Journal of Human Evolution 61 (2011) 89e96
Contents lists available at ScienceDirect
Journal of Human Evolution
journal homepage: www.elsevier.com/locate/jhevol
Adaptation to hard-object feeding in sea otters and hominins
Paul J. Constantino a, *, James J.-W. Lee b, Dylan Morris b, Peter W. Lucas c, Adam Hartstone-Rose d,
Wah-Keat Lee e, Nathaniel J. Dominy f, Andrew Cunningham c, Mark Wagner g, Brian R. Lawn a, b
a
Department of Biology, Marshall University, 1 John Marshall Drive, Huntington, WV 25755, United States
Ceramics Division, National Institute of Standards and Technology, Gaithersburg, MD, United States
c
Center for the Advanced Study of Human Paleobiology, Department of Anthropology, The George Washington University, Washington, D.C., United States
d
Department of Biology, Pennsylvania State Altoona, Altoona, PA, United States
e
Advanced Photon Source, Argonne National Laboratory, Argonne, IL, United States
f
Department of Anthropology, Dartmouth College, Hanover, NH, United States
g
Department of Engineering, The George Washington University, Washington, D.C., United States
b
a r t i c l e i n f o
a b s t r a c t
Article history:
Received 19 July 2010
Accepted 8 February 2011
The large, bunodont postcanine teeth in living sea otters (Enhydra lutris) have been likened to those of
certain fossil hominins, particularly the ’robust’ australopiths (genus Paranthropus). We examine this
evolutionary convergence by conducting fracture experiments on extracted molar teeth of sea otters and
modern humans (Homo sapiens) to determine how load-bearing capacity relates to tooth morphology
and enamel material properties. In situ optical microscopy and x-ray imaging during simulated occlusal
loading reveal the nature of the fracture patterns. Explicit fracture relations are used to analyze the data
and to extrapolate the results from humans to earlier hominins. It is shown that the molar teeth of sea
otters have considerably thinner enamel than those of humans, making sea otter molars more susceptible to certain kinds of fractures. At the same time, the base diameter of sea otter first molars is larger,
diminishing the fracture susceptibility in a compensatory manner. We also conduct nanoindentation
tests to map out elastic modulus and hardness of sea otter and human molars through a section
thickness, and microindentation tests to measure toughness. We find that while sea otter enamel is just
as stiff elastically as human enamel, it is a little softer and tougher. The role of these material factors in
the capacity of dentition to resist fracture and deformation is considered. From such comparisons, we
argue that early hominin species like Paranthropus most likely consumed hard food objects with
substantially higher biting forces than those exerted by modern humans.
Ó 2011 Elsevier Ltd. All rights reserved.
Keywords:
Tooth morphology
Fracture
Wear
Diet
Dental evolution
Enamel mechanical properties
Introduction
Early hominins of the genus Paranthropus had what has been
termed a ’robust’ masticatory apparatus that included large jaws
and anteriorly positioned musculature, along with very large
postcanine teeth with low and rounded (bunodont) cusps (Rak,
1983). Similar tooth morphology has been noted in extant sea
otters (Fisher, 1941) (Fig. 1). This has led to the proposition that sea
otter dentition may serve as a useful model for inferring the eating
habits of Paranthropus (Walker, 1981). However, no detailed
comparison appears to have been made on the teeth of these
distantly related mammals to assess the degree of morphological,
and, presumably functional, convergence.
* Corresponding author.
E-mail address: [email protected] (P.J. Constantino).
0047-2484/$ e see front matter Ó 2011 Elsevier Ltd. All rights reserved.
doi:10.1016/j.jhevol.2011.02.009
Sea otters (Enhydra lutris) consume a variety of hard foods
including clams, mussels, abalone, snails, crabs, and sea urchins
(Murie, 1940; Kenyon, 1969; Vandevere, 1969; Ostfeld, 1982; Kvitek
et al., 1988; Riedman and Estes, 1990; Watt et al., 2000). In some
populations, individuals target particular prey (Estes et al., 2003;
Tinker et al., 2008; Newsome et al., 2009). However, even in
areas with a high degree of inter-individual dietary variation, all
otters appear to have a “hard food component” to their diet (Estes
et al., 2003; Tinker et al., 2008). Although the contents of some
mollusks are accessed with the aid of stones (Hall and Schaller,
1964), most shelled prey are placed directly in the mouth and
chewed whole (Kenyon, 1969; Vandevere, 1969; Calkins, 1978).
Indeed, the scat of sea otters often contains the remains of mollusk
shells and sea urchin plates and spines (Murie, 1940). During
consumption of the sea urchin masticatory apparatus, Enhydra
actually chews one of the hardest biogenic composites in nature,
Aristotle’s lantern (Wang et al., 1997). Several lines of evidence
90
P.J. Constantino et al. / Journal of Human Evolution 61 (2011) 89e96
Figure 1. Dentition of fossil hominins (Paranthropus boisei), modern humans (Homo
sapiens) and sea otters (Enhydra lutris), left to right. Note similar blunt, rounded
(bunodont) morphology in all species.
suggest that early hominins such as Paranthropus were eating
comparably hard foods (Grine, 1981; Rak, 1983; Demes and Creel,
1988; Hylander, 1988; Constantino, 2007; Constantino et al.,
2009, 2010). The extent to which the tooth structure of Enhydra
and Paranthropus reflects a shared capacity to break down such
hard food objects forms a central theme of the present study.
Accordingly, here we conduct controlled failure tests on
extracted molars of sea otters to quantify sustainable biting forces
for these animals. Analogous tests on modern human molars
provide a useful basis for comparison, not only in determining
relative biting forces but also in illustrating how fracture modes
may depend on differences in tooth morphology. Appropriate
fracture equations serve to account for the observed fracture modes
in terms of characteristic dimensions, namely tooth size (transverse
width or radius) and enamel thickness. Indentation tests on tooth
sections are also conducted to compare key enamel material
properties—modulus, hardness, and toughness. Finally, using the
fracture equations as a predictive tool, we draw inferences about
the diet of Paranthropus boisei, the most derived of the “robust”
australopiths (Constantino and Wood, 2007; Wood and
Constantino, 2007).
However, in some tests (e.g., synchrotron imaging) it was necessary
to use premolars and canines because of size and orientation
constraints imposed by the instrumentation. The human molar
specimens were cleaned and stored in distilled water immediately
after extraction. The sea otter teeth were received frozen but then
stored in aqueous solution for several days before testing. Specimens with noticeable preexisting cracks or other damage incurred
during extraction or storage were eliminated from the sample
population. Individual teeth for fracture testing were mounted
with their roots embedded in epoxy blocks, cusps uppermost.
Thereafter and throughout the subsequent testing procedure, these
teeth were kept moist by continually squirting drops from a water
bottle.
A few human and sea otter molars were sectioned buccolingually along a vertical plane through the most prominent mesial
cusps (protoconid and metaconid in lower teeth and protocone and
paracone in upper teeth). The sectioning was accomplished by
traditional cutting and polishing methods. Examples are shown in
Fig. 2 for (A) sea otters and (B) modern humans. These sections
demonstrate a common bunodont morphology, i.e., rounded and
blunt occlusal surfaces. They also illustrate some important differences, notably a greater tooth base size and thinner enamel coat for
the sea otter. The means and standard deviations of these dimensions measured for the two species, along with some values from
the literature for humans (Kono, 2004) and P. boisei (Beynon and
Wood, 1986; Demes and Creel, 1988), are included in Table 1.
Faintly visible within the enamel in the section views is the
appearance of ’HuntereSchreger bands’ (HS), indicating a crossing
(decussation) of mineralized prisms within the enamel structure,
previously proposed as a source of impedance of cracks that seek
Methods and results
Preparation of tooth specimens
Human molar teeth were provided by the Pfaffenberger Laboratories at the National Institute of Standards and Technology
(NIST). The teeth were extracted from anonymous male and female
patients ranging in age from 18 to 25 years. Approval to test these
specimens was granted by the NIST Internal Review Board. Sea otter
teeth were obtained “from the United States Geological Survey and
Marine Wildlife Veterinary Care and Research Center of the California Department of Fish and Game (CDFG).” These specimens
were extracted from the skulls of deceased animals. Permission to
transport and test the teeth was granted by the CDFG. All remains of
these animals are ultimately to be lodged at the California Academy
of Sciences.
Both lower and upper human molars from each position in the
tooth row (e.g., M1, M2, etc.) were included in the study. For sea
otters, we focused mainly on the lower first molars because of their
prominent role in mastication and their relatively large size (Fig. 1).
Figure 2. Buccolingual sections through mesial cusps of (A) sea otter M1, and (B)
human M1. Note relatively large tooth base and thinner enamel in the otter. HunterSchreger (HS) bands are visible in the enamel as alternating light and dark bands, an
effect caused by some enamel prisms being sectioned head-on (diazones) and some
enamel prisms being sectioned longitudinally (parazones).
P.J. Constantino et al. / Journal of Human Evolution 61 (2011) 89e96
91
Table 1
Data for sea otter M1 and modern human molars, means and standard deviations.
Species
Sea otter (Enhydra lutris)
Human (Homo sapiens)
Hominin (Paranthropus boisei)
Tooth size R (mm)
a
7.0 0.2
4.9 0.1b
9.0 0.2d
Enamel thickness d (mm)
a
0.65 0.1
1.3 0.1c
2.8 0.2d
Modulus E (GPa)
a
77 4
80 4a
80 4e
Hardness H (GPa)
a
3.0 0.3
4.0 0.4a
4.0 0.4e
Toughness T (MPa m1/2)
0.8 0.2a
0.7 0.1a
0.7 0.1e
Teeth tested in wet state.
a
Data from current measurements.
b
Data from Demes and Creel (1988). Demes and Creel report molar crown areas as the sum of product of buccolingual and mesiodistal diameters of the 3 M teeth for each
species. From their data, we calculate human molar size as R ¼ 0.5 (total molar crown area/3)1/2.
c
Data from Kono (2004), average enamel cap volume divided by EDJ area.
d
Data from Beynon and Wood (1986), Demes and Creel (1988).
e
Assumed same as for human.
weak interprism paths (Boyde, 1976; Rasmussen et al., 1976;
Osborn, 1981; Koenigswald et al., 1987; Rensberger, 2000; Bajaj
and Arola, 2009a; Chai et al., 2009a).
a real-time image of the internal tooth structure under compressive
loading.
Indentation experimentsdmaterial properties
Failure experimentsdfracture modes
Fracture experiments aimed at simulating biting were conducted on sea otter lower first molars (four tests) and modern
human upper and lower molars (M1, M2, and M3; 20 tests) by
loading the uppermost cusps with a metal disk (prototypical ’hard’
contact) in a mechanical testing machine (Lawn et al., 2009; Lee
et al., 2009). Each tooth tested was from a different individual
and was subjected to a single loading cycle. The load was delivered
vertically downward on the most prominent cusp, generating weak
but significant ’hoop’ tensile stresses in the enamel coat (Chai et al.,
2009b). A common loading protocol was used in all tests, and the
displacement rate held fixed such that failure occurred over
a period of several minutes. Crack progress during the loading
sequence was continually recorded by a high resolution camera
system in all tests.
Additional fracture tests were run on individual sea otter
(n ¼ 30) and human (n ¼ 10) teeth at the 32-ID x-ray imaging
beamline at the Advanced Photon Source in Argonne National
Laboratory in Illinois. In these experiments, a custom testing stage
was rigged onto the beamline stage and the tooth disk-loaded along
its axis as before. The tooth was scanned during testing to produce
Nanoindentation tests were run on modern human (n ¼ 1) and
sea otter (n ¼ 1) molar tooth sections to obtain information on two
basic material properties, plane strain elastic modulus E (Young’s
modulus divided by 1 n2, with n Poisson’s ratio) and hardness H. A
three-sided Berkovich pyramidal indenter was used at a fixed
penetration of 0.4 mm corresponding to loads in the range 1 mN to 2
mN, sufficient to probe below any surface damage and to encompass enamel prism diameters within the contact zone. For each
tooth, three transects running from the EDJ to the outer enamel
surface (OES) with indents 20 mm apart, were placed at the two
most mesial cusps and the central occlusal basin that connects
them. The quantities E and H were deconvoluted from the digital
load-displacement data using the widely adopted approach of
Oliver and Pharr (1992).
Vickers microindentation tests were made in the enamel of
molar sections at somewhat higher loads, 1 N to 5 N, in order to
produce contact impressions with well-defined corner cracks.
Toughness (T) was then estimated from the lengths of the corner
cracks using a well-documented indentation toughness equation
(Anstis et al., 1981). Mean and standard deviation values of T thus
obtained (six indents in a single specimen per species) are included
Figure 3. Radialemedian (R) and margin (M) fracture modes in (A) sea otter M1, and (B) human M3. Schematic in (C) shows simplified tooth geometry and fracture modes.
92
P.J. Constantino et al. / Journal of Human Evolution 61 (2011) 89e96
in Table 1. The value for sea otters is a little higher than for humans,
suggesting that the former may have a slightly greater intrinsic
resistance to crack growth. The indentation corner crack patterns
were less well formed in the sea otter teeth, so the toughness value
for this animal is subject to greater uncertainty.
Results
loaded cusp, as shown in Fig. 3A for sea otters and Fig. 3B for
humans. Crack visibility is enhanced by reflection from the interior
crack walls in the translucent enamel. The final crack patterns in
Fig. 3 are similar in the two species. The longitudinal cracks either
started from the cuspal contact region and ran downward toward
the base (radialemedian cracks, R), or started from the cervical
margin and ran upward toward the contact (margin cracks, M). In
During the loading experiments, cracks formed within the
enamel and ran longitudinally around the side wall adjacent to the
Figure 4. Transverse sections cut through molars: (A) sea otter M1, loaded to 550 N
and sectioned to depth 2.2 mm below the cuspal surface, (B) human M3, loaded to
450 N and sectioned to depth 4.4 mm. Sections shown at same scale. From Chai et al.
(2009).
Figure 5. Sequence of three longitudinal synchrotron x-ray images of a sea otter
canine during loading: (A) zero load, (B) intermediate load, radial crack initiated near
the EDJ (arrows), (C) critical load, tooth failure from crack propagation around side
walls of enamel. Cracks are visible as light shadow regions within the enamel.
P.J. Constantino et al. / Journal of Human Evolution 61 (2011) 89e96
most instances, the two crack types evolved simultaneously,
although there was a tendency for M cracks to extend completely
around a side wall first (Lee et al., 2009). In both human and sea
otter teeth, the critical loads required to attain any such visually
observed fracture condition ranged from 400 N up to 700 N. Ultimately, at loads in excess of 1000 N, the enamel began to delaminate from the underlying dentin. Post-test examinations of the
cuspal areas of the indented teeth revealed noticeable cuspal flattening from plastic deformation in the contact area, even at loads
well below those for crack initiation.
Transverse sections cut through partially fractured sea otter and
human teeth at depths sufficient to intersect the dentin are shown
in Fig. 4 (Chai et al., 2009a). These images confirm that longitudinal
cracks remain contained within the enamel shell in a ribbon
configuration, i.e., a channel-like geometry with long edges intersecting the outer and inner enamel surfaces (Fig. 3C). Also observed
in Fig. 4 are wavy, microcrack-like defects, termed ’tufts’ (T), weak
hypocalcified interfaces emanating from the enameledentin junction (EDJ) into the enamel (Sognnaes, 1949; Osborn, 1969; Palamara
et al., 1989). The appearance of these tufts in the two images
highlights a certain commonality in the tooth microstructure in
mammalian species. Previous studies have shown tufts to be
principal sources of longitudinal crack initiation (Chai et al., 2009a;
93
Myoung et al., 2009). Such defects are not ordinarily visible in
images of the external enamel surface, such as Fig. 3.
Fig. 5AeC shows a sequence of three longitudinal views generated from the x-ray image data for a single sea otter canine: (A) zero
load, no cracks, (B) intermediate load, radial crack initiation at the
EDJ, and (C) critical load, crack propagation around the enamel wall.
The cracks in Fig. 5C are seen as the light shadow regions. Rotation
of the x-ray image confirmed that the cracks circumvent the tooth
crown and remain confined within the enamel walls (Lucas et al.,
2009). Fig. 6 shows a virtual transverse section generated from
the x-ray computed tomography data for a partially fractured
human molar. This view is analogous to the optical section view in
Fig. 4B, with the advantage that the x-ray technique is completely
non-destructive and thus free of potential specimen-preparation
artifacts. Again, cracks are seen emanating from tuft-like defects in
the enamel adjacent to the EDJ (Chai et al., 2009).
Nanoindentation results are shown in Fig. 7 as a function of
normalized distance from the EDJ to the OES, to enable comparisons between species. There is a consistent increase in E and H with
distance from the EDJ, broadly consistent with the trends reported
for molars of humans and howler monkeys (Cuy et al., 2002;
Darnell et al., 2009). Mean and standard deviation mid-range
values for E and H, evaluated from the data within 0.4e0.6
Figure 6. X-ray tomography transverse section computer-generated from the image data for a human M3 loaded to 200 N, at depth 4.4 mm below the tooth cusp. Note tufts
emanating into the enamel from the EDJ (cf. Fig. 4B). Circular fringes are a diffraction artifact.
94
P.J. Constantino et al. / Journal of Human Evolution 61 (2011) 89e96
Figure 8. Values of critical forces PM for sea otters, modern humans, and Paranthropus
boisei, calculated from equation (1) in conjunction with data in Table. Error bars reflect
data uncertainties in Table 1.
Figure 7. Plane strain elastic modulus (E) and hardness (H) across sections of sea otter
and modern human molar tooth enamel, plotted as function of normalized distance
from EDJ to outer enamel surface. Each data point is an individual nanoindentation.
normalized distance in Fig. 7, are included in Table 1. Whereas the
data for modulus E in humans and sea otters tend to overlap within
the scatter, the values of H are systematically lower in sea otters.
The latter result indicates notably softer enamel in the sea otter
dentition. As for P. boisei, measurements of material properties are
unavailable for this species, so for the sake of ensuing calculations
we assume them to have the same average values as for modern
humans. Justification for this assumption comes from the apparently similar degrees of enamel prism decussation in the two
species (Grine and Martin, 1988; Teaford and Ungar, 2000), as well
as from the fact that enamel material properties do not appear to
show strong variation among the great apes (Maas and Dumont,
1999; Lee et al., 2010).
Fracture analysis
Explicit equations have previously been obtained for the critical
contact loads required to drive longitudinal cracks around the side
wall of an idealized dome-shaped enamel/dentin structure of
enamel thickness (d) and base radius (R) as shown in Fig. 3C (Lee
et al., 2009). The critical load for first (margin) fracture may be
represented by a simple relation
PM ¼ CTRd1/2
(1)
where T ¼ toughness of the enamel coat and C z 6.0 is a dimensionless quantity (Lee et al., 2009). The critical load (PM) may be
considered to represent a ’failure’ condition, in that longitudinal
cracks are the precursor for delamination of the enamel from the
dentin underlayer (Popowics et al., 2001). Note that once representative values of tooth dimensions and material parameters are
ascertained, equation (1) can be used to make a priori predictions of
critical fracture conditions.
Values of PM determined for sea otters, modern humans and
P. boisei using input data from Table 1 are plotted in Fig. 8. First
consider sea otters and modern humans. The magnitudes of PM for
these two species are similar, with PM z 750 N. These loads lie at
the upper end of the range of observed critical loads in the experimental fracture tests. The comparability of PM for the two species is
interesting, for sea otters have much thinner enamel, seemingly
making the teeth of this animal more vulnerable to fracture in
equation (1). However, any such susceptibility is mitigated to some
extent by the greater molar base radius, providing greater support
for the applied load. The predicted value of PM for P. boisei is two to
three times as high as for sea otters or modern humans, because of
greater tooth size and enamel thickness. This uncommonly high
value indicates a considerably greater capacity to resist tooth
fracture for this group of fossil hominins, implying a greater
capacity to consume hard foods.
Discussion
The results above indicate interesting similarities between sea
otter and modern human molar teeth. The most immediate similarity lies in the tooth morphology: rounded with blunt (bunodont)
cusps. This suggests an element of commonality in the nature of the
diet between the two species. The dome-like morphology of
a bunodont tooth is well configured to dissipate tensile stresses
arising from high occlusal forces. Quantitative evaluation of the
load-bearing capacities of sea otter and human teeth indicates that
both species can indeed sustain substantial biting forces. The estimates for humans and hominins in Fig. 8 are commensurate with
those from jaw mechanics (Demes and Creel, 1988), and in the case
of sea otters are more than adequate to account for the breakdown
of shelled and other hard food objects. Other similarities lie in the
nature of the microstructure, indicated by the appearance of tufts at
the EDJ in Fig. 4, providing sources for crack initiation; and HuntereSchreger bands, providing intrinsic resistance to the propagation of ensuing cracks. The common presence of tufts highlights an
intrinsic weakness of the enamel structure. On the other hand, the
P.J. Constantino et al. / Journal of Human Evolution 61 (2011) 89e96
criss-crossing prism pattern within the decussation zone suggests
some inbuilt mechanism of resistance to subsequent crack propagation. In this view, teeth are remarkably damage-tolerant structures (Chai et al., 2009a); enamel is innately configured to contain
cracks, not to avoid them.
There are also some distinctive differences in the tooth structures of sea otters and modern humans. Most striking is the
considerably thinner enamel in the sea otters, by a factor of about
two (Table 1). This makes the tooth more vulnerable to initiation of
radial cracks beneath the contact, from enhanced flexure of the
enamel coat on the underlying soft dentin substrate (Lucas et al.,
2008), e.g., as observed in Fig. 5. On the other hand, the base
radius of sea otter molars is considerably greater than that of
humans, diminishing the magnitude of the hoop tensile stresses
that drive the cracks and hence providing some compensatory
resistance to failure (Rudas et al., 2005). There may be subtle
differences in the microstructure, too. A preliminary visual
inspection appears to indicate that sea otter enamel features
a somewhat higher intensity of HuntereSchreger bands, signifying
more pronounced changes of direction from one band of prisms to
the next. If confirmed, such an enhancement in the decussation
pattern may go part way to explaining the slightly greater toughness in the sea otter enamel. In this context, the measurements of
Bajaj and Arola (2009b), confirming enhanced toughness in the
regions of high decussation near the EDJ, could have some bearing
on the differences between the two species.
We have focused on the role of thick enamel in inhibiting
fracture, but thick enamel is also a factor in combating wear
through abrasion and microcracking (crumbling) (Molnar and
Gantt, 1977; Osborn, 1981; Macho and Spears, 1999). Severe wear
can expose the inner dentin and result in the inability of the animal
to break down harder foods (Cuozzo and Sauther, 2006), thereby
threatening its longevity (DeGusta et al., 2003; King et al., 2005).
Contrary to the observations of Walker (1981), the dentition of
some deceased sea otters evinced excessive wear, possibly from the
pervasive presence of sand particulates in the diet (Lawn et al.,
2009). In this context, recall the softness (diminished H) of sea
otter enamel relative to humans in Fig. 7B, making sea otters more
susceptible to wear. In such cases, the dentition may continue to
function under some duress, albeit with a tendency toward a softer
diet. Wear can also enhance the initiation of fracture by further
thinning the enamel coat in the occlusal region and thereby
increasing flexure, although it is less likely to affect the critical load
PM in equation (1) needed to drive side-wall fractures to completion
in the contact far field (Ford et al., 2009). The interaction between
wear and fracture in animals such as sea otters is a subject that
bears further exploration.
Conclusions
The capacity of the fracture relations in equation (1) to account
broadly for the magnitudes of the forces required to cause tooth
failure in our simulated biting tests lends confidence in making
predictions about the bite forces exerted by ancestral hominins in
dietary function. We have given special mention to P. boisei because
of its extreme postcanine tooth size and enamel thickness, the
greatest of any known hominin (Beynon and Wood, 1986; Wood,
1991; Aiello and Dean, 2002). Such extreme dimensions protect
the teeth during biting (Fig. 8), particularly in relation to the incidence of radial and margin cracks, and probably also to the incidence of chipping (Constantino et al., 2010), suggesting an
adaptation to very hard and tough foods. The high degree of wear
noted on many Paranthropus teeth also suggests that wear from
frequent chewing on foods containing small hard particles may
have been as important as fracture in selecting for thick tooth
95
enamel. It is interesting to reflect that severe tooth wear can also
occur in modern humans, not only from grinding (bruxism) but also
from variations in diet (Molnar, 1972). There, however, conspecific
care can extend the life of the afflicted human individual well
beyond the loss of normal tooth function. Our ancestors may have
engaged in analogous behavior as early as two million years ago
(Lordkipanidze et al., 2005), although no evidence has yet been
presented to suggest that this is the case with Paranthropus.
Acknowledgments
We wish to thank Jim Estes, Melissa Miller, and the Marine
Wildlife Veterinary Care Research Center for providing access to the
sea otter specimens. Permission to transport and test the sea otter
teeth was granted by the California Department of Fish and Game.
Gary Schumacher, Sabine Dickens and Anthony Guiseppetti of
the Pfaffenberger American Dental Association laboratories at the
National Institute of Standards and Technology provided the
human molar specimens. Use of the Advanced Photon Source (APS)
at Argonne National Laboratory was supported by the U.S.
Department of Energy, Office of Basic Energy Sciences, under
contract no. DE-AC02-06CH11357. Thanks also to Jake Socha and
Alex Deriy for their assistance at the APS. Amanda Keown obtained
the section view in Fig. 2A and Rebecca Kirkpatrick provided useful
comments on the manuscript. This work was supported by a grant
from the National Science Foundation (#0851351 to P.L., P.C., J.J.W.L. and B.L.), by a National Research Council Postdoctoral
Fellowship (J.J-W.L) and by the George Washington University
Research Enhancement Fund (P.C.).
References
Aiello, L., Dean, C., 2002. An Introduction to Human Evolutionary Anatomy.
Academic Press, London.
Anstis, G.R., Chantikul, P., Marshall, D.B., Lawn, B.R., 1981. A critical evaluation of
indentation techniques for measuring fracture toughness: I. Direct crack
measurements. J. Am. Ceram. Soc. 64, 533e538.
Bajaj, D., Arola, D.D., 2009a. On the R-curve behavior of human tooth enamel.
Biomaterials 30, 4037e4046.
Bajaj, D., Arola, D.D., 2009b. Role of prism decussation in fatigue crack growth and
fracture of human enamel. Biomaterials 30, 4037e4046.
Beynon, A.D., Wood, B.A., 1986. Variations in enamel thickness and structure in East
African hominids. Am. J. Phys. Anthropol. 70, 177e193.
Boyde, A., 1976. Enamel structure and cavity margins. Oper. Dent. 1, 13e28.
Calkins, D.G., 1978. Feeding behavior and major prey species of the sea otter,
Enhydra lutris, in Montague Strait, Prince William Sound, Alaska. Fish B. NOAA.
76, 125e131.
Chai, H., Lee, J.J.-W., Constantino, P.J., Lucas, P.W., Lawn, B.R., 2009a. How are teeth
so brittle yet so resilient? Science 106, 7289e7293.
Chai, H., Lee, J.J.-W., Kwon, J.-Y., Lucas, P.W., Lawn, B.R., 2009b. A simple model for
enamel fracture from margin cracks. Acta Biomat. 5, 1663e1667.
Constantino, P.J., 2007. Primate Masticatory Adaptations to Fracture-Resistant
Foods. Anthropology. Ph.D. Dissertation. The George Washington University.
Constantino, P., Wood, B., 2007. The evolution of Zinjanthropus boisei. Evol.
Anthropol. 16, 49e62.
Constantino, P.J., Lucas, P.W., Lee, J.J.-W., Lawn, B.R., 2009. The influence of fallback
foods on great ape tooth enamel. Am. J. Phys. Anthropol. 140, 653e660.
Constantino, P.J., Lee, J.J.-W., Chai, H., Zipfel, B., Ziscovici, C., Lawn, B.R., Lucas, P.W.,
2010. Tooth chipping can reveal the diet and bite forces of fossil hominins. Biol.
Lett. 6, 826e829.
Cuozzo, F.P., Sauther, M.L., 2006. Severe wear and tooth loss in wild ring-tailed
lemurs (Lemur catta): a function of feeding ecology, dental structure, and
individual life history. J. Hum. Evol. 51, 490e505.
Cuy, J.L., Mann, A.B., Livi, K.J., Teaford, M.F., Weihs, T.P., 2002. Nanoindentation
mapping of the mechanical properties of human molar tooth enamel. Arch. Oral
Biol. 47, 281e291.
Darnell, L.A., Teaford, M.F., Livi, K.J.T., Weihs, T.P., 2009. Variations in the mechanical
properties of Alouatta palliata molar enamel. Am. J. Phys. Anthropol. 141, 7e15.
DeGusta, D., Everett, M.A., Milton, K., 2003. Natural selection on molar size in a wild
population of howler monkeys (Alouatta palliata). Proc. R. Soc. Lond. B. S270,
S15eS17.
Demes, B., Creel, N., 1988. Bite force, diet, and cranial morphology of fossil hominids. J. Hum. Evol. 17, 657e670.
96
P.J. Constantino et al. / Journal of Human Evolution 61 (2011) 89e96
Estes, J.A., Riedman, M.L., Staedler, M.M., Tinker, M.T., Lyon, B.E., 2003. Individual
variation in prey selection by sea otters: patterns, causes, and implications.
J. Anim. Ecol. 72, 144e155.
Fisher, E.M., 1941. Notes on the teeth of the sea otter. J. Mammal. 22, 428e433.
Ford, C., Bush, M.B., Lawn, B.R., 2009. Effect of wear on stress distributions and
potential fracture in teeth. J. Mater. Sci. Mater. Med. 20, 2243e2247.
Grine, F.E., 1981. Trophic differences between ’gracile’ and ’robust’ australopithecines: a scanning electron microscope analysis of occlusal events. S. Afr. J. Sci.
77, 203e230.
Grine, F.E., Martin, L.B., 1988. Enamel thickness and development in Australopithecus and Paranthropus. In: Grine, F.E. (Ed.), Evolutionary History of the
“Robust” Australopithecines. Aldine de Gruyter, New York, pp. 3e42.
Hall, K.R.L., Schaller, G.B., 1964. Tool-using behavior of the California sea otter.
J. Mammal 45, 287e298.
Hylander, W.L., 1988. Implications of in vivo experiments for interpreting the functional significance of "robust" australopithecine jaws. In: Grine, F.E. (Ed.), Evolutionary History of the ’Robust’ Australopithecines. Aldine, New York, pp. 55e83.
Kenyon, K.W., 1969. The sea otter in the eastern Pacific Ocean. N. Amer. Fauna
68, 1e352.
King, S.J., Arrigo-Nelson, S.J., Pochron, S.T., Semprebon, G.M., Godfrey, L.R.,
Wright, P.C., Jernvall, J., 2005. Dental senescence in a long-lived primate links
infant survival to rainfall. Proc. Nat. Acad. Sci. 102, 16579e16583.
Koenigswald, W.von, Rensberger, J.M., Pretzschner, H.U., 1987. Changes in the tooth
enamel of early Paleocene mammals allowing increased diet diversity. Nature
328, 150e152.
Kono, R.T., 2004. Molar enamel thickness and distribution patterns in extant great
apes and humans: new insights based on a 3-dimensional whole crown
perspective. Anthropol. Sci. 112, 121e146.
Kvitek, R.G., Fukayama, A.K., Anderson, B.S., Grimm, B.K., 1988. Sea otter foraging on
deep-burrowing bivalves in a California coastal lagoon. Mar. Biol. 98, 157e167.
Lawn, B.R., Lee, J.J.-W., Constantino, P.J., Lucas, P.W., 2009. Predicting failure in
mammalian teeth. J. Mech. Behav. Biomed. Mater. 2, 33e42.
Lee, J.J.-W., Kwon, J.-Y., Chai, H., Lucas, P.W., Thompson, V.P., Lawn, B.R., 2009.
Fracture modes in human teeth. J. Dent. Res. 88, 224e228.
Lee, J.J.W., Morris, D., Constantino, P.J., Lucas, P.W., Smith, T.M., Lawn, B.R., 2010.
Properties of tooth enamel in great apes. Acta Biomat. 6, 4560e4565.
Lordkipanidze, D., Vekua, A., Ferring, R., Rightmire, G.P., Agustí, J., Kiladze, G.,
Mouskhelishvili, A., Nioradze, M., de Leon, M.S.P., Tappen, M., Zollikofer, C.P.E.,
2005. The earliest toothless hominin skull. Nature 434, 717e718.
Lucas, P., Constantino, P., Wood, B., Lawn, B., 2008. Dental enamel as a dietary
indicator in mammals. Bioessays 30, 374e385.
Lucas, P.W., Constantino, P.J., Lee, J.J.W., Hartstone-Rose, A., Chai, H., Lee, W.K.,
Dominy, N., 2009. Primate dental enamel: what it says about diet. In:
Koppe, T., Meyer, G., Alt, K.W. (Eds.), Comparative Dental Morphology. Karger,
Basel, pp. 44e48.
Maas, M.C., Dumont, E.R., 1999. Built to last: the structure, function, and evolution
of primate dental enamel. Evol. Anthropol. 8, 133e152.
Macho, G.A., Spears, I.R., 1999. Effects of loading on the biomechanical behaviour of
molars of Homo, Pan, and Pongo. Am. J. Phys. Anthropol. 109, 211e227.
Molnar, S., 1972. Tooth wear and culture: a survey of tooth functions among some
prehistoric populations. Curr. Anthropol. 13, 511e526.
Molnar, S., Gantt, D.G., 1977. Functional implications of primate enamel thickness.
Am. J. Phys. Anthropol. 46, 447e454.
Murie, O.J., 1940. Notes on the sea otter. J. Mammal 21, 119e131.
Myoung, S., Lee, J., Constantino, P., Lucas, P., Chai, H., Lawn, B., 2009. Morphology
and fracture of enamel. J. Biomech. 42, 1947e1951.
Newsome, S.D., Tinker, T., Monson, D.H., Oftedal, O.T., Ralls, K., Staedler, M.M.,
Fogel, M.L., Estes, J.A., 2009. Using stable isotopes to investigate individual
diet specialization in California sea otters (Enhydra lutris nereis). Ecology 90,
961e974.
Oliver, W.C., Pharr, G.M., 1992. Improved technique for determining hardness and
elastic modulus using load and displacement sensing indentation experiments.
J. Mater. Res. 7, 1564e1583.
Osborn, J.W., 1969. The 3-dimensional morphology of the tufts in human enamel.
Acta Anat. 73, 481e495.
Osborn, J.W., 1981. Dental Anatomy and Embryology. Blackwell, Oxford.
Ostfeld, R.S., 1982. Foraging strategies and prey switching in the California sea otter.
Oecologia 53, 170e178.
Palamara, J., Phakey, P.P., Rachinger, W.A., Orams, H.J., 1989. The ultrastructure of
spindles and tufts in human dental enamel. Adv. Dent. Res. 3, 249e257.
Popowics, T.E., Rensberger, J.M., Herring, S.W., 2001. The fracture behavior of human
and pig molar cusps. Arch. Oral Biol. 46, 1e12.
Rak, Y., 1983. The Australopithecine Face. Academic Press, New York.
Rasmussen, S.T., Patchin, R.E., Scott, D.B., Heuer, A.H., 1976. Fracture properties of
human enamel and dentine. J. Dent. Res. 55, 154e164.
Rensberger, J.M., 2000. Pathways to functional differentiation in mammalian
enamel. In: Teaford, M.F., Smith, M.M., Ferguson, M.W.J. (Eds.), Development,
Function and Evolution of Teeth. Cambridge University Press, Cambridge, pp.
252e268.
Riedman, M.L., Estes, J.A., 1990. The sea otter (Enhydra lutris): behavior, ecology, and
natural history. Biol. Rep. USFWS 90, 1e126.
Rudas, M., Qasim, T., Bush, M.B., Lawn, B.R., 2005. Failure of curved brittle layer
systems from radial cracking in concentrated surface loading. J. Mater. Res. 20,
2812e2819.
Sognnaes, R.F., 1949. The organic elements of enamel. II. The organic framework of
the internal part of the enamel, with special regard to the organic basis for the
so-called tufts and Schreger’s bands. J. Dent. Res. 28, 549e557.
Teaford, M.F., Ungar, P.S., 2000. Diet and the evolution of the earliest human
ancestors. P. Nat. Acad. Sci. 97, 13506e13511.
Tinker, M.T., Bentall, G., Estes, J.A., 2008. Food limitation leads to behavioral
diversification and dietary specialization in sea otters. Proc. Nat. Acad. Sci. 105,
560e565.
Vandevere, J.E., 1969. Feeding Behaviour of the Southern Sea Otter. Proceedings of
the Sixth Annual Conference on Biological Sonar and Diving Mammals. Stanford
Research Institute, Biological Sonar Laboratory, Menlo Park, California.
Walker, A.C., 1981. Diet and teeth. Dietary hypotheses and human evolution. Phil.
Trans. R. Soc. Lond. B. 292, 57e64.
Wang, R.Z., Addadi, L., Weiner, S., 1997. Design strategies of sea urchin teeth:
structure, composition and micromechanical relations to function. Phil. Trans.
R. Soc. Lond. B. 352, 469e480.
Watt, J., Siniff, D.B., Estes, J.A., 2000. Inter-decadal patterns of population and dietary change in sea otters at Amchitka Island, Alaska. Oecologia 124, 289e298.
Wood, B.A., 1991. Koobi Fora Research Project. In: Hominid Cranial Remains, vol. 4.
Clarendon Press, Oxford.
Wood, B., Constantino, P., 2007. Paranthropus boisei: fifty years of evidence and
analysis. Yearbk. Phys. Anthropol. 134, 106e132.