Australopithecus anamensis: a finite-element approach to studying the functional adaptations of extinct hominins.
ABSTRACT Australopithecus anamensis is the stem species of all later hominins and exhibits the suite of characters traditionally associated with hominins, i.e., bipedal locomotion when on the ground, canine reduction, and thick-enameled teeth. The functional consequences of its thick enamel are, however, unclear. Without appropriate structural reinforcement, these thick-enameled teeth may be prone to failure. This article investigates the mechanical behavior of A. anamensis enamel and represents the first in a series that will attempt to determine the functional adaptations of hominin teeth. First, the microstructural arrangement of enamel prisms in A. anamensis teeth was reconstructed using recently developed software and was compared with that of extant hominoids. Second, a finite-element model of a block of enamel containing one cycle of prism deviation was reconstructed for Homo, Pan, Gorilla, and A. anamensis and the behavior of these tissues under compressive stress was determined. Despite similarities in enamel microstructure between A. anamensis and the African great apes, the structural arrangement of prismatic enamel in A. anamensis appears to be more effective in load dissipation under these compressive loads. The findings may imply that this hominin species was well adapted to puncture crushing and are in some respects contrary to expectations based on macromorphology of teeth. Taking together, information obtained from both finite-element analyses and dental macroanatomy leads us to suggest that A. anamensis was probably adapted for habitually consuming a hard-tough diet. However, additional tests are needed to understand the functional adaptations of A. anamensis teeth fully.
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ABSTRACT: The East African hominin Paranthropus boisei was characterized by a suite of craniodental features that have been widely interpreted as adaptations to a diet that consisted of hard objects that required powerful peak masticatory loads. These morphological adaptations represent the culmination of an evolutionary trend that began in earlier taxa such as Australopithecus afarensis, and presumably facilitated utilization of open habitats in the Plio-Pleistocene. Here, we use stable isotopes to show that P. boisei had a diet that was dominated by C(4) biomass such as grasses or sedges. Its diet included more C(4) biomass than any other hominin studied to date, including its congener Paranthropus robustus from South Africa. These results, coupled with recent evidence from dental microwear, may indicate that the remarkable craniodental morphology of this taxon represents an adaptation for processing large quantities of low-quality vegetation rather than hard objects.Proceedings of the National Academy of Sciences 06/2011; 108(23):9337-41. · 9.81 Impact Factor
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ABSTRACT: Many researchers have suggested that Australopithecus anamensis and Australopithecus afarensis were among the earliest hominins to have diets that included hard, brittle items. Here we examine dental microwear textures of these hominins for evidence of this. The molars of three Au. anamensis and 19 Au. afarensis specimens examined preserve unobscured antemortem microwear. Microwear textures of these individuals closely resemble those of Paranthropus boisei, having lower complexity values than Australopithecus africanus and especially Paranthropus robustus. The microwear texture complexity values for Au. anamensis and Au. afarensis are similar to those of the grass-eating Theropithecus gelada and folivorous Alouatta palliata and Trachypithecus cristatus. This implies that these Au. anamensis and Au. afarensis individuals did not have diets dominated by hard, brittle foods shortly before their deaths. On the other hand, microwear texture anisotropy values for these taxa are lower on average than those of Theropithecus, Alouatta or Trachypithecus. This suggests that the fossil taxa did not have diets dominated by tough foods either, or if they did that directions of tooth-tooth movement were less constrained than in higher cusped and sharper crested extant primate grass eaters and folivores.Philosophical Transactions of The Royal Society B Biological Sciences 10/2010; 365(1556):3345-54. · 6.23 Impact Factor
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ABSTRACT: Accumulating isotopic evidence from fossil hominin tooth enamel has provided unexpected insights into early hominin dietary ecology. Among the South African australopiths, these data demonstrate significant contributions to the diet of carbon originally fixed by C(4) photosynthesis, consisting of C(4) tropical/savannah grasses and certain sedges, and/or animals eating C(4) foods. Moreover, high-resolution analysis of tooth enamel reveals strong intra-tooth variability in many cases, suggesting seasonal-scale dietary shifts. This pattern is quite unlike that seen in any great apes, even 'savannah' chimpanzees. The overall proportions of C(4) input persisted for well over a million years, even while environments shifted from relatively closed (ca 3 Ma) to open conditions after ca 1.8 Ma. Data from East Africa suggest a more extreme scenario, where results for Paranthropus boisei indicate a diet dominated (approx. 80%) by C(4) plants, in spite of indications from their powerful 'nutcracker' morphology for diets of hard objects. We argue that such evidence for engagement with C(4) food resources may mark a fundamental transition in the evolution of hominin lineages, and that the pattern had antecedents prior to the emergence of Australopithecus africanus. Since new isotopic evidence from Aramis suggests that it was not present in Ardipithecus ramidus at 4.4 Ma, we suggest that the origins lie in the period between 3 and 4 Myr ago.Philosophical Transactions of The Royal Society B Biological Sciences 10/2010; 365(1556):3389-96. · 6.23 Impact Factor
Australopithecus anamensis: A Finite-
Element Approach to Studying the
Functional Adaptations of Extinct
GABRIELE A. MACHO,1* DAISUKE SHIMIZU,1YONG JIANG,2
AND IAIN R. SPEARS3
1Hominid Palaeontology Research Group, Department of Human Anatomy and Cell
Biology, University of Liverpool, Liverpool, United Kingdom
2William Lee Innovation Center, University of Manchester Institute of Science and
Technology (UMIST), Manchester, United Kingdom
3Sport and Exercise Subject Group, School of Social Sciences and Law, University of
Teesside, Middlesbrough, United Kingdom
Australopithecus anamensis is the stem species of all later hominins and
exhibits the suite of characters traditionally associated with hominins, i.e.,
bipedal locomotion when on the ground, canine reduction, and thick-enameled
teeth. The functional consequences of its thick enamel are, however, unclear.
Without appropriate structural reinforcement, these thick-enameled teeth
may be prone to failure. This article investigates the mechanical behavior of A.
anamensis enamel and represents the first in a series that will attempt to
determine the functional adaptations of hominin teeth. First, the microstruc-
tural arrangement of enamel prisms in A. anamensis teeth was reconstructed
using recently developed software and was compared with that of extant
hominoids. Second, a finite-element model of a block of enamel containing one
cycle of prism deviation was reconstructed for Homo, Pan, Gorilla, and A.
anamensis and the behavior of these tissues under compressive stress was
determined. Despite similarities in enamel microstructure between A. ana-
mensis and the African great apes, the structural arrangement of prismatic
enamel in A. anamensis appears to be more effective in load dissipation under
well adapted to puncture crushing and are in some respects contrary to expec-
tations based on macromorphology of teeth. Taking together, information ob-
tained from both finite-element analyses and dental macroanatomy leads us to
suggest that A. anamensis was probably adapted for habitually consuming a
hard-tough diet. However, additional tests are needed to understand the func-
tional adaptations of A. anamensis teeth fully.
© 2005 Wiley-Liss, Inc.
Key words: Australopithecus anamensis; enamel microstruc-
ture; finite-element stress analyses; paleobiology;
F/00025/A; Grant sponsor: the Natural Environment Research
Council; Grant number: NER/A/S/2003/00347.
*Correspondence to: Gabriele A. Macho, Hominid Palaeontol-
ogy Research Group, Department of Human Anatomy and Cell
Biology, University of Liverpool, Liverpool L69 3GE, United
Kingdom. Fax: 44-151-794-5517. E-mail: firstname.lastname@example.org
sponsor:theLeverhulmeTrust;Grantnumber:Received 12 January 2005; Accepted 13 January 2005
Published online 3 March 2005 in Wiley InterScience
THE ANATOMICAL RECORD PART A 283A:310–318 (2005)
© 2005 WILEY-LISS, INC.
The oldest hominins, Orrorin tugenensis, Sahelanthro-
pus tchadensis, and Ardipithecus kadabba, are conten-
tious and both their taxonomic status and phylogenetic
relationships are hotly debated (Balter, 2001; Senut et al.,
2001; Brunet et al., 2002; Wolpoff et al., 2002; Haile-
Selassie et al., 2004). Uncertainties stem from the frag-
mentary nature of the material and the paucity of compa-
rable parts among them, while the polarity of the
characters traditionally associated with hominins (i.e., bi-
pedality, canine reduction, and thick-enameled teeth) has
recently come under scrutiny also. As a case in point,
while enamel thickness is generally considered a defining
feature of hominins, a recent study emphasizes the impor-
tance of canine reduction and morphology over this char-
acter (Haile-Selassie et al., 2004). Less contentious with
regard to its phylogenetic position is A. anamensis at
about 4.2–3.9 Ma from well-dated deposits at Kanapoi and
Allia Bay east of Lake Turkana (Leakey et al., 1995, 1998).
This species shows clear adaptations toward bipedalism,
canine reduction, and thick-enameled teeth (Leakey et al.,
1995, 1998; Ward et al., 1999, 2001) and is generally
regarded the stem species of all later hominins. While the
postcranium clearly indicates that the species was bipedal
when on the ground (Leakey et al., 1995, 1998; Ward et
al., 1999, 2001), the functional consequences of the spe-
cies’ masticatory apparatus remain inconclusive (Ward et
al., 1999, 2001). The cranial features are primitive and in
many respects resemble those of extant great apes (Ward
et al., 1999, 2001), but preliminary analyses, primarily
based on overall tooth size, enamel thickness, and man-
dibular corpus size, led to propositions that A. anamensis
may have exploited a dietary niche different from the
extant great apes as well as from later hominins (Teaford
and Ungar, 2000; Ward et al., 2001). Although thick-
enameled (and larger) teeth are indeed traditionally asso-
ciated with hard object feeding (Kay, 1981), a theoretical
study has shown that such inferences may not necessarily
be warranted (Macho and Spears, 1999). Without struc-
tural reinforcement of its internal structure, thick enamel,
because of its anisotropic structure, is brittle and prone to
failure. Strength and fracture resistance are conferred to
the tissue by differently oriented bundles of prisms (i.e.,
decussation) and by systematic differences in crystal ori-
entation between the prism heads and the interprismatic
matrix (von Koenigswald et al., 1987; Rensberger, 2000).
This overall correlation between the tissue’s ability to
absorb load and its microstructural features is undis-
puted, but the precise relationships are understood only
poorly. Biomechanical tests are destructive and although
they provide information about the bulk behavior of the
tissue, they are unable to pinpoint areas of weaknesses
within the tissue (Popowics et al., 2004). As these areas of
weaknesses occur on a microstructural level (Rasmussen
et al., 1976), they are inaccessible to traditional stress/
strain measurements (e.g., strain gauges). Here we
present a new approach to overcome these difficulties. By
creating finite-element models of virtual test specimens of
deviating (and decussating) enamel of A. anamensis teeth
and by subjecting these models to compressive stress, we
inquire (nondestructively) whether the enamel of A. ana-
mensis may have been adapted to cope with high levels of
stress. In the present study, the loads applied to the
enamel blocks (i.e., perpendicular to the predominant long
axes of the prisms) are not directly related to certain
masticatory functions, but are chosen to test propositions
that the microstructural arrangement may (or may not)
confer strength to the dental tissue irrespective of enamel
thickness. Inferences about the dietary niche of A. ana-
mensis can thus be based on more informed evidence.
MATERIALS AND METHODS
Prior to creating the finite-element models, reconstruc-
tion of the enamel microstructure from naturally broken
surfaces was undertaken using recently developed soft-
ware (Jiang et al., 2003; Macho et al., 2003). Briefly, the
mathematical algorithms underlying the graphic model
are based on the assumption that prism deviation (and
consequently decussation) among primates is brought
about by biophysical processes, i.e., the interplay of secre-
tion of ameloblasts and the cell-cell adhesion among them.
The imbalance of forces thus created at the advancing
enamel front will cause prisms to buckle. However, the
contribution of each of these factors will change over time,
i.e., throughout the lifetime of an ameloblast and from
earlier- to later-forming enamel. Validation of the model’s
predictive capabilities against measured primate speci-
mens using controlled breaks further revealed that there
are systematic differences in prism arrangements be-
tween even closely related species (Jiang et al., 2003;
Macho et al., 2003). Because of the interconnectivity of the
advancing enamel front, however, differences in prism
organization within a tooth (species) are of degree rather
than kind (Macho et al., 2003). This is apparent even on a
macroscopic level, e.g., when inspecting longitudinal
breaks (Fig. 1). In general, the species-specific pattern of
undulation is most strongly expressed toward the cusp,
where enamel is thickest, and least toward the cervical
margin, where prisms tend to be relatively straight. Pre-
liminary analyses also indicate that functional cusps ex-
hibit a higher degree of prism decussation (particularly
through reduced cycle length), although the general pat-
tern of undulation is comparable to that of guiding cusps
(data not shown). These observations may explain the
indicate 100 ?m. Despite changes in morphological appearance apico-
cervically, fundamental differences in prism arrangement are apparent
throughout the length of the break even at the macroscopic level.
Naturally broken teeth of Homo (H) and A. anamensis (A). Bars
AUSTRALOPITHECUS ANAMENSIS AND DIET
tight, statistically significant correlations between prism
undulation and enamel thickness within and between spe-
cies (Fig. 3). Differences in prism arrangement can thus be
successfully exploited for paleobiological and functional
Sample Preparation and Graphic Modeling
Naturally broken enamel surfaces of the following A.
anamensis specimens were lightly etched for 20 sec with
5% HCl and high-resolution casts (PROVIL light, epoxy
resin) were taken for SEM (backscatter) analyses. The
specimens studied are KNM-KP 29287F (rM3), KNM-KP
29287G (lM3), KNM-KP 31715A (lM1/2), KNM-KP 31717C
(lM2), KNM-KP 31721A (rM2), KNM-KP 31721B (lM3)
KNM-KP 31732B (?), KNM-KP 31732B(2) (lM3), KNM-KP
34725F (rI2), KNM-KP 34725J (rI2), KNM-KP 34725N
(lLC), KNM-KP 35839C (lP3), and KNM-KP 35851 (lM2/3).
Not all impressions revealed clear microstructures and
the breaks were not always along clearly defined planes
with regard to the tooth axes. Thus, modeling (Jiang et al.,
2003; Macho et al., 2003) was restricted to only four spec-
imens, but inspection of the other specimens revealed
comparable patterns of prism decussation (Fig. 2). Unfor-
tunately, only a single transverse break was available for
study (KNM-KP 29287F), but this was not very informa-
tive (i.e., broken obliquely and too far cervically). Conse-
quently, the predictions of prism deviation in the tangen-
tial plane must be considered preliminary. Given the
nature of the sample, error margins for the reconstructed
enamel microstructures of A. anamensis are likely to be
greater than they are for the extant species (Jiang et al.,
2003; Macho et al., 2003). Despite this, however, the vir-
tual breaks induced in the graphic models compare well
visually with the appearance of real broken enamel sur-
faces (Fig. 2). Morphological comparisons were made with
previously published data (Jiang et al., 2003; Macho et al.,
2003) (Figs. 2 and 3).
Finite-Element Modeling and Analyses
To determine the biomechanical behavior of the differ-
ent enamels, the graphic models of decussating enamel
from comparable regions of the guiding cusps of A. ana-
mensis, Pan troglodytes, Gorilla gorilla, and Homo sapiens
were converted to composite finite-element models. The
geometry of the three-dimensional models, taken from the
(mid)crown area of guiding cusps, was imported into MSC-
.Mentat, the finite-element preprocessing software (MSC
Software, 2002). This process involved recreating prism
cross-sections (x-y plane) and extruding the section in the
out-of-plane dimension. The controlling geometry for the
extrusion was a square B-spline imported from the
graphic models (Fig. 2). Each model was then expanded to
create a cuboid enamel block encompassing at least one
full cycle of deviating prisms in the z-y plane for Pan (M1,
126 ?m:140 ?m:695 ?m), Gorilla (M1, 125 ?m:139.5 ?m:
685 ?m), Homo (M3, 246 ?m:270 ?m:1,335 ?m), and
KNM-KP 35851 (M2/3, 232.2 ?m:256 ?m:1,270 ?m); the
longest dimension of each specimen represents the respec-
tive enamel thickness from the dentinoenamel junction
(DEJ) to the outer enamel surface (OES) along the long
axes of the predominant direction of the prisms. The di-
mensions of the enamel blocks were roughly proportional
(i.e., Pan ? 1:1.10:5.52; Gorilla ? 1:1.12:5.48; Homo ?
1:1.10:5.43; A. anamensis ? 1:1.10:5.47).
Each prism path was divided into 28 elements. The
length of these elements was based on the local curvature
of the controlling splines. Hence, elements in regions of
high prism deviations are shorter in length than those in
regions of low deviations (Fig. 2). In cross-section, each
prism consists of four elements (Fig. 4, Table 1). Following
Spears (1997), different properties were assigned to each
element to take into account differences in crystal orien-
tation (Fig. 4, Table 1).
On a microstructural level, enamel is made up of a
complex arrangement of enamel prisms, whereas on an
ultrastructural level, enamel is composed of differently
oriented hydroxyapatite crystals held together by an inor-
ganic matrix. Given that the crystals are considerably
stiffer than the matrix, enamel (as most biological mate-
rials) behaves in a complex manner. Specifically, in cases
where loads are applied along the direction of the crystals,
most of the internal stresses are carried by the crystals
and hence the behavior of enamel is similar to that of
crystals (i.e., higher stiffness). In contrast, when loads are
applied across the direction of crystals, most of the inter-
nal stresses are carried by the inorganic matrix and the
behavior of enamel in this direction is more similar to that
of the matrix. Consequently, the stiffness of enamel is
different in different directions, i.e., it is anisotropic with
respect to stiffness. For modeling purposes, this behavior
of enamel can be simplified by assuming that the crystals
are oriented in parallel within a small region, i.e., within
one element (Fig. 4). This allows enamel to be modeled
with orthotropic (i.e., a simple representation of anisot-
ropy) behavior, in which the material properties are de-
fined along three directions [x-, y-, and z-axes; Fig. 4,
Table 1; see also Shimizu et al. (2005) for more details].
The orientation of crystals within each element was de-
fined following Waters (1980) (Fig. 4) and the local prop-
erties were calculated using equations based on composite
theory (Fung, 1977).
For validation, a small piece of straight enamel was
created and its biomechanical behavior (i.e., Young’s mod-
uli) was appraised against published experimental data
(Craig et al., 1961; Stanford et al., 1960; Xu et al., 1998).
When comparing the data in Figure 4, it needs to be borne
in mind that these experimental studies either did not
specify the loading direction (Stanford et al., 1960) or did
not test the tissue’s behavior in the y-direction. However,
as regards the tissue’s behavior in the x- and z-direction,
the finite-element results obtained in our validation ex-
periments compare well with those derived from experi-
mental studies; using paired t-tests, the results are sta-
tistically significant at the 0.5% probability level (Fig. 4).
With these results being satisfactory, each model of de-
cussating enamel was expanded by 20% to add a dentine
block at the DEJ, with an isotropic Young’s modulus of
16.6 GPa (Macho and Spears, 1999). The total number of
elements for each model is thus Pan ? 257,869; Gorilla ?
168,784; Homo ? 288,601; A. anamensis ? 272,503. These
models were then subjected to an applied pressure of 1
MPa as predicted to occur during human mastication (Fer-
nandes et al., 2003), which was applied perpendicular to
the predominant direction (i.e., y-direction) of the enamel
block. The model was fixed inferiorly at the x-z plane. Due
to lateral deflection induced by the load employed and
microstructural inhomogeneities, tensile stresses across
the prisms occurred. Such internal tension arises under
compressive loads that would occur during mastication
MACHO ET AL.
and are potentially harmful to the structure of enamel
(Rensberger, 2000) and the relative build-up of these
stresses is therefore reported for comparative purposes
Limitations of Finite-Element Models
It should be noted that there are several limitations
with regard to the finite-element models and the valida-
tion process, which may or may not be overcome in the
future. With regard to the models, it is assumed that the
crystal orientation between prism head and interpris-
matic matrix (IPM) and the chemical composition of the
enamel matrix are the same for all species and throughout
the tissue (Cuy et al., 2002). Also, the structural detail of
the simulated dentine and the DEJ (Marshall et al., 2001,
2003) is simplistic when compared to that of enamel. How-
pithecus anamensis. A: The planes are illustrated on a schematic tooth
and a reconstructed enamel specimen is shown. The curves in the
tangential plane (i.e., x-y plane) are highlighted by arrows and compared
with the appearance on an SEM picture in longitudinal plane. The right-
Reconstruction of prism deviation (decussation) in Australo-
hand picture shows a cycle of prism undulation in superior view, while
the arrow indicates that the entire enamel front is pushed toward one
side (although the degree varies among specimens). B: The recon-
structed curves of prisms are shown along the x-z plane and the y-z
AUSTRALOPITHECUS ANAMENSIS AND DIET
ever, preliminary analyses indicate that due to the rela-
tively low stiffness and direction of loading, detailed mod-
eling of the structure of dentine and the DEJ does not
affect stress distribution within the enamel. Hence, an
isotropic Young’s modulus (E ? 16.6 GPa) was considered
sufficient to represent this behavior (Spears and Macho,
1998). A more important limitation of the model in terms
of the calculations of stress is the constraints assigned
along the x-z plane. Ideally, in order to overcome this
limitation, the whole tooth (or at least a larger piece of
enamel) would have to be modeled. However, given the
level of detail used in our microstructural modeling (to-
gether with current computational limits), this is not pos-
sible at present.
With regard to the validation process, it is noteworthy
that although the overall deformation behavior of the
model compares well with that in experiments, data do not
exist (and cannot be obtained through traditional biome-
chanical testing, e.g., strain gauges) with which to com-
pare the magnitudes of internal stress (i.e., at the ultra-
structural level). In other words, as the localization of
stress occurs on a prismatic level, strain gauges would
have to be smaller than the dimensions of the prisms in
order to measure stresses.
With regard to the loading conditions prescribed, only
compressive stress was applied to the enamel blocks. De-
pending on the diet and stage of the chewing cycle, the
direction and position of external loads on the teeth will
vary. In this first article, it is hoped that blocks would be
tested under the type of stress that would mainly occur
when guiding cusps are subjected to vertical cusp-tip
loads. However, during later phases of chewing, the func-
tional cusps will undergo loading and the guiding cusps
may become loaded laterally and may be subjected to
bending. Consequently, the compressive loads applied in
the present study do not represent the range of loads
occurring during mastication. Also, the static nature of
the model is restricting its use to predict fracture initia-
tion. Therefore, the possibility that these localized cracks
propagate through the structure and may threaten the
integrity of the animal is based on our subjective interpre-
tation of localized stresses.
Taken together, the predictions of actual values of
stress, although based on well-proven algorithms, should
remain theoretical. However, it should also be noted that
by maintaining consistency in all aspects other than prism
orientation, the relative magnitudes and locations of
stress are suitable for comparative purposes, although
caution should be adopted when making inferences about
In the transverse plane (x-z plane) and in comparable
regions within the tooth, prism deviation in A. anamensis
appears to be comparable to that in Pan, but in the lon-
gitudinal (y-z) plane, A. anamensis more closely resembles
Gorilla (Fig. 2, Table 2). The similarities in the longitudi-
nal plane are in part brought about by undulations of
prisms in a tangential plane, i.e., in the x-y plane close to
the DEJ; this is similar between A. anamensis and goril-
las. In terms of enamel thickness, A. anamensis is close to,
or exceeds, modern humans in the regions studied (Table
2). Yet relative prism deviation is relatively low in A.
anamensis, such that the overall scaling between enamel
thickness and true prism length follows the relationship
found in the great apes, rather than the thick-enameled
humans (Fig. 3). This may indicate relatively little de-
cussation in this species, which may render the tissue
prism lengths are given. The regression lines are forced through the
origin (? 0). Note that A. anamensis has the same scaling relationship as
the extant African apes, which differs at the 0.1% probability level from
that of the thick-enameled Homo sapiens.
The scaling relationships between enamel thickness and true
a single prism being highlighted. In B, the crystal orientation for the
elements is shown. C gives the results of the validation procedure.
Experimental data are taken from (1) Stanford et al. (1960), (2) Craig et al.
(1961), and (3) Xu et al. (1998). Results of a paired t-test indicate that the
results obtained from the finite-element model do not differ from those
Geometry of the finite-element model (A) with the elements of
MACHO ET AL.
susceptible to fracture. To test these propositions, finite-
element models of virtual enamel specimens from compa-
rable regions of the guiding cusps were created and com-
pressed along the y-direction, i.e., perpendicular to the
direction of greatest stiffness (Shimizu et al., 2005), where
potentially damaging tensile stresses across prisms would
TABLE 1. Element size and material properties used to create the finite-element models*
Dimensions of elements for each prism (?m)
Crystal orientation within each element (degrees)
Young’s modulus (E/GPa)32.1 32.1109
Shear modulus (G/GPa)13.6 3131
0.313Poisson’s ratio (?)
*See Figure 4 for key.
models are scaled to the same size and a longitudinal section through
the middle of the enamel block is shown. Tensile stresses (i.e., maximum
principal stresses) are reported. Note the blue regions indicate no tensile
Results of the finite-element stress analyses are shown. Allstress in any plane. Peak tensile stresses (yellow contours) reach similar
levels but the locations (and directions across prisms) differ between
AUSTRALOPITHECUS ANAMENSIS AND DIET
be expected to be highest (Rasmussen et al., 1976). Differ-
ences in prism attitude between species, which would
affect the behavior of the tissue during mastication, were
not taken into account. Consequently, the models pre-
sented here and the inferences drawn should be regarded
as preliminary accounts of the strength of these different
tissues (Fig. 5).
The maximum principal stresses yielded in the analyses
are comparable among species, but there are differences in
location and relative distribution within the tissue (Figs. 5
and 6). More importantly, however, enamel is particularly
susceptible to fracture when internal tension develops
between prisms with the stress acting across their orien-
tation (Rasmussen et al., 1976); this would result in
prisms being torn apart. The magnitudes of such tensile
stresses perpendicular the long axes of prisms (i.e., those
with the greatest damage potential and which are also
perpendicular to the direction of load) are considerably
lower in A. anamensis and Gorilla than they are in either
Homo or Pan (Fig. 7) and they are also relatively localized
close to the DEJ.
Features to be expected in the earliest human ancestors
are a bipedal mode of locomotion when on the ground,
canine reduction, and thick-enameled teeth (Cela-Condo
and Ayala, 2003). Changes in locomotor capabilities argu-
ably have profound implications for the animal’s behavior,
but shifts in dietary capabilities may be of similar or even
greater importance, especially where later species of Aus-
tralopithecus are concerned (Teaford and Ungar, 2000).
Changes in masticatory performance not only allowed
early hominins to exploit varied food sources commonly
associated with increased climatic fluctuations (Teaford
and Ungar, 2000), but to partition the environment among
Teeth are most commonly preserved in the fossil record
and, given their direct involvement in the breakdown of
spaced cross-sections of the model by taxon (A). In order to deter-
mine the stress concentration throughout enamel, the number of
nodes exhibiting the highest stress (e.g., 20% across the entire
model; darkest shading) was determined and expressed as a per-
centage of the total number of nodes at this cross-section (B). This
was also done for 40%, 60%, and 80%. Stress is most localized in A.
anamensis and least in Pan troglodytes.
Maximum values of tensile stress are plotted at equally
prisms, which are considered to be potentially most damaging, are
plotted. Stresses are lowest in A. anamensis and, again, also most
The maximum tensile stresses acting across the long axes of
MACHO ET AL.
food, are the structures on which inferences about dietary
adaptations are usually based. Perhaps even more impor-
tantly, teeth concentrate stress and must withstand the
forces created by the muscles of mastication; they may
thus provide a more reliable signal about the masticatory
performance than the bony structures overlying them.
Regardless, tooth size, shape, and enamel thickness con-
tain both phylogenetic and functional information (Janis
and Fortelius, 1988). For example, with regard to the
thick enamel of hominins, both the polarity of enamel
thickness (Haile-Selassie et al., 2004) and its functional
consequences remain unresolved (Macho and Spears,
1999; Ward et al., 1999, 2001; Wood and Strait. 2004),
thus making it difficult to address paleobiological ques-
tions. To contribute toward resolving these issues, enamel
microstructure in A. anamensis teeth was reconstructed
and the virtual models thus created were then subjected to
biomechanical tests using finite-element stress analyses.
Enamel microstructure of A. anamensis teeth shows a
unique combination of features not seen in any of the
extant hominoids studied (Fig. 2, Table 2). Despite its
thick enamel, however, prism deviation in this hominin is
relatively low, resulting in the scaling relationship be-
tween projected prism length (i.e., enamel thickness) and
true prism length being the same as in the great apes (Fig.
3). Although it could be argued from a phylogenetic per-
spective that the similarities in enamels between A. ana-
mensis and the African apes may have been expected,
such scaling relationships are surprising from a functional
perspective: the results could imply only moderate cross-
ing-over of bundles of prisms, i.e., little decussation, and
hence low resistance to crack propagation. However, given
the complex manner in which bundles of prisms are ar-
ranged in A. anamensis, this need not be the case.
Under the same applied compressive stress, the magni-
tudes of maximum tensile stress are comparable among
species (Figs. 5 and 6), but the magnitude and location of
stress concentration acting across prisms differ markedly
between taxa (Fig. 7). As regards the latter, overall stress
concentration is lowest in A. anamensis and Gorilla and is
concentrated close to the DEJ, especially in A. anamensis.
Given the large degree of decussation in this region as well
as the region’s close proximity to the crack-preventing
mechanism of the DEJ (Marshall et al., 2001, 2003), it is
improbable that any cracks initiating in this part will
propagate through the enamel structure. In contrast, Pan
and Homo have the highest tensile stresses away from the
DEJ (i.e., in regions of lower decussation) and conse-
quently may be more prone to fracture. Cracks initiating
at these sites could travel easily through the outer enamel
part where prisms are relatively straight, especially in
modern humans (Jiang et al., 2003). These results make
evident that prism deviation per se is only a poor predictor
of the biomechanical behavior of the tissue, whereas the
complex three-dimensional arrangement of prisms with
regard to the direction of load appears to be more infor-
Despite similarities in enamel microstructure and over-
all magnitude and concentration of stresses in A. anamen-
sis and Gorilla, there are fundamental differences be-
reconstruction of the dietary adaptations of A. anamensis.
Compared with chimpanzees, gorillas are adapted to a
more fibrous, relatively tough and varied diet (Kuroda et
al., 1996), with their high-cusped, thin-enameled molars
providing sufficient shearing crests to cope with such a
fibrous diet (Kay, 1977). Conversely, A. anamensis teeth
are thick-enameled, low-cusped, and show a greater de-
gree of asymmetry than those of the great apes (Ward et
al., 1999). The results of the present analyses indicate that
under the loads employed (i.e., compressive stress), the
enamel of A. anamensis is apparently well adapted to cope
with high loads acting predominantly across the long axes
of prisms. Other factors being equal, it could be argued
that this hominin species presumably coped with high
loads occurring during phase 1 of the chewing cycle, i.e.,
puncture crushing, thus supporting propositions that A.
anamensis was adapted to a hard-brittle diet. However,
such inferences may be premature in light of the fact that
the enamel blocks were not tested under all types of stress
occurring during mastication (e.g., shear stress). Perhaps
even more important, they are also rendered questionable
when other factors are considered. As a case in point, the
greater asymmetry of teeth when compared to the great
apes (Ward et al., 1999) would suggest a greater lateral
excursion of the mandible (Spears and Macho, 1998; Ma-
TABLE 2. Comparisons of the prism paths between A. anamensis and extant
Frequency (x-z plane)
Amplitude (x-z plane)
Frequency (y-z plane)
Amplitude (y-z plane)
Distribution across length (x-z)
Prism path relative to enamel thickness
Frequency (x-z plane)
Amplitude (x-z plane)
Frequency (y-z plane)
Amplitude (y-z plane)
Distribution across length (x-z)
Possible tangential curves
*Data taken from Macho et al. (2003).
Homo/Gorilla ? Pan/A. anamensis
Homo ? Pan/A. anamensis ? Gorilla
Gorilla/A. anamensis ? Pan ? Homo
Homo ? Pan ? Gorilla/A. anamensis
A. anamensis ? Homo ? Pan ? Gorilla
Pan/Gorilla/A. anamensis ? Homo
Gorilla ? Homo ? Pan ? A. anamensis
Homo ? Pan ? A. anamensis ? Gorilla
Gorilla ? Pan ? A. anamensis ? Homo
Homo ? Pan ? Gorilla ? A. anamensis
Pan/Gorilla/A. anamensis ? Homo
A. anamensis (?) ? Gorilla ? Pan ? Homo
AUSTRALOPITHECUS ANAMENSIS AND DIET
cho and Spears, 1999) in this species, which would be
required when breaking down tough foods. Hence, when
the evidence is considered together, it would seem most
parsimonious at present to propose that A. anamensis
habitually consumed hard-tough (rather than hard-brit-
tle) foods, while the thick enamel in A. anamensis may
have been an adaptation toward wear resistance.
To summarize, although steps are taken to reconstruct
the enamel microstructure both accurately and repeat-
edly, and to subject these virtual models to well-proven
tests used in engineering, the functional interpretations
must still be regarded preliminary. However, the results
yielded from such analyses in conjunction with informa-
tion derived from the macromechanics of the teeth allow
more convincing inferences regarding the habitual diet of
The authors thank the Trustees of the National Mu-
seum of Kenya. Dr. Meave Leakey generously supported
the study, provided access to the material, and made use-
ful comments on the manuscript. Thanks to Dr. Callum
Ross for the invitation to contribute this manuscript.
Balter M. 2001. Scientists spar over claims of earliest human ances-
tor. Science 291:1460–1461.
Brunet M, Guy F, Pilbeam D, Talsso Mackaye H, Likius A, Ahounts D,
Beauvillain A, Blondel C, Bocherens H, Boisserie J-R, De Bonis L,
Coppens Y, Dejax J, Denys C, Duringer P, Eisenmann V, Fanone G,
Fronty P, Geraads D, Lehmann T, Lihoreau F, Louchart A, Maha-
mat A, Merceron G, Mouchelin G, Otero O, Pelaez Campomanes P,
Ponce de Leon M, Rage J-C, Sapanet M, Schuster M, Sudre J, Tassy
P, Valentin X, Vignaud P, Viriot L, Zazzo L, Zollikofer C. 2002. A
new hominid from the Upper Miocene of Chad, Central Africa.
Cela-Conde CJ, Ayala FJ. 2003. Genera of the human lineage. Proc
Natl Acad Sci USA 100:7684–7689.
Craig RG, Peyton FA, Johnson DW. 1961. Compressive properties of
enamel, dental cements and gold. J Dent Res 40:936–945.
Cuy JL, Mann AB, Livi KJ, Teaford MF, Weihs TP. 2002, Nanoinden-
tation mapping of the mechanical properties of human molar tooth
enamel. Arch Oral Biol 47:281–291.
Fernandes CP, Glantz P-OJ, Svensson SA, Bergmark A. 2003. A novel
sensor for the bite force determinations. Dent Mat 19:118–126.
Fung YC. 1977. A first course in continuum mechanics, 2nd ed. Engle-
wood Cliff, NJ: Prentice-Hall.
Haile-Selassie Y, Suwa G, White TD. 2004. Late Miocene teeth from
Middle Awash, Ethiopia, and early hominid dental evolution. Sci-
Janis CM, Fortelius M. 1988. On the means whereby mammals
achieve increased functional durability of their dentitions, with
special reference to limiting factors. Biol Rev Camb Phil Soc 63:
Jiang Y, Spears IR, Macho GA. 2003. The three-dimensional visual-
isation model of prismatic enamel: an aid to interpreting fractured
surfaces on a micro-structural level. Arch Oral Biol 48:449–457.
Kay RF. 1977. The evolution of molar occlusion in the Cercopithecidae
and early Catarrhines. Am J Phys Anthrop 46:327–352.
Kay RF. 1981. The nut-cracker: a new theory of the adaptations of the
Ramapithecinae. Am J Phys Anthrop 55:141–151.
Kuroda S, Nishihara T, Suzuki S, Oko RA. 1996. Sympatric chimpan-
zees and gorillas in the Ndoki Forest, Congo. In: McGrew WC,
Marchant LF, Nishida T, editors. Great ape societies. Cambridge:
Cambridge University Press. p 71–81.
Leakey MG, Feibel CS, McDougall I, Walker A. 1995. New four-
million-year-old hominid species from Kanapoi and Allia Bay, Ke-
nya. Nature 376:565–571.
Leakey MG, Feibel CS, McDougall I, Ward C, Walker A. 1998. New
specimens and confirmation of an early age of Australopithecus
anamensis. Nature 393:62–66.
Macho GA, Spears IR. 1999. The effects of loading on the biomechani-
cal behaviour of molars of Homo, Pan and Pongo. Am J Phys
Macho GA, Jiang Y, Spears IR. 2003. Enamel microstructure: a truly
three-dimensional structure. J Hum Evol 45:821–830.
Marshall GW, Balooch M, Gallagher RR, Gamsky SA, Marshall SJ.
2001. Mechanical properties of the dentinoenamel junction: AFM
studies of nanohardness, elastic modulus, and fracture. J Biomed
Mat Res 54:87–95.
Marshall SJ, Balooch M, Habelitz S, Balooch G, Gallagher R, Mar-
shall GW. 2003. The dentin-enamel junction: a natural, multilevel
interface. J Eur Ceramic Soc 23:2897–2904.
Popowics TE, Rensberger JM, Herring SW. 2004. Enamel microstruc-
ture and microstrain in the fracture of human and pig molar cusps.
Arch Oral Biol 49:595–605.
Rasmussen ST, Patchin RE, Scott DB, Heuer AH. 1976. Fracture
properties of human enamel and dentin. J Dent Res 55:1362–1368.
Rensberger JM. 2000. Pathways to functional differentiation in mam-
malian enamel. In: Teaford MF, Smith MM, Ferguson MWJ, edi-
tors. Development, function and evolution of teeth. Cambridge:
Cambridge University Press. p 252–268.
Shimizu D, Macho GA, Spears IR. 2005. Effect of prism orientation
and loading direction on contact stresses in prismatic enamel of
primates: implications for interpreting wear patterns. Am J Phys
Anthrop (in press).
Senut B, Pickford M, Gommery D, Mein P, Cheboi K, Coppens Y.
2001. First hominid from the Miocene (Lukeino Formation, Kenya).
C R Acad Sci 332:137–144.
Spears IR. 1997. A three-dimensional finite-element model of pris-
matic enamel: a re-appraisal of the data on the Young’s Modulus of
enamel. J Dent Res 76:1690–1697.
Spears IR, Macho GA. 1998. Biomechanical behaviour of modern
human molars: implications for interpreting the fossil record. Am J
Phys Anthrop 106:467–482.
Stanford JW, Weigel KV, Paffenbarger GC, Sweeney WT. 1960. Com-
pressive properties of hard tooth tissues and some restorative ma-
terials. J Am Dent Assoc 60:746–756.
Teaford MF, Ungar PS. 2000. Diet and the evolution of the earliest
human ancestor. Proc Natl Acad Sci USA 97:13506–13511.
von Koenigswald W, Rensberger JM, Pfretzschner HU. 1987. Changes
in the tooth enamel of early Palaeocene mammals allowing dietary
diversity. Nature 328:150–152.
Ward C, Leakey M, Walker A. 1999. The new hominid species Aus-
tralopithecus anamensis. Evol Anthrop 7:197–205.
Ward C, Leakey M, Walker A. 2001. Morphology of Australopithecus
anamensis from Kanapoi and Allia Bay, Kenya. J Hum Evol 41:
Waters NE. 1980. Some mechanical and physical properties of teeth.
In: Vincent JVF, Curry JD, editors. The mechanical properties of
biological materials. Cambridge: Cambridge University Press. p
Wolpoff MH, Senut B, Pickford M, Hawks J. 2002. Sahelanthropus or
“Sahelpithecus.” Nature 419:581–582.
Wood B, Strait D. 2004. Patterns of resource use in early Homo and
Paranthropus. J Hum Evol 46:119–162.
Xu HHK, Smith DT, Jahanmir S, Romberg E, Kelly JR, Thompson
VP, Rekow ED. 1998. Indentation damage and mechanical proper-
ties of human enamel and dentin. J Dent Res 77:472–480.
MACHO ET AL.