
that the fibula has a weight-bearing function, carrying 6.4e
19.0% (depending on the study and ankle position) of the
load borne by the leg.
Differences between human and ape fibulae have been
noted (for a review, see Aiello and Dean, 1990). A series of
differences related to the distal articulation with the talus
have been described (Stern and Susman, 1983), including (1)
the course of the proximal border of the distal articular facet,
which is obliquely disposed to the long axis of the fibular shaft
in apes and perpendicular to it in humans, and (2) the proximal
segment of the distal articular surface, which, with the fibular
shaft oriented vertically, faces almost directly medially in hu-
mans and significantly inferiorly in apes. Indirect evidence of
the different mechanical role of the fibula in apes can also be
inferred from the overall morphology of the talocrural joint.
Latimer et al. (1987) described a series of differences in this
region between apes and humans. The authors found that the
angle between the long axis of the tibia and the rotational
axis of the talocrural joint is nearly 90?in humans and greater
than 90?in African apes, resulting in a superolaterally inclined
tibia and fibula in the latter. Latimer et al. (1987) also found
that the angle between the joint’s rotational axis and the supra-
talar articular surface is smaller in humans than in African
apes. These authors suggested that the above characteristics
relate to varus and valgus knee positions in great apes and hu-
mans, respectively, and are consequences of habitual force
transmission through the proximal ankle joint (via the tibia
and fibula) during different types of postures and locomotion.
In addition to morphofunctional evidence, studies of sub-
strate reaction force provide important clues about the role
of the fibula in sharing hindlimb loads in primates. In a recent
study performed on lemurs, Carlson et al. (2005) found that
mediolateral forces during quadrupedal locomotion, both on
the ground and in the trees, are important in primates. In par-
ticular, they found that lemurs exerted medially directed side-
to-side forces more frequently during arboreal quadrupedalism
than laterally directed forces, both in the forelimb and in the
hindlimb. In contrast, when on the ground, lemurs exerted lat-
erally directed side-to-side forces more frequently. The direc-
tion of the substrate reaction force is an important indicator of
the plane in which limb bones are bent (Rubin and Lanyon,
1982; Biewener et al., 1983; Demes et al., 2001). Given that
the fibula is positioned laterally in the hindlimb, Carlson
et al.’s (2005) results suggest that the fibulae of primates
that are more arboreal should bear more load than those of pri-
mates that are more terrestrial. No studies have investigated
mediolateral substrate reaction forces in the hindlimb of an-
thropoid primates. However, in an examination of forelimb
substrate reaction forces in quadrupedal anthropoids, Schmitt
(2003) found that, on an arboreal support, all of the species
studied held their humerus in an adducted position and more
frequently exerted medially directed side-to-side forces than
they did when walking on the ground. Given the similarities
observed with respect to the forelimb and hindlimb in lemurs
noted above, it is likely that the same is true for anthropoids.
However, more studies are needed in order to substantiate this
To my knowledge, only one previous study has investigated
differences in cortical characteristics of the fibula among hom-
inoids. McLean and Marzke (1994) compared the cortices of
chimpanzee and human fibulae and found that, in general,
chimpanzees have a proportionally thicker fibular cortex
than do humans, and that the differences are most pronounced
on the anterior aspect. With respect to the lateral aspect, hu-
mans and chimpanzees had the same values and the authors
explained this finding as a possible consequence of the strong
and repeated contraction of the peroneal muscles in humans.
The fibula has probably been overlooked in biomechanical
studies for two main reasons: (1) the fibula is a narrow bone,
which decreases its likelihood of being preserved in compari-
son to the more massive femur and tibia, and thus it is rare in
museum collections and in the fossil record; (2) the fibula is
less involved in supporting body weight than are the femur
and tibia (Lambert, 1971; Takebe et al., 1984; Goh et al.,
1992; Wang et al., 1996; Funk et al., 2004).
D. Marchi / Journal of Human Evolution 53 (2007) 647e655
Here, I report the results of an analysis of the cross-sec-
tional geometric properties of the fibula articulated with the
tibia (i.e., the two bones articulated as they are found in the
living animal) in a hominoid sample comprising modern hu-
mans, chimpanzees, gorillas, orangutans, and gibbons. The
primary goal of this study is to determine if CSG characteris-
tics of the tibiofibular complex are useful in distinguishing
broad locomotor behaviors (see below) among living homi-
noids. On the basis of the studies of the morphofunctional
characteristics of the tibia and fibula and of the articular char-
acteristics of the ankle (Barnett and Napier, 1952, 1953; Stern
and Susman, 1983; Latimer et al., 1987; Ruff, 2003), as well
as studies of substrate reaction force (Schmitt, 2003; Carlson
et al., 2005), we can conclude that: (1) apes have a more mo-
bile fibula than humans; (2) the steeper the dorsiflexion of the
foot, the more mobile is the fibula; (3) primates that are more
arboreal exert medially directed side-to-side forces and bear
their hindlimb in adducted postures more frequently than pri-
mates that are more terrestrial. Here, I test these expectations
using the CSG properties of the tibia and fibula. Because of the
greater mobility of the fibula and the orientation of the sub-
strate reaction forces discussed above, I predict that the fibula
will be more robust (i.e., more mechanically stressed) in apes
than it is in humans. In addition, I predict that apes that are
more arboreal (i.e., chimpanzees and Asian apes) will possess
a more robust fibula relative to the tibia than does the gorilla
(i.e., more terrestrial) due to both the higher degree of dorsi-
flexion of which they are capable (because of their more fre-
quent arboreal activities; e.g., Doran, 1996; Remis, 1998)
and the greater frequency of medially oriented substrate reac-
tion forces to which they are exposed.
Because the load in the lower section of the hindlimb is
shared by both the tibia and the fibula, I analyzed the relative
(to the tibia) robusticity of the fibula. In this way, the problem
of size standardization of CSG properties, which could create
problems in comparisons of primates with different limb pro-
portions (such as humans and apes), is avoided (Marchi,
The results of this research, besides providing a character-
ization of the cross-sectional geometric properties of the fibula
(a bone that has received relatively little attention), should be
applicable to paleoanthropological studies. In particular, un-
derstanding the biomechanical relationship between the tibia
and fibula in living hominoids may contribute to a better char-
acterization of the locomotor behaviors of fossil hominoids.
Materials and methods
A total of 87 osteological specimens (Table 1) were ana-
lyzed. Due to differences in the proportion of cortical area
to total area between subadults and adults (Ruff et al.,
1994), only full adults for each species were sampled. Individ-
uals with complete long-bone epiphyseal fusion and no signs
of senescence (e.g., arthritic changes, osteoporosis) were se-
lected. The human sample consisted of a medieval (seventh
century) sample from a German necropolis (Neuburg, Donau).
The ape sample is composed of wild-shot and captive chim-
panzees, gorillas, orangutans, and gibbons (Table 1).
Given the artificiality of captive environments, differences
in locomotion between captive and wild-shot animals are ex-
pected. Sarmiento (1985), in a comparison of wild and captive
orangutans, found that free-ranging animals spend a higher
percentage of time practicing locomotor behavior than captive
animals. Among the skeletal differences he found between the
two groups, only the differences in long-bone torsion were
considered reflective of the differences in locomotor behav-
iors. (It should be noted that the author did not collect data
on the fibula.)
Sarmiento (1985) had a well-documented history of captiv-
ity for the sample he studied. The orangutans had been born or
raised in a zoo or brought to the zoo at a very early age. For
the sample analyzed in the present study, there is no history
of how long the animals were kept in captivity or the captive
habitat type. However, in the catalog of the museums from
which samples were taken, the region from which the animal
came is reported for every individual (both wild-shot and cap-
tive). Therefore, the captive chimpanzees, orangutans, and
gibbons analyzed here are unlikely to have been born in
Given that the chimpanzee sample contains 11 captive in-
dividuals out of 17, the orangutan sample three captive in-
dividuals out of 12, and the gibbon sample three captive
individuals out of 17, sample size would be appreciably re-
duced if only wild-shot animals are considered. Thus, cap-
tive and wild-shot subsamples within each species were
statistically tested for significant differences in order to de-
termine if the subsamples could be pooled for analysis (see
Sex was known for all of the apes. For the humans, sex
had to be assigned. The good state of preservation of the
sample permitted a reliable sex attribution by means of pel-
vic and cranial traits (Brothwell, 1981; White and Folkens,
6 (all captive)
12 (all wild-shot)
4 (1 captive, 3 wild-shot)
10 (all wild-shot)
11 (5 captive, 6 wild-shot)
5 (1 captive, 5 wild-shot)
8 (2 captive, 6 wild-shot)
7 (3 captive, 4 wild-shot)
Total 44 (7 captive, 25 wild-shot) 43 (11 captive, 20 wild-shot)
1From the Anthropologische Staatssammlung at the Universita ¨t Mu ¨nchen,
Germany. Medieval humans (seventh century) from a German necropolis
2From the Schultz collection and the primate collection at the Universita ¨t
Zu ¨rich Irchel, Switzerland, and from the Zoologische Staatssammlung at the
Universita ¨t Mu ¨nchen, Germany.
3Pan troglodytes troglodytes, P. t. schweinfurthii, and P. t. sp.
4Gorilla gorilla gorilla.
5Pongo pygmaeus pygmaeus, Pongo p. abelii, Pongo pygmaeus sp.
6Hylobates lar and Hylobates hoolock.
D. Marchi / Journal of Human Evolution 53 (2007) 647e655
A tibia and a fibula (same side) from each individual in the
sample were selected for study. Approximately equal numbers
of left and right sides per sex and species were taken.
One cross section at a level equal to 50% of the tibial length
measured from the distal end of the bone was taken (Fig. 1).
The definitions of bone length, the orientation of reference
axes, and the section location for the tibia follow those used
by Ruff (2002). Because the tibia and fibula were treated as
a complex, only the tibia was positioned according to the
above criteriadthe fibula was articulated to it in the anatom-
ical position. The location of the cross section in the fibula was
determined by that in the tibia with the two bones articulated
Polysiloxane molds were placed around the diaphysis of
each bone to obtain the subperiosteal contours, and estimates
of endosteal contours were obtained from measurements of bi-
planar radiographs of the diaphysis. In absence of a CT scan-
ner, this method yields reasonably accurate results (O’Neill
and Ruff, 2004).
Reconstructed cross sections were analyzed with a version
of the program SLICE (Nagurka and Hayes, 1980), provided
by Dr. Michael Black and adapted as a macro routine inserted
in Scion Image release Beta 4.03 for Windows 95 to XP
(freely available at www.scioncorp.com). The cross-sectional
properties measured in this study were cortical area (CA)
and the polar section modulus (Zp). The CA is proportional
to axial compressive and tensile strength, and Zpis propor-
tional to torsional strength and (twice) average bending
strength. The polar section modulus is equal to the polar mo-
ment of area (J) of the section divided by the perpendicular
distance from the neutral axis to the outermost fiber of the sec-
tion (Ruff, 2002). In the absence of bone-breadth datadas is
the case in this studydZp can be approximated as J0.73
(Ruff, 1995, 2002).
The polar moment of area is less applicable to torsional
analyses in strongly asymmetrical sections like the tibial mid-
shaft (Ruff, 2000; Daegling, 2002). However, the use of J as
a measure of general mechanical rigidity (i.e., bending
strength) is appropriate (Daegling, 2002). Bending loads
seems to be far more important in primate tibiae than torsional
loads (Demes et al., 2001), and thus the use of Zp(proportional
to J) is appropriate in this study.
Apes show a particularly wide range of locomotor habits, in-
cluding acrobatic arm-swinging, quadrumanous climbing, qua-
drupedal knuckle- or fist-walking, and short bouts of bipedal
locomotion (Fleagle, 1976, 1980; Sugardjito, 1982; Sugardjito
and van Hooff, 1986; Cant, 1987; Tuttle and Watts, 1985; Hunt,
1992; Remis, 1993, 1995; Doran, 1996). All ape species are
fully capable of arboreal activity, though they differ consi-
derably in the amount of time spent in trees. The principal dis-
tinction between the locomotor patterns of ape taxa is the
percentage of the repertoire spent in different activities and
the patterns used during travel between feeding or resting sites
(Fleagle, 1976). Chimpanzees and gorillas differ considerably
in the amount of time spent in trees, with chimpanzees being
more arboreal (Doran, 1996; Remis, 1998), even if recent stud-
ies seem to indicate that lowland gorillas (the species included
here) are probably more arboreal than previously believed
(Remis, 1995, 1997, 1998; however, given that Remis’s sample
was not habituated, she could not identify with certainty the
natural percentage of time spent in trees). Both African apes
travel along the ground using the characteristic knuckle-
walking quadrupedal locomotion. Asian apes rarely descend
to the ground (Fleagle, 1976, 1980; Sugardjito, 1982; Sugar-
djito and van Hooff, 1986). During arboreal travel, gibbons
mainly brachiate (Fleagle, 1980; Hollihn, 1984), while orang-
utans move cautiously, resting their weight on multiple sup-
ports (i.e., through quadrumanous scrambling; Sugardjito,
1982; Sugardjito and van Hooff, 1986).
Given the small size of the sample analyzed here, no fine-
grained locomotor categories were investigated. Following
arguments made by Ruff (2002) and Marchi (2005), I will in-
vestigate the association between CSG properties of hindlimb
long bones and broad locomotor differences among apes, re-
ferring particularly to more arboreal hominoids vs. more ter-
For this study, orangutans, chimpanzees, and gibbons were
grouped in the category ‘‘more arboreal apes’’ and gorillas in
the category ‘‘more terrestrial apes.’’ It can be argued that
chimpanzees are fully adapted to quadrupedal locomotion on
the ground as are gorillas, or that orangutans and gibbons dif-
fer in arboreal locomotor behaviors, or that the arboreal loco-
motor behaviors of chimpanzees and orangutans are different.
The difference in specific locomotor behaviors among the spe-
cies included in the two categories proposed above is
Fig. 1. Positioning of the right human tibiofibular complex; 50% is the level at which cross-sectional properties were measured (tibial positioning after Ruff, 2002).
D. Marchi / Journal of Human Evolution 53 (2007) 647e655
unquestionable. However, recent studies (Schmitt, 2003; Carl-
son et al., 2005) have demonstrated that primates position their
limbs in a more adducted posture and more frequently exert
medially directed side-to-side forces on arboreal supports
than when walking on the ground. Thus, if a species spends
more time in an arboreal environment, then its fibula should
be subjected to a different biomechanical loading regime
than that experienced by a species spending more time on
the ground. Therefore, I believe it is correct in the context
of this study to group the hominoids in two broad categories
(more arboreal vs. more terrestrial).
Statistical tests were performed to determine whether there
were significant differences between wild-shot and captive ape
subsamples. Due to the small size of the samples and possible
nonnormal distributions, ManneWhitney U-tests between
wild-shot and captive cross-sectional proportions of the tibia
to fibula (logged ratios) were carried out for chimpanzees,
orangutans, and gibbons (only one captive animal was present
in the gorilla sample, and its CSG values were comparable to
those of the other individuals).
Comparisons of tibial/fibular proportions among the differ-
ent species analyzed in this study were carried out using tradi-
tional bivariate plots to provide further means of visualizing
species differences in proportions. On each bivariate plot, an
isometric line centered on the mean x-y of the pooled hominoid
sample was plotted. The percent prediction error [PPE ¼
(observed value? predicted value)/predicted value? 100] was
used to compare the position of each species relative to every
other species with respect to the isometric line. The PPE pro-
vides the distance of the data point from the isometric line
on the y-axis. Tukey multiple-comparison tests among pairs
of species means for the PPE values were also performed.
All statistical analyses were carried out with the PC program
STATISTICA 7 (Statsoft, 2004).
Table 2 provides descriptive statistics for raw cortical areas
and polar section moduli of the tibia and fibula for each
Wild-shot vs. captive
Results of ManneWhitney U-tests between wild-shot and
captive tibia-to-fibula cross-sectional proportions (logged ra-
tios) within species (chimpanzees, orangutans, and gibbons)
are reported in Table 3. Differences between wild-shot and
captive animals are not significant for any of the parameters
analyzed here, and thus, the two subsamples can be pooled
within each species for analysis of cross-sectional properties.
Results of the Tukey multiple-comparisons tests between
species for tibial on fibular CA and Zpat mid-diaphysis are
given in Table 4. Humans have the relatively highest tibial/fib-
ular CA, followed by gorillas. Chimpanzees, orangutans, and
gibbons show relatively lower tibial CA than humans and go-
rillas, although chimpanzees and orangutans are not signifi-
cantly different from gorillas. Results are similar for Zp,
although gorillas are not significantly different from humans,
and the chimpanzee value is significantly lower than that for
gorillas. Orangutans, chimpanzees, and gibbons are not signif-
icantly different from each other. These results are illustrated
in the bivariate plots of each species relative to the isometric
line (Fig. 2a,b)dhumans (fully terrestrial) and gorillas (the
most terrestrial ape) fall above the isometric line (positive
values in the PPE test; Table 4), while chimpanzees, orangu-
tans, and gibbons (the more arboreal hominoids) fall below
the line (negative values in the PPE test; Table 4).
The only exception to the pattern described above is a chim-
extremely gracile fibula with no sign of pathology in the skele-
ton. The individual has an estimated body mass of 31 kg, the
lowest of the sample (average female body mass ¼ 40.1 kg;
see Table 1 in Marchi, 2005). The same patterns identified
out this specimen (results not shown). The other captive female
reason for the position of the outlier relative to the other female
chimpanzees is the extremely gracile fibula compared to the
tibia. More data are necessary to determine if this finding is re-
lated to differences in body size and/or locomotion.
In summary, when the two leg bones are compared to each
other, the more terrestrial hominoids (humans and gorillas)
Mean and standard error of tibial and fibular cortical areas (CA) and polar section moduli (Zp) at mid-diaphysis (raw values)
Homo mean (SE)
Pan mean (SE)
Gorilla mean (SE)
Pongo mean (SE)
Hylobates mean (SE)
1Cortical area (mm2) at mid-diaphysis.
2Polar section modulus (mm3) at mid-diaphysis.
D. Marchi / Journal of Human Evolution 53 (2007) 647e655
exhibit a relatively more robust tibia, and the more arboreal
hominoids (chimpanzees, orangutans, and gibbons) exhibit
a relatively more robust fibula.
This study shows that humans possess a stronger tibia rel-
ative to the fibula than do apes, especially with regard to cor-
tical area (Fig. 2a; Table 4). This result is not unexpected
because of the important role of the tibia in weight-bearing
in bipedal locomotion. In fact, although earlier studies sug-
gested that 16.7% of the static load of the lower leg in humans
was carried by the fibula (Lambert, 1971), more recent studies
(Takebe et al., 1984; Goh et al., 1992; Funk et al., 2004) indi-
cate that, with the ankle in a neutral position, the load distri-
bution to the fibula is only about 6e7% of the total force
transmitted through the lower leg. Thus, CSG results are in ac-
cord with studies on the load-bearing role of the fibula in hu-
mans. In particular, because cortical area should primarily
reflect axial load (Ruff and Hayes, 1983), a particularly high
value for this parameter (Fig. 2a) was expected in the human
The relatively more robust fibula of apes also appears to be
a consequence of their locomotor repertoire. Because of the
agility and range of limb motion that arboreality demands,
apes (and primates in general) are characterized by a relatively
mobile fibula (Carleton, 1941; Barnett and Napier, 1953). Hu-
mans, because of their adaptation to habitual terrestrial biped-
alism, have lost much of this freedom in the lower leg (Barnett
and Napier, 1953).
Because of the greater mobility of the fibula and the anat-
omy of their talofibular articulation (Stern and Susman,
1983; Latimer et al., 1987; Gebo, 1992), the apes should
bear a greater amount of load on their fibulae than humans.
In a study conducted on humans, Barnett and Napier (1952)
found that the axis of rotation of the ankle is inclined proximo-
medially to distolaterally during dorsiflexion (dorsiflexion
axis). The authors also found that the mobility of the fibula
is related to the steepness of the dorsiflexion axis (the steeper
the dorsiflexion axis, the more mobile is the fibula) and that
the fibula rotates laterally relative to the tibia during dorsiflex-
ion. In a study of the characteristics of the talocrural joint of
African apes and humans, Latimer et al. (1987) found that
the obliquity of the dorsiflexion axis (called the talocrural
axis in their study) is greater in African apes than in humans.
Such a result suggests a greater degree of dorsiflexion in apes
than in humans. Moreover, behavioral studies have demon-
strated the importance of climbing activitiesdwhich require
greater ankle dorsiflexion than human bipedal locomotiondin
the locomotor repertoire of all apes (Fleagle, 1976, 1980; Sug-
ardjito, 1982; Sugardjito and van Hooff, 1986; Cant, 1987;
Tuttle and Watts, 1985; Hunt, 1992; Remis, 1995; Doran,
1996). Studies of hindlimb-joint angles during bipedal and
quadrupedal walking in chimpanzees (Susman, 1983; Susman
and Brain, 1988; Stern, 2000) also indicate a greater degree of
dorsiflexion in ape locomotion in comparison to human biped-
alism. Thus, following Barnett and Napier (1952), the tor-
sional effect on the fibula produced during dorsiflexion in
African apes will be greater than that in humans, with a conse-
quent increase of mechanical stress on the fibula and, there-
fore, an increase in values for fibular CSG variables.
Greater mechanical stress in ape fibulae is also a conse-
quence of the general orientation of the distal tibia and fibula
of apes compared to humans (Aiello and Dean, 1990), which
is expected to increase load on the ape fibula during locomo-
tion in general. In addition, because of the varus position of the
hindlimb of apes, the bending moments are greater in apes
than in humans (Preuschoft, 1970). In apes, the tibia is more
slender and weaker than in humans and the space between
the fibula and the tibia (spatium interosseum) is wider because
of the more pronounced laterally concave curvature of the tib-
ial diaphysis. As a consequence, the tibia transmits a larger
part of the forces to the fibula in apes than in humans (Preu-
schoft, 1970). Moreover, the larger peroneal muscles (and
the presence of the flexor fibularis muscle) of apes would be
expected to create higher bending loads on the fibula (Stern
and Susman, 1983; Aiello and Dean, 1990; McLean and
Marzke, 1994). Only a few quantitative studies have been
Descriptive statistics for tibial and fibular cortical areas and polar section moduli (Zp) at mid-diaphysis (size-standardized values) of wild-shot and captive chim-
panzees, orangutans, and gibbons
Pan Pongo Hylobates
(SE) (n¼ 6)
(SE) (n ¼2)
1CA¼ln (cortical area tibia/cortical area fibula).
2Zp¼ln (polar section modulus tibia/polar section modulus fibula).
Results of Tukey tests for interspecific comparisons of tibial/fibular percent
prediction errors (PPE)
1PPE¼(observed y?predicted y)/predicted y?100.
2CA¼ln (tibial cortical area/fibular cortical area).
3Letters indicate results of Tukey multiple-comparisons tests: possession
of same letter¼nonsignificant difference (p>0.05) between groups; a¼
highest mean, b¼next highest mean, etc.
4Zp¼ln (tibial polar section modulus/fibular polar section modulus).
D. Marchi / Journal of Human Evolution 53 (2007) 647e655
performed to determine the relative mass of these muscles in
apes and humans (Tuttle, 1970; Thorpe et al., 1999; Payne
et al, 2006). From these studies, it appears that apes have
heavier peroneal muscles than humans. However, all of these
studies have only taken a few individuals into consideration,
and thus a statistical treatment of the results was not possible.
More studies are needed in order to understand the possible
role of the peroneal muscles and flexor fibularis muscle in af-
fecting fibular bending loads.
Even if all apes have generally more robust fibulae com-
pared to tibiae than humans, some interesting differences
among them, related to their different degrees of arboreality,
can be outlined. Gorillas possess the relatively least robust fib-
ula among apes (Table 4). Moreover, gorillas overlap exten-
sively with humans for Zp. The other apes analyzed in this
study (chimpanzees, orangutans, and gibbons) possess rela-
tively (to the tibia) more robust fibulae than gorillas. Chimpan-
zees, orangutans, and gibbons are all highly arboreal species,
yet they have different locomotor behaviors. The grouping
of chimpanzees, orangutans, and gibbons might reflect the
fact that they have a foot-ankle complex with a generalized
structure, which enables them to use a wide variety of locomo-
tor modes and substrates (Vereecke et al., 2005). Therefore,
the fibula of these species is more mobile (Carleton, 1941;
Barnett and Napier, 1953) than that of the more terrestrial go-
rilla. In addition, studies of substrate reaction force in primates
walking in terrestrial and arboreal environments (Schmitt,
2003; Carlson et al., 2005) have demonstrated that primates
bear their limbs in a more adducted position and more fre-
quently exert medially directed side-to-side forces on arboreal
supports than when walking on the ground. Thus, the more ar-
boreal apes (i.e., chimpanzees, orangutans, and gibbons) are
expected, on average, to use more adducted hindlimb postures
than the more terrestrial gorilla, resulting in greater mechani-
cal loading of the fibula.
The position of gorillas relative to the other hominoids stud-
ied here indicates a load-sharing pattern in the lower leg that
falls between that of humans (the only fully terrestrial species
examined here) and those of the other apes (which are charac-
terized by a greater degree of arboreality). Although western
lowland gorillas (the species analyzed in this study) regularly
use arboreal substrates, Remis (1993, 1995, 1997) found that
both sexes of this taxon, but particularly males, travel between
trees primarily terrestrially. In terms of body size, gorillas (es-
pecially males) are far larger than the other apes (Smith and
Jungers, 1997), which requires a less mobile fibula to stabilize
the ankle during terrestrial locomotion (Walmsley, 1918; Car-
leton, 1941; Barnett and Napier, 1953). This, associated with
the fact that the sample studied here is composed mainly of
males, may be the cause of the relatively (to the tibia) lower
fibular cross-sectional properties of gorillas as compared to
the other apes, and of their grouping closer to humans. Body
size may explain the similarities between humans and gorillas
in another way: both are large-bodied primates, and it could be
argued that body size influences relative fibular robusticity. To
test this hypothesis, I compared PPE results of gorilla males
and females (results not shown here). The two sexes are not
significantly different for this comparison (ManneWhitney
U-test). If body mass played a role in the relative robusticity
of the fibula, then there should be differences between male
and female gorillas,given that theestimatedbody mass formales
is more than twice that of females (Marchi, 2005; Table 1).
Therefore, the difference between gorillas and the other
(more arboreal) apes is due to some other fact, and on the basis
of the evidence presented here, it seems that the degree of
arboreality may be a plausible explanation.
Tibial/fibular cross-sectional diaphyseal proportions appear
to be related to differences in positional and locomotor behav-
ior among hominoids. Direct tibia/fibula comparisons are good
indicators of arboreality in hominoids, with the more arboreal
hominoids (chimpanzees, orangutans, and gibbons) possessing
Fig. 2. (a) Comparison of tibial and fibular ln-transformed cortical area (CA) and (b) polar section modulus (Zp) at mid-diaphysis in Homo, Pan, Gorilla, Pongo,
and Hylobates. Cortical area is in mm2, polar section modulus is in mm3. The lines are isometric reference lines centered on the mean x-y of the pooled data set.
D. Marchi / Journal of Human Evolution 53 (2007) 647e655
relatively robust fibulae and the more terrestrial hominoids
(humans and gorillas) possessing relatively robust tibiae.
These results, besides providing CSG characterization of the
fibula, a bone that has previously received relatively little at-
tention, may also be helpful for reconstructing the locomotor
behavior of fossil hominoids.
Fleagle (1979) suggested that the articular surfaces of the
long bones provide more information about the mechanics of
movement of an animal than do other parts of the bone, and
Ruff (2002) demonstrated that long-bone (humerus, radius,
ulna, femur, and tibia) articular and cross-sectional proportions
combined can distinguish between locomotor modes among
primates, at least to the level of broad locomotor differences.
Comparative studies that combine cross-sectional diaphyseal
properties and articular dimensions of the tibiofibular complex
will be useful in further investigating the relationship between
morphology and behavior among hominoids in this anatomical
Many people and institutions contributed time, resources,
facilities, and advice, all of which made this work possible.
To all of the people who made skeletal collections available,
and who assisted me in technical aspects of data collection,
I am very thankful: Paolo Agnelli and Riccardo Mugnai
(‘‘La Specola’’ Museum, Firenze, Italy); Karin Isler and Elisa-
beth Langenegger (University of Zurich, Irchel, Switzerland);
Gisela Grupe and Olav Ro ¨hrer-Ertl (Universita ¨t Mu ¨nchen,
Germany). I express my gratitude to James Funk for providing
important manuscripts on tibial and fibular loading and espe-
cially to Christopher Ruff and Daniel Schmitt for helpful com-
ments during the preparation of the manuscript.
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