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The Structural Rigidity of the Cranium of Australopithecus africanusImplications for Diet Dietary Adaptations and the Allometry of Feeding Biomechanics.

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THE ANATOMICAL RECORD 293:583–593 (2010)
The Structural Rigidity of the Cranium
of Australopithecus africanus:
Implications for Diet, Dietary
Adaptations, and the Allometry of
Feeding Biomechanics
Department of Anthropology, University at Albany, Albany, New York
Department of Mechanical and Industrial Engineering, University of Massachusetts,
Amherst, Massachusetts
Department of Biomedical Sciences, Texas A&M Health Science Center, Baylor College of
Dentistry, Dallas, Texas
Division of Basic Medical Sciences, Mercer University School of Medicine, Macon, Georgia
Department of Anthropology, University of Vienna, Vienna, Austria
Department of Human Evolution, Max-Planck-Institute for Evolutionary Anthropology,
Leipzig, Germany
Department of Scientific Computing, Florida State University, Tallahassee, Florida
Department of Anthropology, Center for the Advanced Study of Hominid Paleobiology,
The George Washington University, Washington, District of Columbia
School of Human Evolution and Social Change, Institute of Human Origins, Arizona
State University, Tempe, Arizona
Department of Anatomy, Kansas City University of Medicine and Biosciences, Kansas
City, Missouri
Department of Biology, Mercer University, Macon, Georgia
Department of Organismal Biology and Anatomy, University of Chicago, Chicago, Illinois
Australopithecus africanus is an early hominin (i.e., human relative)
believed to exhibit stress-reducing adaptations in its craniofacial skeleton
that may be related to the consumption of resistant food items using its
premolar teeth. Finite element analyses simulating molar and premolar
biting were used to test the hypothesis that the cranium of A. africanus
is structurally more rigid than that of Macaca fascicularis, an Old World
monkey that lacks derived australopith facial features. Previously generated finite element models of crania of these species were subjected to isometrically scaled loads, permitting a direct comparison of strain
magnitudes. Moreover, strain energy (SE) in the models was compared after results were scaled to account for differences in bone volume and muscle forces. Results indicate that strains in certain skeletal regions below
Grant sponsor: National Science Foundation (Physical
Anthropology HOMINID Program); Grant numbers: NSF BCS
0725219, 0725183, 0725147, 0725141, 0725136, 0725126;
0725122; 0725078; Grant sponsor: EU FP6 Marie Curie Actions
(EVAN); Grant number: MRTN-CT -2005-019564.
*Correspondence to: David S. Strait, Department of Anthropology, University at Albany, 1400 Washington Avenue, Albany,
NY 12222. Fax: (518) 442-5710. E-mail:
Received 7 January 2010; Accepted 11 January 2010
DOI 10.1002/ar.21122
Published online in Wiley InterScience (www.interscience.wiley.
the orbits are higher in M. fascicularis than in A. africanus. Moreover,
although premolar bites produce von Mises strains in the rostrum that
are elevated relative to those produced by molar biting in both species,
rostral strains are much higher in the macaque than in the australopith.
These data suggest that at least the midface of A. africanus is more rigid
than that of M. fascicularis. Comparisons of SE reveal that the A. africanus cranium is, overall, more rigid than that of M. fascicularis during
premolar biting. This is consistent with the hypothesis that this hominin
may have periodically consumed large, hard food items. However, the SE
data suggest that the A. africanus cranium is marginally less rigid than
that of the macaque during molar biting. It is hypothesized that the SE
results are being influenced by the allometric scaling of cranial cortical
C 2010 Wiley-Liss, Inc.
bone thickness. Anat Rec, 293:583–593, 2010. V
Key words: finite element analysis; skull; hominin; human
evolution; diet; strain; bone
Strain, a measure of deformation, is a useful parameter for estimating bone deformation patterns and the
response of bone to external loads (e.g., Bouvier and
Hylander, 1981; Hylander, 1977, 1984; Hylander et al.,
1991; Hylander and Johnson, 1997). However, there are
nonetheless challenges inherent in using strain to
assess the overall structural performance of skeletal
objects of complex geometry. A major issue is that strain
gauge measurements record local deformations at particular sites on an object (i.e., as recorded from a strain
gage), but in an irregular structure (like a skull) there
can be regions exhibiting very high and also very low
strains (e.g., Hylander et al., 1991; Ross, 2001; Ross and
Metzger, 2004), making it difficult to characterize the rigidity of the entire object from gage data. This problem
becomes more acute when comparing objects of different
shape (e.g., skulls of different species). Even if those
objects are subjected to equivalent loads, the patterning
of local strains may be difficult to interpret, particularly
if different regions exhibit elevated (or reduced) strains
in the different structures (e.g., Skull X exhibits higher
strains than Skull Y in Region A but lower strains in
Region B).
To facilitate comparisons between whole objects
(rather than simply parts of objects), Dumont et al.
(2009) suggested using strain energy (SE) as a measure
of overall structural performance (see also Farke, 2008)
for a slightly different use of SE. SE is equivalent to the
work done on an object by external forces, and thus
encapsulates the net effect of deformations across an
entire structure. Dumont et al. (2009) further laid the
theoretical foundations for controlling and quantifying
the effects of size on SE metrics.
Here, we use SE to evaluate the structural performance of the skulls of two primate species, Macaca fascicularis (an Old World monkey) and Australopithecus
africanus [an extinct hominin (human relative)]. Strait
et al. (2009) recently used finite element analysis (FEA)
to compare feeding biomechanics in these two species.
Their analysis incorporated information about muscle
architecture, muscle activity patterns, bone material
properties, and in vivo bone strain collected in living
primates (Richmond et al., 2005; Ross et al., 2005;
Strait et al., 2005, 2007, 2008, 2009). They tested the
hypothesis that certain derived facial features in A.
africanus were adaptations that structurally reinforced
the face against loads imposed by premolar biting (Rak,
1983). That hypothesis predicts that strain in the anterior face will be elevated during premolar biting, and
that the derived traits (particularly, the position of the
root of the zygomatic arch and the presence of a pillar
of bone running along the nasal margin) will affect either the nature or magnitude of the strains recorded
there. Results were consistent with both predictions
insofar as both von Mises strain and strain energy density (SED) in the anterior face were elevated in both
models during premolar biting (as opposed to biting on
the molars alone or all of the cheek teeth at once), but
that the nature of the deformations of the two models
were different; minimum principal strain (compression)
was much higher than maximum principal strain (tension) in the rostrum of A. africanus, but these variables
had similar magnitudes in M. fascicularis. Strait et al.
(2009) suggested that premolar biting may have been
an adaptively significant behavior in A. africanus and
that such bites may have been used during the ingestion of large, ‘‘hard’’ objects like nuts and seeds (such
objects are more precisely described as being ‘‘stresslimited’’ insofar as they fracture under the application
of high forces; Lucas, 2004).
One counterintuitive aspect of Strait et al. (2009)
results is that they observed that the A. africanus skull
exhibited higher strain and SED density values than the
M. fascicularis skull under all loading regimes. This
might have been unexpected given that the former is
hypothesized to possess derived stress-absorbing facial
traits whereas the latter does not. However, as noted
above, it is difficult to directly compare entire skulls
using localized strain values, and the comparison is further complicated by the fact that the two finite element
models (FEMs) differed in size and were not subjected to
equivalent loads. Here we use principles of isometric
scaling to compare strain and SE in the two models. We
hypothesize that, with appropriate size adjustment, the
cranium of A. africanus is structurally more rigid than
that of M. fascicularis during feeding, particularly when
biting on the premolars.
TABLE 1. Muscle force magnitudes applied to
the finite element models, in Newtons
Finite Element Analysis
FEA is an engineering technique used to examine how
structures of complex design respond to external loads
(e.g., Huiskes and Chao, 1983). In FEA, the structure of
interest (e.g., a skull) is modeled as a mesh of simple
bricks and tetrahedra (finite elements) joined at nodes,
the elements are assigned material properties, certain
nodes are constrained against motion, forces are applied,
and displacements, stresses, and strains at each node and
within each element are calculated. Recent advances in
computer software and imaging technology have made it
possible to capture and digitally reconstruct skeletal geometry with great precision, thereby facilitating the generation of detailed FEMs of bony structures, including
nonhuman vertebrate crania (Dumont et al., 2005; Richmond et al., 2005; McHenry et al., 2007; Rayfield, 2001,
2004, 2005a,b, 2007; Rayfield et al., 2007; Wroe, 2007;
Bourke et al., 2008; Farke, 2008; Moreno et al., 2008;
Pierce et al., 2008; Rayfield and Milner, 2008; Wroe et al.,
2007, 2008; Kupczik et al., 2007, 2009; Moazen et al.,
2008, 2009a,b; Strait et al., 2005, 2007, 2008, 2009). However, the incorporation of realistic muscle forces, bone material properties, modeling constraints, and experimental
bone strain data are equally important components of
FEA that are necessary to ensure biologically meaningful
results (e.g., Richmond et al., 2005; Ross et al., 2005;
Strait et al., 2005; Rayfield, 2007).
The methods used to create, load, constrain, and validate the M. fascicularis and A. africanus models have
been described comprehensively elsewhere (Strait et al.,
2005, 2007, 2008, 2009). Briefly, in both models, computed tomography scans were used as the basis for creating solid models in a computer-assisted-design (CAD)
software package. In the case of A. africanus, additional
modeling steps were necessary to create a composite
skull model consisting of parts of two fossil specimens
and to reconstruct missing or distorted morphology. The
solid models were converted into finite element meshes
in commercially available FEA software. The M. fascicularis model contains 311,057 brick and tetrahedral elements, whereas the A. africanus model contains 778,586
elements. Although the element numbers differ dramatically, the macaque model was meshed here with midside
nodes in facial regions, whereas the australopith model
did not have midside nodes. As a result, the two models
were meshed with similar numbers of nodes (337,073 vs.
303,312, respectively). As a test of mesh density, the
macaque model was also analyzed without midside
nodes, and during molar biting a mesh of 131,293 nodes
produced only a 4% reduction in SE. This suggests that
our models have sufficient mesh density.
In Strait et al. (2009), regions corresponding to different areas of cortical bone in the M. fascicularis model
were assigned orthotropic material properties (elastic
modulus, Poissons’ ratio, and shear modulus) using data
collected from macaques by Wang and Dechow (2006)
(see also Strait et al., 2005, 2007, 2008, 2009). These
properties were not used by them (Strait et al., 2009) in
the A. africanus model because preliminary analyses
(Wang et al., 2006; Dechow, unpublished observations)
Anterior temporalis
Superficial masseter
Deep masseter
Medial pterygoid
Balancing side
Anterior temporalis
Superficial masseter
Deep masseter
Medial pterygoid
M. fascicularis
A. africanus
suggest that the material properties of craniofacial bone
in apes and humans differ subtly from those of Old
World monkeys on a region-by-region basis. Instead, the
A. africanus model was assigned isotropic material properties corresponding to the average of all of the regional
material properties in M. fascicularis. These average
values appear to be similar to the average values in
apes and humans (Dechow, unpublished observations).
Thus, in Strait et al. (2009), the models were assigned
different sets of material properties and those differences have an effect on overall structural rigidity. Because
the objective of this study is to focus more specifically on
the mechanical consequences of shape differences
between the two models, both were assigned the same
set of isotropic properties, thereby eliminating any differences due to those variables. Trabecular bone was
modeled as a volume (rather than as individual trabeculae) using material properties derived from Ashman
et al. (1984).
Force vectors corresponding to the right and left anterior temporalis, superficial masseter, deep masseter, and
medial pterygoid muscles were applied to nodes on the
neurocranium, zygomatic arch, and lateral pterygoid
plate. Vector orientations were determined by considering the relative origins and insertions of each muscle.
Muscle force magnitudes (Table 1) in M. fascicularis
were calculated using a combination of muscle physiologic cross-sectional area and electromyographic data
(Ross et al., 2005; Strait et al., 2005, 2007, 2008, 2009).
These muscle forces reflect the fact that during any
given bite, the muscles act slightly out of phase to each
other and thus are never all simultaneously acting at
peak levels. Strait et al. (2009) applied muscle forces to
the A. africanus model that were calculated using physiological cross-sectional area (PCSA) data gathered from
Pan troglodytes, the common chimpanzee. However, in
this study, a different set of forces was applied to the A.
africanus model (see below). Moreover, to facilitate calculation of SE (see below), muscle forces were applied
using a small number of vectors (20), which likely introduces some displacement artifacts into the FEA results.
Constraints were applied to multiple nodes at the
right and left articular eminences and either the left
molars or left premolars. Muscle forces act to pull the
skull models down onto the constrained nodes, generating reaction forces representing the joint forces at the
temporomandibular joints and the bite force during either molar or premolar biting.
The M. fascicularis model has previously been validated (Strait et al., 2005, 2008, 2009) against bone
TABLE 2. Surface areas and volumes of the
finite element models
M. fascicularis
A. africanus
tural rigidity in the A. africanus and M. fascicularis
Surface area (mm2)
Volume (mm3)
strain data collected during in vivo chewing experiments. Data on maximum shear strain, principal strain
ratio, and the orientation of maximum principal strain
were collected from nodes on the model corresponding to
regions in which experimental data had also been gathered. For most regions and most strain measures, the
FEA-generated data fell within the envelope of values
derived from in vivo experiments, indicating that the
macaque model deforms in a broadly realistic fashion.
Calculation and Comparison of SE
SE in each model is equal to the work done on the
skulls by the muscle forces. This is calculated as onehalf of the sum of the dot products of the muscle force
vectors and the displacements of the nodes at which the
vectors are applied in the x-, y- and z-directions. Some
FEA software packages calculate SE automatically as
part of their standard output, but this was not the case
with the software used here (Algor FEM Pro). Thus,
displacements were extracted from the models and SE
was calculated for each using a spreadsheet program.
This process was simplified by having relatively few
force vectors (and, hence, few nodes from which to collect displacements).
The SE results from the two models cannot be directly
compared because the models are at different scales.
Comparison can occur only after the SE value of one
model is adjusted to control for differences between the
models in bone volume and force (note that ‘‘bone volume’’ excludes the air and soft-tissue filled cavities in
the cranium; Table 2). In the case considered here, the
raw SE value for M. fascicularis was compared to the
scaled SE value for A. africanus. Following Dumont
et al. (2009), the scaled SE value for A. africanus was
calculated as:
Scaled SEA ¼ ðVA = VM Þ1=3 ðFM = FA Þ2 SEA
where SEA, VA, and FA equal the SE of, the bone volume
of, and the forces applied to the A. africanus model,
respectively, and VM and FM represent the bone volume
of and forces applied to the M. fascicularis model. Scaled
SEA represents the SE that would have been observed in
the A. africanus model if it possessed the same volume
and was subjected to the same forces as the M. fascicularis model.
As mentioned, SE is equivalent to work (one-half of
force times displacement), and because the forces have
been equalized, a comparison between scaled SEA and
SEM (the SE of the macaque model) reflects the different
displacements recorded in the two models at the nodes
at which forces are applied. These displacements are
themselves the products of the deformation of each
model as a whole, meaning that the ratio scaled SEA/
SEM records the proportional difference in overall struc-
Muscle Forces in the A. africanus Model
Examination of Eq. (1) reveals that it has a very useful property. Namely, it allows the calculation of scaled
SEA for any set of forces applied to the A. africanus and
M. fascicularis models, so long as the ratio of the forces
applied to the two models is known (Dumont et al.,
2009). In other words, under such conditions, the magnitudes of the forces applied to the A. africanus model will
not affect the value of scaled SEA. This may seem counterintuitive, but imagine a special case in which the
macaque and A. africanus models retained their shapes
but had the same bone volume (i.e., a very large macaque or a very small australopith). Because the ratio of
volumes is equal to one, scaled SEA is purely a product
of the squared ratio of the applied forces. If equivalent
forces were applied to both models, then the ratio of
forces would be equal to one, meaning that the raw SE
values for the two models can be directly compared
because scaled SEA would be equal to raw SEA. Now consider a case in which the forces applied to the A. africanus model were five times greater than those applied to
the M. fascicularis model. The SE in the A. africanus
model will be 25 times greater than that in the macaque
model, because SE is equal to one-half the product of
force and displacement, and in a linearly elastic model
(as employed here) displacement varies in direct proportion to force. In other words, SE increases as a square of
force because work is equal to the area underneath the
force-displacement curve. Returning to Eq. (1), the raw
value of SEA is multiplied by the square of the ratio of
forces, which is now equal to 1/25. Thus, the increase in
SEA caused by the greater forces is cancelled out by the
decrease in the square of the force ratio, meaning that
the value of scaled SEA remains unchanged.
In theory, we could apply the same forces to the two
models as were used by Strait et al. (2009), but this is
problematic in practice because each of the A. africanus
muscle forces differs distinctly from the corresponding
macaque muscle forces (e.g., the force of the anterior
temporalis in A. africanus is 10 times greater than
that in M. fascicularis, but the force of the superficial
masseter is only approximately five times greater). This
variation makes it difficult to calculate the ratio of forces
applied to the two models. Consequently, a new set of
muscle forces was calculated and applied to the FEM of
A. africanus.
Given that any set of forces can be applied to the A.
africanus model for the purpose of examining SE (so
long as the ratio of those forces and the macaque forces
are known), we chose to apply forces such that the differences in the stress states of the two models were
purely a function of shape. Such forces facilitate the calculation of scaled SEA and are useful for comparing
strains. Consider two objects of the same shape but different size, for example, a large and a small version of
the macaque cranium. As shown by Dumont et al.
(2009), if forces are applied to each cranium such that
they maintain the same ratio of force to bone surface
area, then they will be in the same stress state (recall
that stress is equal to force divided by area), meaning
that the strains observed in the two crania will be
identical. Note that in place of bone surface area, one
may substitute bone volume to the two-thirds power.
Now assume that the large macaque cranium has the
same bone surface area as the A. africanus cranium. If
the muscle forces applied to the large macaque were
now applied to the australopith, then the differences
between their stress states and resulting strains would
be a result of shape rather than force. Moreover, recall
that the large and small macaques have identical stress
states. This means that the strains in the small macaque
can be directly compared to those in A. africanus, and
any differences can be attributed directly to the differences in the shapes of the crania [with the caveat that
FEMs of the two crania must be constructed using similar assumptions regarding geometry (i.e., the presence
or absence of particular cavities within the crania)].
Thus, in our FEAs, muscle force magnitudes in the A.
africanus model were calculated by multiplying the macaque magnitudes by the ratio of the surface areas of the
A. africanus and M. fascicularis models (Tables 1 and 2).
This procedure also simplifies the calculation of scaled
SEA, because the ratio of areas in the two models can be
substituted in place of FM/FA in Eq. (1).
Strain maps of the FEAs are presented in Fig. 1. During molar biting, both the M. fascicularis and A. africanus models exhibit high von Mises strains in the
working-side zygomatic root and arch and a complex and
steep strain gradient in the working-side infraorbital
region. Both models exhibit higher strains on the working- than on the balancing-side, and both show low
strains along the supraorbital torus and the nasoalveolar
region (below the nasal aperture). The models differ in
that the macaque shows regions of moderately elevated
von Mises strain on the working-side dorsal rostrum
region (just below the inferior margins of the orbit),
whereas the australopith shows elevated strains in the
Fig. 1. Von Mises strain in the finite element models during molar and premolar biting. A: M. fascicularis model during molar biting. B: A. africanus model during molar biting. C: M. fascicularis model during
premolar biting. D: A. africanus model during premolar biting.
TABLE 3. Strain energy recorded during finite
element analyses, in Newton millimeters
M. fascicularis
Strain energy (SEM)
A. africanus
Strain energy (SEA)
Scaled SEA
Scaled SEA/SEM
FEA of
molar biting
FEA of
premolar biting
postorbital bars and interorbital pillar (just above the inferior margins of the orbit).
During premolar biting, many of the basic strain patterns seen during molar biting remain largely unchanged,
but von Mises strains along the dorsal rostrum, nasal
margin, and lateral rostrum are elevated in both species.
However, the species differ in that the magnitude of those
elevated strains are much higher in M. fascicularis than
in A. africanus.
Strain Energy
Both FEMs exhibited higher SE during premolar than
during molar loading (Table 3). In the macaque model,
SE during premolar bites was 30.6% higher than during
molar bites, whereas in the A. africanus model the difference was 10.2%. As SE increases, structural rigidity
decreases, so these results indicate that premolar bites
are associated with a mechanical cost (decreased rigidity
resulting from increased deformations). However, the
macaque incurs a greater cost than the australopith.
When comparing SE in the macaque model to scaled
SE in the A. africanus model, the A. africanus model
exhibits values that are 4% higher than the macaque
model during molar loading. During premolar loading,
however, the A. africanus model had values that were
12% lower. Thus, compared to M. fascicularis, A. africanus is less rigid during molar biting and more rigid during premolar biting, but A. africanus shows a three
times larger increase in relative rigidity under premolar
loading than the relative decrease in rigidity under
molar loading.
Structural Rigidity
Certain aspects of the results are consistent with the
hypothesis that the A. africanus cranium is more rigid
than the M. fascicularis cranium. Under isometrically
scaled loading conditions, the A. africanus model exhibited lower rostral strains during both types of biting,
suggesting that at least this part of the face is more
rigid in the australopith. High rostral rigidity may
explain why strains in the postorbital bar and interorbital pillar are higher in this species: increased rostral rigidity in A. africanus may have the effect of passing
strains from the mid to the upper face (see also Strait
et al., 2007). Moreover, evidence that SE is lower in A.
africanus than M. fascicularis during premolar biting is
consistent with the hypothesis that aspects of facial
form in A. africanus are adaptations to structurally reinforce the face against premolar-focused bites (Strait
et al., 2009). Strait et al. (2009) have suggested that
these bites may have been used to fracture the shells of
large nuts and seeds that may have been critical resources during periods in which other, more preferred food
items were unavailable (see below).
In contrast, the hypothesis that the A. africanus facial
skeleton is more rigid than that of M. fascicularis is not
corroborated under molar loading. The australopith
model is less rigid (i.e., has a higher SE) during molar
loading than the macaque model. Moreover, in the absence of comparative data (e.g., FEMs of many macaque
individuals) that would allow an assessment of whether
the differences between the species are statistically significant, the only definitive statement that can be made
at present is that the relatively greater australopith rigidity under premolar loading is (three times) greater
(12%) than the relative decrease in australopith rigidity
(4%) under molar loading. The functional significance of
these differences in relative rigidity in the australopith
and macaque models between molar and premolar biting
can be appreciated when one considers the functional
role of muscle recruitment during these two activities.
The ability to generate powerful premolar bites on large,
hard objects such as nuts determines whether an animal
can access a food item. Thus, the goal of premolar biting
plausibly requires recruitment of large amounts of muscle force. This is both required and facilitated by the geometry of the feeding system: that is, the load arm of
the premolars is greater than that of the molars, but the
jaw joints are more stable during premolar biting than
during molar biting (Greaves, 1978; Spencer, 1998). In
contrast, mastication along the molar toothrow acts on
foods already acquired that are being processed for safe
swallowing and is associated with recruitment of less
muscle force than either incisor or premolar biting (Ross
and Hylander, 2000; Ross, unpublished data on Cebus).
Thus, the greater rigidity of the australopith facial skeleton under premolar biting is likely of greater functional
importance than its decreased rigidity under molar
loads. Moreover, a full interpretation of the SE results
may require a consideration of the allometry of cranial
architecture (see below).
Differences in SE values in the A. africanus model
and the M. fascicularis model, appropriately scaled to
account for loading and volume differences, reflect the
differences in the rigidity of the two skull systems under
masticatory loading conditions. To assess and compare
the rigidity of a particular anatomical region (i.e., the
zygomatic arch) with the homologous region in another
skull, one could compute the total SED of the region by
integrating the SED field provided by the finite element
results over the volume of the anatomical region Vi. For
four-noded tetrahedral elements, SED is constant over
the element volume and, therefore,
SEDðx; y; zÞdV ¼
SEVi ¼
SEDe V e
where SED (x,y,z) denotes the SED field, SEDe and Ve
are the SED and volume of element e, and the summation occurs over the Mi elements comprising the volume
Vi. However, differences in performance due to shape
only require accounting for volume and force differences
TABLE 4. Cortical bone thickness (mm) in cranial regions and body mass (kg) in selected primates
Macaca mulattac
Papio anubisc
Pan troglodytesd
Homo sapiensc
Gorilla gorillae
Torus and
bar thicknessa
Mean male
body massb
Mean female
body massb
Values averaged across multiple drill sites in each region, following Wang et al. (2006).
Data from Gordon (2006).
Thickness data from Wang et al. (2006). Values represent means of mixed-sex samples.
Thickness data from a single male chimpanzee.
Thickness data from a single female gorilla.
per Eq. (1) between the two volumetric regions being
compared. The volumes are easily given by the sum of
the element volumes for each region. Unfortunately, in a
generally shaped three-dimensional (3D) region admitting a 3D stress field contained within a larger structure, it is impossible to determine the ‘‘force" carried by
this region. Thus, performances of anatomical regions
based on SE will not allow a simple assessment of the
mechanical impact of shape. Regardless, this could still
be a useful performance measure (e.g., Farke, 2008),
especially if the two systems are scaled to the same total
volume and then subjected to the same total forces.
Then, comparison of strain energies computed for homologous anatomical regions reflects a combination of shape
differences and the relative way forces are transmitted
through the structure.
The muscle forces applied to the A. africanus model
were calculated by ‘‘scaling-up" the M. fascicularis
forces, according to the ratio of surface area in the two
FEMs (i.e., by approximately a factor of 3). However,
even though the muscle forces have been scaled isometrically, it is possible that cranial cortical bone thickness
scales with negative allometry in primates, although
more comparative data are needed to test this possibility. Table 4 summarizes cranial bone thickness and body
mass data in five extant primates. Unfortunately, the
thickness data for two species (Pan troglodytes, Gorilla
gorilla) are preliminary insofar as they are derived from
only one individual in each taxon. Moreover, the cortical
thickness in our A. africanus model is only approximate
(owing to the difficulty in discerning on computer topography scans the boundaries between cortical and matrixfilled trabecular regions), and thus is not presented. The
incomplete nature of the data set therefore precludes
formal regression analysis, but some general patterns
are nonetheless discernable. For example, the very
smallest species (M. mulatta) has moderately to very
thick cortices. Furthermore, within each cranial region,
the species with the thickest cortical bone exhibits values no more than 50% greater than those of the species
with the thinnest cortical bone. In contrast, the species
sampled here vary in body mass by more than an order
of magnitude. Thus, even when taking into account the
fact that thickness increases linearly while mass
increases as a cube, it is clear that variation in bone
thickness does not scale isometrically with bone mass
and may well scale with negative allometry.
Thickness contributes to bone cross-sectional area,
which in turn influences stress, strain, and SE. Thus,
larger primates may be predisposed to having less rigid
crania, because they have proportionally thinner bones.
In this context, the observation that the A. africanus
model exhibits scaled SE within a few percentage points
of the M. fascicularis model may be an indication of the
fact that the A. africanus model, does, in fact, performs
well in responding to feeding loads [although further
study is needed to confirm this (see below)]. Of course,
thickness alone does not describe how bones deform in
response to stress; variation in material properties is
also critical. In this regard, a thin bone that is stiff may
deform to the same degree as a thick bone that is more
compliant (e.g., Wang et al., 2006). Yet, there may be a
delicate balance between bone thickness and stiffness.
There might be two different strategies for increasing
bone or structural strength through either developing
thicker yet less stiff or thinner yet denser bone, suggesting differences in bone adaptation to varying skeletal
geometries and loading regimes at both phylogenetic
and ontogenetic levels (Wang et al., unpublished observations). Thus, there could be regional differences in
how cortical thickness and stiffness interact in macaques
and australopiths, but this is difficult to assess without
better information about general evolutionary patterns
of variation in cortical structure and material properties.
Regardless, the data presented here are sufficient to
suggest that further investigation of the scaling of craniofacial bone thickness is warranted.
The data presented here also explain why Strait et al.
(2009) observed higher magnitude strains in A. africanus than in M. fascicularis. In this analysis, muscle
forces in the former were equal to those in the latter
scaled to approximately a factor of 3; however, in Strait
et al. (2009), the forces of anterior temporalis and superficial masseter in A. africanus were larger by factors of
approximately 10 and 5, respectively. The reason for this
is that A. africanus muscle forces were calculated using
the PCSA of Pan troglodytes, and the PCSAs of these
muscles in chimpanzees are much larger than they are
in macaques. This is consistent with the suggestion of
Anapol et al. (2008) that muscle PCSA scales with positive allometry in catarrhine primates. Thus, the scaling
of PCSA may also be a factor to consider when assessing
the structural performance of primate crania.
The possibility that biomechanical variables like stress,
strain, and SE may be influenced by the scaling of craniofacial bone thickness, and muscle PCSA is a hypothesis
that can be tested by gathering more comparative data
on bone and muscle architecture, and by examining feeding biomechanics using FEA in a wide range of primates.
If supported, the hypothesis has potentially far-reaching
consequences. In particular, it implies that large primates
are predisposed to have structurally less rigid crania in
relation to the forces being applied to them. This, in turn,
suggests that large species that consume resistant food
items ought to be under particularly high selective pressure to evolve stress-reducing adaptations. Australopithecus africanus may be one such species. One way of
testing this possibility is to compare A. africanus to other
primates in the same general size range. In particular,
FEAs comparing A. africanus and P. troglodytes should
eliminate allometry as a confounding variable and allow
a more complete test of the hypothesis that the cranium
of A. africanus is structurally more rigid than those of
primates lacking derived australopith facial features.
Diet and Dietary Adaptations
Strait et al. (2009) suggested that certain derived craniofacial features in A. africanus are adaptations for
feeding on large, hard objects. This statement is not
equivalent to one suggesting that such food items were
frequently consumed by those hominins. The reason for
this discrepancy is that there is a fundamental difference between reconstructing the diet of an extinct organism and explaining why some of its anatomical traits
may have evolved. Although these goals are related, the
methods frequently used to address these two questions
are not equally well-suited to both.
Two widely used methods of dietary reconstruction are
isotopic analysis and dental microwear analysis. Dental
microwear refers to the microscopic damage done to the
surfaces of teeth by the foods (or other items) being consumed. Its principle strength is that it records direct information about the material properties of the objects
being processed by the teeth (e.g., Scott et al., 2005;
Ungar et al., 2008). Its principle weakness is that it is
ephemeral; any given microwear feature may be
replaced by another in a matter of days or weeks (Teaford and Oyen, 1989). In fossils, therefore, microwear is
conservatively interpreted as recording information
about diet only with respect to the days just before the
individual in question died. Given this narrow time window, microwear preserved on any given tooth may not
necessarily reflects the full dietary breadth of an individual or species. To compensate for this, large samples are
needed to maximize the chances of adequately assessing
diet, but in fossil species the potentially confounding
impact of taphonomic bias should not be discounted.
Isotopic analysis examines the chemical signal preserved in mineralized tissues that are left behind by the
food items being consumed (e.g., Schoeninger, 1995).
Strontium/calcium analysis (e.g., Sillen, 1992; Sillen
et al., 1995) provides information about trophic level
(e.g., carnivore, omnivore, and herbivore), but the
method most widely applied to early hominins has been
stable carbon isotope analysis (Lee-Thorp et al., 1994;
Sponheimer and Lee-Thorp, 1999; Sponheimer et al.,
2006; Van der Merwe et al., 2008), which records
whether or not the individual in question consumed either plants that used the C3 or C4 photosynthetic pathways or the animals that ate those plants. The main
strength of carbon isotope analysis is that it, too, pro-
vides direct information about what was eaten. Moreover, the isotopic signal is not replaced; it is preserved in
perpetuity once it has been established (although the
signal can be impaired by diagenesis). A potential weakness is that it, like microwear analysis, provides information only about discrete time periods. Carbon isotope
analyses of early hominins have typically been performed on dental enamel, and the isotopes record dietary
information about the time during which the enamel
was formed. Thus, the time frame of an analysis
depends critically on the method used to collect the
data. Data obtained from large enamel fragments contain dietary information averaged over weeks or months,
whereas data obtained using laser ablation methods
may provide information on the scale of days (e.g., Sponheimer et al., 2006). Of course, the fine-grained time
scale of the laser ablation method is also a strength insofar as it allows the assessment of seasonal fluctuations
in diet (Sponheimer et al., 2006). Regardless, both methods, when applied to primate teeth, only provide information about diet during the individual’s juvenile
period. A second potential weakness of carbon isotope
analysis is that if there is any mixture in the isotopic
signal (i.e., an isotopic signature indicating the presence
of both C3 and C4 foods), then it is impossible to exclude
the possibility that any given food item was eaten.
Dental microwear and isotopic analyses facilitate dietary reconstruction but do not directly explain adaptation. To do the latter, it is necessary to use functional
morphology. Functional morphology (including biomechanics) examines how and why anatomical systems
work (e.g., Bock and von Wahlert, 1965). Its primary
strength is that it, among the three methods discussed
here, is the only one that can provide information about
why a given morphological trait may have evolved [especially when interpreted within a phylogenetic framework
(e.g., Lauder, 1990)]. It is also the only one of the three
that can potentially provide information on both shortand very long term time scales (e.g., bone remodeling vs.
the inheritance of morphology, respectively), although it
may be difficult to disentangle these disparate sources of
morphological change. The primary weakness of functional morphology is that it, in contrast to microwear
and isotopic analysis, only provides indirect information
about diet. In other words, it allows dietary inferences
but does not record specific evidence of the foods that
were eaten.
Given the strengths and weaknesses of the three
methods discussed above, what can be inferred about
diet and dietary adaptations in A. africanus? This species evidently had an isotopically mixed diet (e.g., Sponheimer and Lee-Thorp, 1999). While informative, this
information does not allow us to exclude any given food
item from the diet. With respect to microwear (Scott
et al., 2005; Ungar et al., 2008), A. africanus exhibits
microwear fabrics that vary in anisotropy and have complexity values that are slightly higher than those of
extant primate folivores. However, complexity in this
species is, on average, lower in magnitude and less variable than that observed in extant primates said to ‘‘fall
back" on hard food sources during time periods in which
their preferred foods are unavailable. Scott et al. (2005)
interpret these data to mean that this species fell back
on tough vegetation and that hard objects comprised a
comparatively minor proportion of the diet.
The dietary reconstruction of Scott et al. (2005) might
be accurate [although the possibility that large, hard
objects might not be detectable using microwear analysis
(Lucas et al., 2008; Lawn and Lee, 2009) urges caution],
but this is not equivalent to saying that hard objects
were selectively unimportant dietary variables. Assessment of the latter possibility requires an evaluation of
functional morphology.
Results presented here and elsewhere (Strait et al.,
2009) suggest that the facial skeleton of A. africanus is
well-suited to withstand loads applied to the premolars.
If derived facial traits in this species are adaptations to
withstanding premolar bites, what types of food items
might have been bitten? Assuming that dietary adaptations in A. africanus are related to the consumption of
resistant food items, we can, as a heuristic device, classify food items into a few simple categories so as to facilitate discussion. Resistant foods can be separated into
those that are ‘‘tough" or displacement-limited (foods
that fail when subjected to high displacements; Lucas,
2004) and those that are ‘‘hard" or stress-limited (those
that fail under the application of high forces; Lucas,
2004). Note that the terms ‘‘hard" and ‘‘tough" are
imprecise in this context, because many stress-limited
foods are, in fact, tough (insofar as tough is the opposite
of brittle). Foods may also be classified as being either
small (items that can be positioned anywhere in the oral
cavity without ingestive preprocessing) or large (those
that require ingestive preprocessing before they can be
positioned on the molars).
Given these categories, a functional assessment of early
hominin dental topography argues strongly that displacement-limited foods were not selectively important components of the diet, regardless of how frequently such foods
were consumed. ‘‘Gracile" australopiths, including A. africanus, exhibit reduced shearing crests on their molars
relative to extant African apes (e.g., Ungar, 2004), suggesting that this reduction is, broadly speaking, phylogenetically derived. Hominin premolar occlusal topography
has not been formally studied using advanced methods,
but there is no reason to expect that the same results
would not also be observed. Shearing crests are critical in
primates for processing displacement-limited foods (e.g.,
Kay, 1977; Lucas, 2004), so it is very difficult to argue
that craniodental traits in A. africanus are adaptations
for feeding on such foods because their teeth are evidently not especially well-designed for doing so.
This conclusion applies even if ultimately it can be
shown that occlusal topography in A. africanus is phylogenetically primitive. With the elimination of displacement-limited foods as selectively important variables,
the remaining resistant foods are stress-limited. Small
items seem unlikely to be sources of premolar bites,
because such items can be easily positioned on the
molars, where higher bite forces can typically be generated (Greaves, 1978; Smith, 1978; Spencer, 1998). By
this logic, large, stress limited objects appear most likely
to be the selectively important variables driving the evolution of derived facial form in A. africanus (and, possibly, other australopiths). Such food items include large
nuts and seeds. After cracking the resistant outer shell
with the premolars, the smaller, less resistant seed contents could have been removed manually and positioned
on the molars for mastication. Dominy et al. (2008) have
suggested that bulbs and corms are also hard objects
that may have been selectively important for australopiths, but those foods are hard only in the sense that
they are as stiff as seed kernels; they are orders of magnitude less stiff than many seed shells.
The absence of a hard object microwear signal in A.
africanus may be due to any of several factors: 1) large,
hard objects may not induce microwear, as predicted by
established principles of fracture mechanics (Lucas et al.,
2008; Lawn and Lee, 2009), 2) none of the A. africanus
specimens examined for microwear ate large, hard objects
in the days or weeks before they died, or 3) A. africanus
relied on large, hard objects less frequently than do
extant primate hard object feeders (e.g., fall back episodes
do not occur seasonally but rather are separated by several years). These possibilities can be evaluated through
experimentation, increased sampling, and analysis of
other types of evidence revealing how food items damage
teeth (Lawn and Lee, 2009; Strait et al., 2009).
A. africanus may have habitually eaten tough, displacement-limited vegetation, but the selective importance of those foods is likely to have been less than that
of large, stress-limited foods. That a generalist species
would eat considerable quantities of foods for whose consumption the species is not especially well-designed
should not be surprising; generalist species do not have
to do many things well, they merely have to do many
things adequately. If they do something especially well,
it should reflect a behavior upon which their survival
periodically depends. The early hominin Paranthropus
bosei provides a particularly apt example. Microwear
data gathered from several specimens have been interpreted to suggest that hard objects were not habitually
consumed by this species (Ungar et al., 2008). However,
qualitatively different microwear data have just been
presented for P. boisei from Konso, Ethiopia (Suwa
et al., 2009) that may be consistent with hard object
feeding. Given that dental topography in P. boisei is
more bunodont than that of any other hominin, it would
appear that members of this species in many Rift Valley
localities were eating a fair amount of abrasive, possibly
tough foods in spite of their dental topography. However,
at other localities that exhibit different environmental
conditions (as at Konso; Suwa et al., 1995), their teeth
and faces were well-suited to cope with the challenges of
consuming the hard foods upon which their survival
may have depended.
FEA was used to compare the overall structural performance of the crania of M. fascicularis and A. africanus during feeding. Strain and SE data were consistent
with the idea that the face of this australopith is structurally reinforced to withstand premolar loads. However,
scaled SE in A. africanus was greater than that of M.
fascicularis during molar biting, a result that was inconsistent with the hypothesis that the cranium of the former would be more rigid than that of the latter. A
possible explanation of this finding is that the thickness
of cranial bone may scale with negative allometry in primates. Additional data on bone thickness are needed to
test this possibility, but, if true, an implication is that
analyses of structural rigidity in primate crania will be
easiest to interpret when comparing species within narrow size ranges.
The authors thank Francis Thackeray and Stephanie
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structure, dietary, diet, feeding, adaptation, rigidity, cranium, australopithecus, africanusimplications, biomechanics, allometric
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