Dental microwear texture analysis of two families of subfossil lemurs from
J.R. Scotta, L.R. Godfreyb, W.L. Jungersc, R.S. Scottd, E.L. Simonse, M.F. Teafordf, P.S. Ungarg,*,
aEnvironmental Dynamics Doctoral Program, University of Arkansas, 113 Ozark Hall, Fayetteville, AR 72701, USA
bDepartment of Anthropology, University of Massachusetts, 240 Hicks Way, Amherst, MA 01003, USA
cDepartment of Anatomical Sciences, Health Sciences Center, School of Medicine, Stony Brook University, Stony Brook, NY 11794, USA
dDepartment of Anthropology, Rutgers, State University of New Jersey, New Brunswick, NJ 08901, USA
eDivision of Fossil Primates, Duke Primate Center, 1013 Broad Street, Durham, NC 27705, USA
fCenter for Functional Anatomy and Evolution, Johns Hopkins University School of Medicine, 1830 E. Monument St., Baltimore, MD 21205, USA
gDepartment of Anthropology, University of Arkansas, Old Main 330, Fayetteville, AR 72701, USA
hDepartment of Anthropology and Biology, Pennsylvania State University, 409 Carpenter Building, University Park, PA 16802, USA
a r t i c l e i n f o
Received 18 July 2008
Accepted 16 November 2008
a b s t r a c t
This study employs dental microwear texture analysis to reconstruct the diets of two families of subfossil
lemurs from Madagascar, the archaeolemurids and megaladapids. This technique is based on three-
dimensional surface measurements utilizing a white-light confocal profiler and scale-sensitive fractal
analysis. Data were recorded for six texture variables previously used successfully to distinguish between
living primates with known dietary differences. Statistical analyses revealed that the archaeolemurids
and megaladapids have overlapping microwear texture signatures, suggesting that the two families
occasionally depended on resources with similar mechanical properties. Even so, moderate variation in
most attributes is evident, and results suggest potential differences in the foods consumed by the two
families. The microwear pattern for the megaladapids indicates a preference for tougher foods, such as
many leaves, while that of the archaeolemurids is consistent with the consumption of harder foods. The
results also indicate some intraspecific differences among taxa within each family. This evidence suggests
that the archaeolemurids and megaladapids, like many living primates, likely consumed a variety of food
? 2008 Elsevier Ltd. All rights reserved.
Diet is widely hypothesized to be a principal factor contributing
to the differences between living primate species. For instance, it
has been directly correlated with critical ecological factors such as
group size and composition, habitat range, and even locomotion
(Fleagle, 1999). With so many important elements of the primate
niche tied to subsistence, it is no wonder that paleoprimatologists
seek to learn all they can about the diets of past species. In fact, in
addition to revealing information about critical aspects of the
ecology of fossil taxa, dietary reconstructions help us understand
the processes of evolution and extinction.
The adaptive radiation of the lemurs of Madagascar provides
reconstruction. Geographic isolation and limited competition have
made these forms the primate equivalent of Darwin’s finches.
Extant lemurs are represented by morethan 100 species within five
families, with a substantive range of adaptations (see summary by
Wright, 1999). But the subfossil record shows that this radiation
was even more remarkable just a few hundred years ago. In fact,
during the past two millennia, the range of their sizes, shapes, and
adaptations was greater than that of the rest of the primate order
(summarized in Godfrey and Jungers, 2002; Jungers et al., 2002).
What were they like? What ecological niches on Madagascar did
they occupy? These are questions that can best be addressed with
careful reconstruction of their paleoecology, especially of their
Dental microwear is the study of microscopic scratches and pits
formed on the surfaces of teeth as the result of use. Because of the
direct relationship between the microwear and the material
properties of foods and abrasives, analysis of dental microwear
reveals important clues regarding the diet and ecology of fossil
* Corresponding author.
E-mail address: email@example.com (P.S. Ungar).
Contents lists available at ScienceDirect
Journal of Human Evolution
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Journal of Human Evolution 56 (2009) 405–416
species. Scratches on the tooth surface are associated with the
shearing of tough foods, like most types of leaves, although some
woody seeds can also be tough (Teaford and Walker,1984; Teaford,
1988; Lucas, 2004, Lucas et al., 2008). Pits are indicative of hard
food consumption, like many seeds (Strait,1993; Silcox and Teaford,
2002). Dental microwear has been examined for both fossil and
extant mammals representing a broad range of taxa, including
primates (e.g., Jacobs,1981; Rafferty and Teaford,1992; Strait,1993;
Daegling and Grine, 1994; Lucas and Teaford, 1994; Teaford et al.,
1996; Ungar, 1996, 1998; Ungar and Teaford, 1996; King, 2001;
Rafferty et al., 2002; Leakey et al., 2003; Godfrey et al., 2004; Ungar
et al., 2004, 2008; El Zaatari et al., 2005; Merceron et al., 2005a),
perissodactyls (e.g., Hayek et al., 1991; MacFadden et al., 1999;
Solounias and Semprebon, 2002; Kaiser et al., 2003), artiodactyls
(e.g., Solounias et al.,1988; Solounias and Moelleken,1993; Hunter
and Fortelius,1994; Rivals and Deniaux, 2003; Franz-Odendaal and
Solounias, 2004; Merceron et al., 2004a,b; Semprebon et al., 2004;
Merceron et al., 2005b; Merceron and Ungar, 2005; Merceron and
Madelaine, 2006; Schubert et al., 2006; Ungar et al., 2007), rodents
(Gutierrez et al., 1998; Lewis et al., 2000; Hopley et al., 2006),
carnivorans (Van Valkenburgh et al., 1990; Anyonge, 1996),
proboscideans (Capozza, 2001; Filippi et al., 2001; Green et al.,
2005), and other taxa (Krause,1982; Biknevicius,1986; O’Leary and
Teaford, 1992; Silcox and Teaford, 2002).
Previous studies of dental microwear in subfossil lemurs have
yielded differing results, particularly regarding the degree of die-
tary specialization in the Archaeolemuridae and Megaladapidae, as
well as variation between species within these families (Rafferty
et al., 2002; Godfrey et al., 2004). These studies used different
methods of characterizing the enamel surface, looking at micro-
wear features at entirely different scales, so it is possible that
overlap might be reported usingone method, but notthe other. One
of these studies, using conventional scanning electron microscope
(SEM) based analysis, reported that Archaeolemur did not specialize
solely on hard objects and that there were interspecific differences
in diet and dental microwear for both families (Rafferty et al.,
2002). By contrast, the other study, using low-magnification light
microscopy, found no overlap between the Archaeolemuridae
(which the authors classified as hard-object feeders) and the
Megaladapidae (classified as folivores; Godfrey et al., 2004).
Previous reconstructions of diet
The dentitions of archaeolemurids are highly derived and have
been the ultimate source of much debate concerning their diet.
Archaeolemurids have large, spatulate incisors, bilophodont molars
that converge on those found in extant cercopithecines, and upper
and lower premolars that form a continuous shearing blade. Early
reconstructions based on these features made analogies to modern
baboons and suggested that the archaeolemurids were primarily
fruit eaters with some hard-object feeding related to fruit selection
(Tattersall,1973,1982). Recent studies of dental microstructure and
dental development have refined these earlier hypotheses and
assigned a more specialized hard-object diet to Archaeolemur
(Ravosa and Simons, 1994; King et al., 2001; Godfrey et al., 2005).
Like Cebus and Paranthropus, Archaeolemur has very thick and
highly decussated enamel, two traits also thought to be related to
hard-object processing, given expected shear forces across the
joint, although Ravosa and Simons (1994) described variation in the
ontogeny of this feature. Studies of fecal pellets associated with
several individuals of Archaeolemur cf. edwardsi have, on the other
hand, suggested a generalized and omnivorous diet, including fruit
and seeds, gastropods, arthropods, crustaceans, and small verte-
brates (Burney et al., 1997; Vasey et al., in preparation).
Dental microwear evidence has also been used to interpret the
diet of Archaeolemur. A study of dental microwear using SEM
techniques reconstructed this genus as having an eclectic diet
based on the absence of clear diagnostic microwear features
(Rafferty et al., 2002). Among the species of Archaeolemur, larger
features were documented on the teeth of A. majori and
A. cf. edwardsi, the northern variety of A. edwardsi. This was thought
to indicate either ecogeographic variation in the incidence of hard-
object feeding among the archaeolemurids or perhaps the impor-
tance of ‘‘fallback foods’’ in the diet of Archaeolemur (Rafferty et al.,
Low magnification light microscopy analysis of Archaeolemur
microwear provided different results. Godfrey et al. (2004) found
the Archaeolemuridae had dietary signatures that were not similar
to any of those in extant lemurs, with the singular exception of
some similarities to Daubentonia madagascariensis. They concluded
that the Archaeolemuridae were frugivorous seed predators that
regularly exploited hard objects. High frequencies of pitting on the
enamel surface were documented, along with scratches that were
classified as coarse and hypercoarse. The authors found examples
of large pits on the teeth of all surveyed individuals, as well as
features they described as puncture pits. No significant differences
were found in use wear signatures between the two species of
Dietary reconstructions of Hadropithecus have varied, depend-
ingon the traits examined. Hadropithecus has large, thick-enameled
molars that wear flat and relatively smaller anterior teeth, much
like the dentition of the extant gelada baboon (Jolly, 1970; Tatter-
sall, 1973). Jolly argued that the long forelimbs of H. stenognathus
would have allowed it to sit on the ground and pluck grass from its
surroundings, much like Theropithecus gelada today. This, combined
with the dentition, suggested a graminivorous or granivorous diet
for Hadropithecus to both Jolly (1970) and Tattersall (1973). These
findings were later questioned based on new attributions of post-
cranial remains of Hadropithecus that demonstrated that the fore-
limbs were not nearly as elongated as Jolly hypothesized (Godfrey
et al., 1997).
Dental microwear evidence has been used to argue against the
gelada baboon model. Although Hadropithecus material is rare and
the sample size analyzed was therefore small, SEM-based study of
microwear revealed a high overall incidence of features suggesting
an abrasive diet (Rafferty et al., 2002). Occlusal surfaces were
described as dominated by wide features, particularly scratches.
The microwear surface of Hadropithecus bore no resemblance tothe
often compared Theropithecus and ruled out a grass-eating
Low magnification light microscopy documented high pit
frequencies on the enamel surfaces of Hadropithecus suggesting
a close association with the hard-object feeder, Cebus apella (God-
frey et al., 2004). According to this study, Hadropithecus use-wear
signatures are least like those of Theropithecus, the taxon to which
these subfossil lemurs are most often compared. The authors
documented similar surface features on the teeth of Hadropithecus
and Archaeolemur: a high frequency of pits, puncture pits, coarse,
and hypercoarse scratches. Hadropithecus, however, had even
greater numbers of puncture pits than either of the Archaeolemur
species. Thus, the authors suggested Hadropithecus was a more
dedicated hard-object feeder. However, a recent study of dietary
indicators including stable isotope analysis, relative enamel thick-
ness, and orientation patch counts has suggested that the diet of
J.R. Scott et al. / Journal of Human Evolution 56 (2009) 405–416406
Hadropithecus might have been more like that of Theropithecus than
previously thought (Godfrey et al., 2008).
The megaladapids lack maxillary incisors and have molars that
increase in size from anterior to posterior (Godfrey and Jungers,
2002). Members of the genus, along with other subfossil lemurs,
also have a fused mandibular symphysis, a rarity in strepsirrhines.
Their enormous teeth exhibit large shearing crests on the upper
and lower molars, which led early researchers to conclude that
Megaladapis was likely a folivore (Thenius, 1953). Tattersall (1975)
also invoked a folivory model by comparing the Megaladapis jaw
apparatus to that of extant Australian koalas. Based on dental
morphology, Godfrey et al. (1997) posited up to 20% frugivory in all
species of Megaladapis, with the majority of the remaining diet
being accounted for by folivory. More recently, Jungers et al. (2002)
calculated the shearing quotients of several species of Megaladapis
and other extinct and extant lemurs, corroborating the inference of
strong folivory in the former.
Dietary reconstruction inferred using an SEM-based study of
dental microwear confirmed the folivore label. The documented
microwear features included narrow pits, a high incidence of
narrow scratching, and a low overall frequency of pitting (Rafferty
et al., 2002). The study suggested differences within the genus in
degree of folivory, with M. grandidieri and M. madagascariensis, the
smaller species, trending towards more varied diets. M. edwardsi
was classified as a ‘‘hyper-folivore,’’ with narrow scratches and the
lowest frequency of pitting recorded for any primate.
Godfrey et al. (2004), using low magnification light microscopy,
agreed that all Megaladapis species were leaf dominated browsers
and compared them most closely to the extant genera Avahi, Lep-
ilemur, and Alouatta. Their study found no evidence of hard-object
feeding or seed predation, based on a lack of puncture pitting and
a low incidence of pitting overall. They also found no significant
M. edwardsi had slightly larger features and more pitting than the
smaller species. Godfrey and co-authors suggested that this
difference may be related to habitat, as M. edwardsi shared the
spiny scrub forests of southern Madagascar currently occupied by
Lepilemur leucopus, a species with similar use wear patterns. They
also hypothesized that this variation, although not statistically
significant, could be evidence for niche differentiation in the
southern part of Madagascar, where M. edwardsi and M. mada-
gascariensis overlap in range.
This paper brings a new technique, dental microwear texture
analysis, to bear on the study of subfossil lemur microwear, to
provide a new set of results that may illuminate the issue of diet.
This technique is automated and the results are repeatable when
the same area of the facet is scanned. The technique also allows
characterization of surfaces in three-dimensions over a continuous
range of scales and operates at high resolution to facilitate the
identification and exclusion of taphonomically damaged specimens
(Scott et al., 2005, 2006; Ungar et al., 2008). Results should there-
fore allow an independent assessment of interspecific variation
among the Archaeolemuridae and Megaladapidae, as well as
interspecific differences within each genus.
We examined all identified species of archaeolemurids and
megaladapids for this study. These included both species within the
genus Archaeolemur: A. edwardsi (n¼35), and A. majori (n¼7). To
test for the possibility of dietary differences between A. edwardsi
from northern and central Madagascar, specimens from the two
geographic regions were analyzed separately. Although the sample
size for A. majori is small, this taxon was included in the statistical
analyses. Specimens for the only species within the genus Hadro-
pithecus, H. stenognathus, were also examined, although only
a small number (n¼5) were without postmortem damage and
suitable for microwear analysis. All species within the genus Meg-
aladapis were also included: M. edwardsi (n¼15), M. grandidieri
(n¼15), and M. madagascariensis (n¼9).
The specimens used in this study are housed at the American
Museum of Natural History (AMNH), the British Museum of Natural
History (BMNH), the Duke University Lemur Center (DUPC), the
Acade ´mie Malgache (AM), Vienna Naturhistorisches Museum
(NHNW), Oxford University Natural History Museum (OXUM), and
the University of Antananarivo (UA). Table 1 lists the included taxa
and specimens used in the analysis.
As in previous studies of dental microwear (see Teaford and
Robinson,1989; Teaford and Runestad,1992), the maxillary second
molar was used in the analysis whenever possible. When the
maxillary tooth was unavailable or exhibited postmortem damage
that obscured microwear, the second mandibular molar or first
maxillary molar was substituted to maximize sample sizes, espe-
cially for rare subfossil material. Conventional SEM-based micro-
wear studies have shown no consistent pattern of differences in
upper and lower microwear pattern or between tooth types (Gor-
don, 1982, 1984; Teaford and Walker, 1984; Teaford, 1985, 1986;
Grine, 1986, 1987; Bullington, 1991). Additionally, this study
focused on the so-called ‘‘Phase II’’ facets (facets 9,10 n, and x), as is
usual for dental microwear analysis (Kay, 1977; Gordon, 1982;
Teaford and Walker,1984; Kruegeret al., 2008). The criteria used for
determining suitability for microwear analysis were those of Tea-
ford (1988) and based on examination of the sides and occlusal
surfaces of the teeth, and a ‘‘clean’’ enamel use-wear surface free of
post mortem damage, coating, adhesive, or casting defects.
The specimens used in this study came from two different
collections and replicas were prepared separately by three of us
(LG, WJ, and MT). High resolution replicas were prepared using
conventional procedures (Ungar, 1996). Teeth were cleaned using
either acetone or alcohol, and the crown surfaces were molded
Subfossil lemur specimens used in this analysis.a
Archaeolemur cf. edwardsi: DUPC10850, DUPC10895, DUPC10903, DUPC11729,
DUPC11744, DUPC11807, DUPC11819, DUPC11828, DUPC11829, DUPC11830,
DUPC11883, DUPC6803, DUPC7849, DUPC7900, DUPC7927, DUPC7928,
DUPC7943, DUPC7970, DUPC9104, DUPC9106, DUPC9890, DUPC9899, DUPC9907
Archaeolemur edwardsi: BMNH9909, BMNH9965, BMNH9966, BMNH9968,
BMNH9969, BMNH9970, BMNH9972, OXUM5098, UA2769, UA2850, UA5135,
Archaeolemur majori: AMNH30007, DULCBB2, BMNH13923, BMNH7374,
OXUM5099, UA2808, UA5377
Hadropithecus stenognathus: AM Display, AM6382, UA5170, Vienna 1934.IV.2,
Megaladapis edwardsi: AM6031, AM6071, AM6143, AM6174, AMNH30024,
AMNH30025, AMNH30027, AMNH30028, DUPC13663, BMNH13912,
BMNH13916, BMNH13917, BMNH7370, BMNH7438, MMV
Megaladapis grandidieri: AM6173, BMNH9917, BMNH9918, BMNH9920,
BMNH9921A, BMNH9921B, BMNH9921C, BMNH9922A, BMNH9922B,
BMNH9922E, BMNH9975, BMNH9976, BMNH9977, OXUM5101, OXUM5103
Megaladapis madagascariensis: BMNH4848, BMNH4849, DUPC11787, DUPC17218,
DUPC18827, DUPC18935, DUPC18938, OXUM5105, UA5484
aAM¼Acade ´mie Malgache, AMNH ¼American Museum of Natural History,
BMNH¼British Museum, Natural History, DUPC¼Duke University Lemur Center,
UA¼University of Antananarivo, OXUM¼Oxford University Natural History
Museum, UA¼University of Antananarivo, Vienna¼Vienna Naturhistorisches
J.R. Scott et al. / Journal of Human Evolution 56 (2009) 405–416407
with President’s Jet Plus polyvinylsiloxane Regular Body Dental
Impression Material (Colte `ne-Whaledent). Casts were then poured
using clear Epotek 501 epoxy resin and hardener (Epoxy Technol-
ogies). Because white-light confocal microscopy uses white-light to
probe the tooth surface instead of electrons, it was not necessary to
mount replicas on stubs or to coat them with a conductive metal as
would be required for SEM.
Facet 9 of each specimen was scanned using a Sensofar Plm
white-light confocal imaging profiler (Solarius Development Inc.,
Sunnyvale, California). This instrument was used because of its
ability to collect accurate 3D point clouds from the surface of wear
facets to generatedigital elevation models. Elevations are measured
at set x and y intervals, allowing for the construction of a 3D matrix
(Ungar et al., 2003; Scott et al., 2005, 2006).
A 100x objective was used to generate a point cloud for each
surface with a lateral sampling interval of 0.18 mm, a vertical reso-
lution of 0.005 mm, and a field of view of 138?102 mm. We
collected data for four adjoining fields to sample a larger area of
about 276?204 mm. The scans were then leveled using Solarmap
Universal software (Solarius Development Inc., Sunnyvale, CA).
Defects such as dust or other adherents were removed using the
erase function in Solarmap and slope-filtering in Sfrax (Surfract,
www.surfract.com). Resulting data files were saved in .sur format
for analysis using scale-sensitive fractal analysis software (see Scott
et al., 2006 for details).
Scale sensitive fractal analysis
Point cloud data files were analyzed using Toothfrax and Sfrax
programs (Surfract, www.surfract.com). This approach has been
used forawide varietyof industrial applications including adhesion
analyses and food texture studies (Kennedy et al., 1999; Pedreschi
et al., 2000, 2002; Brown and Siegmann, 2001; Zang et al., 2002;
Jordan and Brown, 2006), as well as dental microwear analysis
(Ungar et al., 2003, 2007, 2008; Scott et al., 2005, 2006).
Scale-sensitive fractal analysis takes its origin from studies of
fractal geometry. It is based on the principle that the texture of
a surface changes with the scale at which it is observed. The
apparent profile length of a surface, the apparent area of that
surface, and the apparent volume of features on it change with the
scale of observation. This means a surface that appears to be
smooth when viewed at a coarse scale may be demonstrably rough
at finer scales. Changes in apparent texture at different scales can
be examined for profiles across a surface (length-scale analysis), or
whole surfaces (area-scale and volume-filling vs. scale analyses).
Several texture variables of
researchers have been identified (Ungar et al., 2003; Scott et al.,
2005, 2006). We present data for five of these here: complexity,
scale of maximal complexity, anisotropy, textural fill volume, and
heterogeneity. Values for individual surfaces are reported as
medians of the four fields sampled following Scott et al. (2006).
The texture variables used in this study have been described at
length (Ungar et al., 2003, 2007, 2008; Scott et al., 2005, 2006) and
can be summarized briefly here (see Table 2).
Complexity (Asfc). Area-scale fractal complexity is defined in
terms of change in surface roughness at different scales. Asfc is the
slope of the steepest part of a curve fit to a plot of relative area
versus scale over the range of scales at which those measurements
are made. The steeper the slope, the more complex the surface. Pits
and scratches of different sizes overlaying one another would
generally result in a more complex surface (Ungar et al., 2008).
Complexity has been used successfully to distinguish, among
tougher foods. For example, Scott et al. (2005) demonstrated
that Cebus apella, known for a diet of fruit flesh and hard objects
potential value tomicrowear
like some seeds, has higher and more variable Asfc values than
Alouatta palliata, with its diet of leaves and other tough food items
(also see Ungar et al., 2003). Based on previous reconstructions of
diet, we expected that the archaeolemurids would have higher
values for Asfc than the megaladapids.
Scale of maximum complexity (Smc). Previous studies using
scale-sensitive fractal analysis have suggested that the scale range
over which Asfc is calculated may also be informative (Scott et al.,
2005, 2006). Asfc is calculated for the scales where the relative area
versus scale curve is steepest. These scales yield the scale of
maximum complexity (Smc). Surfaces with greater values for Smc
will tend to have less wear at very fine scales and/or more wear
features at coarser scales. For instance, a surface dominated bylarge
pits with an absence of fine scratches might have a high Smc. We
predicted that the archaeolemurids would have higher values for
Smc than the megaladapids.
Anisotropy (epLsar). Length-scale anisotropy of relief is a
measure of orientation concentration of surface roughness. Surface
anisotropy is calculated by taking profiles of the microwear surface
at different orientations; in this case, five degree intervals ‘‘around
the clock.’’ When the surface is highly anisotropic, the relative
lengths of the profiles differ with orientation. Relative lengths at
given orientations can then be defined as vectors. The normalized
relative length vectors form a rosette diagram when displayed
graphicallyand the length of the mean of these vectors is a measure
of surface anisotropy. A surface dominated by scratches all running
in the same direction would have a high epLsar.
The epLsar measure has been used to distinguish between
primates with tough and hard diets. For example, Scott et al. (2005)
showed that the tough food consumer, Alouatta palliata has
significantly higher anisotropy values than the hard-object feeder,
Cebus apella. They used this distinction to suggest that hard foods
that can be associated with pits leave a complex microwear pattern,
while tough, fibrous foods associated with scratches produce
a more directional pattern. Based on previous reconstructions of
diet, we expected that the megaladapids would have higher values
for epLsar than the archaeolemurids.
Textural fill volume (Tfv, Ftfv). The textural fill volume algorithm
examines the summed volume of square cuboids of a given scale
that fill a surface. Textural fill volume can be computed on a coarse
(Tfv) or fine scale (Ftfv). Tfv is computed as the difference in sum-
med volume for fine cuboids (for this study 2 mm on a side) and
larger ones (for this study 10 mm on a side). This removes the
structure of the overall surface (e.g., facet curvature), limiting
characterization to the microwear features themselves. A surface
that is dominated by more features in the mid scale range is
expected to have a high Tfv.
Dental microwear texture variables, definitions, and examples.
Variable Definition Example
Asfc Surface complexity Pits and scratches overlapping one another
would represent a complex surface
A surface dominated by large pits with an
absence of complexity of fine scratches would
have a high value for Smc
A surface dominated by scratches all running in
the same direction would have a high epLsar
A surface dominated by deep features like pits
would have a high Tfv value
Smc Scale of maximum
Tfv Textural fill volume
FtfvFine textural fill volume A surface dominated by deep features like pits
volume would have a high Ftfv value
HeterogeneityA surface with variable patterns of pitting and
scratches across a facet would have a high
J.R. Scott et al. / Journal of Human Evolution 56 (2009) 405–416 408
Tfv has also been suggested to have the potential to distinguish
between primates that consume foods with different fracture
properties. Cebus apella, for example, has high values for Tfv,
a reflection of the higher pit count on the surface. Tough food
consumers that rely on leaves may have lower Tfv values that
correspond to the fine, scratched microwear surface these foods
produce. We expected that the archaeolemurids would have higher
values for Tfv than the megaladapids.
Heterogeneity (HAsfc). As discussed in the above sections, vari-
ables including surface complexity, roughness, and anisotropy can
provide accurate descriptions of microwear surfaces. However
useful these might be, adjoining scans of the same surface can vary
in their values for each variable. In fact, the amount of variation in
complexity, roughness, and anisotropy across a facet or even
a single scan may be important in characterizing the microwear
Heterogeneity of area-scale fractal complexity (HAsfc) is calcu-
lated by splitting individual scanned areas into successively smaller
subregions given equal numbers of rows and columns. This algo-
rithm is performed by using the Auto-Split function in the Tooth-
frax software. HAsfc is calculated by splitting each individual scan
into smaller sections with equal numbers of rows and columns. The
scans are divided first into 2?2 and into increasingly smaller
sections up to 11?11. Resulting distributions are typically skewed,
so the relative variations in complexity for each set of subregions
were calculated as the median absolute deviation of Asfc divided by
the median of Asfc. Based on previous reconstructions of diet, we
expected that the archaeolemurids would have higher values for
HAsfc(9)and HAsfc(81)than the megaladapids.
Statistical analyses were performed to determine the extent of
variation in microwear texture among taxa following Ungar et al.
(2006, 2008). All data were rank-transformed before analysis
(Conover and Iman, 1981) because unranked microwear data
typically violate assumptions associated with parametric statistical
tests. Data for the variables were compared among species using
a multivariate analysis of variance model, with taxon as the factor,
Asfc, Smc, epLsar, Tfv, HAsfc(9),and HAsfc(81)as the dependent vari-
ables, and values for each individual as the replicates. This test
assesses significance of variation among the taxa in overall
microwear surface texture. Single classification ANOVAs for each
variable and multiple comparisons tests were used to determine
the sources of significant variation (but see Enders, 2003; Keselman
et al., 1998 for alternate approaches to analysis). Because these
groups were chosen for their dietary (and expected microwear)
differences, Fisher’s LSD a priori tests were used to compare
species. Tukey’s HSD post hoc tests were also run to balance risks of
Type I and Type II errors (Cook and Farewell, 1996).
Examples of microwear surfaces for each taxon are illustrated in
Figure 1. Figure 2 shows three-dimensional renderings of surfaces
for both families. Results suggest differences between the two
families and between the species within the families for at least
some of the tested texture variables. Both Wilks’ l and Pillai Trace
results indicated significant variation in the model.
The archaeolemurids tended to have surfaces dominated by
larger features, usually pits, with low anisotropy and moderate
heterogeneity. The megaladapids, in contrast, more often had
surfaces dominated by scratches of varying sizes and depth, with
high anisotropyandmoderate heterogeneity. Thus, the twofamilies
seem to fall into two clusters (Fig. 3), with some overlap between
them. Individual ANOVA results indicate that the archaeolemurids
have significantly higher Asfc, Tfv, and Ftfv than do the mega-
ladapids (Table 3).
Some differences are also evident within each of the families.
For example, both the central and northern variants of A. edwardsi
tend to have smaller, shallower features than A. majori and H.
stenognathus. Further, M. edwardsi tends to have smaller, shallower
features than the other megaladapids. These visually apparent
differences are confirmed by statistical analyses (Table 4). Tukey’s
test results indicate significant differences between A. cf. edwardsi
and A. majori in Tfv, Smc, and Ftfv, with A. majori having higher
values for all variables. A. cf. edwardsi also had significantly lower
Smc values than H. stenognathus. No significant differences in
microwear texture were found between the geographic variants of
A. edwardsi or between A. majori and H. stenognathus. Within the
megaladapids, M. grandidieri has higher values for Tfv, Ftfv, and
HAsfc(81)than M. edwardsi. M. edwardsi also has higher Smc values
than M. madagascariensis. Results from Fisher’s LSD Test generally
corroborate those from Tukey’s, as well as suggesting additional
differences between the archaeolemurids in epLsar and HAsfc(81).
In summary, within the archaeolemurids, the two geographic
variants of A. edwardsi were not consistently different, although
only A. cf. edwardsi sensu stricto is significantly different from A.
majori and H. stenognathus. Overall, A. majori and H. stenognathus
have higher values for fill volume and the scale of maximal
complexity. Within the megaladapids, M. edwardsi has lower values
for fill volume than M. grandidieri and higher scales of maximal
complexity than M. madagascariensis. The data suggest that, among
the archaeolemurids, A. majori and H. stenognathus have larger,
deeper surface features and that among the megaladapids, M.
edwardsi has smaller, shallower surface features. These results are
consistent with dietary differences both between and within
Archaeolemuridae and Megaladapidae.
This study presents new data on the dental microwear of the
Archaeolemuridae and Megaladapidae, based on the application of
a new technique, dental microwear texture analysis. These data
corroborate many of the previous dietary inferences made about
the Archaeolemuridae and Megaladapidae using other methods of
microwear analysis. In essence, they affirm the dietary separation
between the two families and some variation within each family.
This study suggests that these subfossil lemurs, like the majority
of living primates, did not focus on specific food types and
tightly controlled dietary categories. The question then becomes
one of degree. How dedicated a folivore was Megaladapis or how
specialized a hard-object feeder was Archaeolemur or Hadr-
The characterization of Megaladapis as a folivore is reaffirmed by
the low epLsar and Tfv values revealed here. An interesting differ-
ence between these results and those of previous studies concerns
the inference of differences in dietary signals between species of
Megaladapis. Significant differences between the species were not
found using low magnification light microscopy. However, simi-
larities between M. edwardsi and the extant spiny forest/open
woodland-adapted lemur, Lepilemur leucopus and between M.
grandidieri and M. madagascariensis and closed forest lepilemurs
were noted (Godfrey et al., 2004). SEM analysis suggested that M.
edwardsi was more folivorous than other members of the genus
(Rafferty et al., 2002). Results of the present study confirm the
variability within Megaladapis with significant differences from the
other taxa in almost every variable, with a more homogenous
surface and smaller features. When compared to previously pub-
lished data by Scott et al. (2006) for the folivore Alouatta palliata, M.
edwardsi has higher mean values for Asfc, suggesting the inclusion
of harder objects in the diet; however, the lower values for Tfv are
consistent with a highly folivorous diet.
J.R. Scott et al. / Journal of Human Evolution 56 (2009) 405–416409
Fig. 2. Meshed axiomatic representations of microwear surfaces in three dimensions. Each represents a field of view of 204 mm ?276 mm. Vertical scales indicate depth.
Fig. 1. Photosimulations of microwear surfaces generated from point clouds. Each represents a field of view of 204 mm? 276 mm.
J.R. Scott et al. / Journal of Human Evolution 56 (2009) 405–416 410
Megaladapis edwardsi was the largest of the megaladapids, with
an estimated weight of approximately 85 kg, larger than an adult
male chimpanzee (Jungers et al., 2008). Members of the subgenus
Megaladapis, M. madagascariensis (the smallest megaladapid) and
M. grandidieri, evince larger surface features and less anisotropic
surfaces, consistent with a diet including more hard objects,
possibly some fruits. This is consistent with Godfrey et al.’s (1997)
inference that the diet of the Megaladapis species consisted of
approximately 0–20% fruit and 80–100% leaves.
While the microwear data for the megaladapids are more-or-
less consistent with those of earlier studies that reconstructed
members of the genus as folivores, those for the archaeolemurids
are less clearly in agreement. Archaeolemur has been considered
a primary frugivore and hard-object feeder based primarily on its
craniofacial adaptations, dental microstructure, and highly derived
dentition, including large, spatulate upper incisors, a premolar
shearing blade, and quadrate, bilophodont molars (Tattersall 1973,
1982). These adaptations, along with the study of coprolites, have
suggested to previous investigators at least partial reliance on hard
objects and/or tough skinned fruits (Tattersall, 1973; Tattersall and
Schwartz, 1974; King et al., 2001; Godfrey et al., 2005).
Light microscopystudies suggested thatarchaeolemurid
microwear signals were similar to those of Cebus apella (Godfrey
et al., 2004). Godfrey et al. (2004) concluded that the archae-
olemurids were hard-object ‘‘specialists.’’ While microwear texture
analysis results indicate that some of the archaeolemurids had
significantly lower Asfc and higher Tfv than reported for C. apella
(Scott et al., 2005), these subfossil lemurs did have values in line
with those reported for Lophocebus albigena (Scott et al., 2005), an
occasional hard-object feeder (Chalmers, 1968; Lambert et al.,
Previous SEM analysis of the archaeolemurids recorded larger
pits on the surfaces of A. cf. edwardsi than A. edwardsi, and Rafferty
et al. (2002) opined that ecogeographic variation might explain the
difference. Even though this difference was only confirmed with
the Smc variable, ecogeographic variation could be responsible for
some interspecific variation within Archaeolemuridae, particularly
between A. edwardsi, a species with a texture signature that indi-
cates the presence of both hard and tough foods, and the apparent
hard-object feeders, A. majori and H. stenognathus. Godfrey et al.
(1999) proposed that A. edwardsi and A. majori were sympatric in
part of their range in the central highlands and that dietary
differences might reflect niche partitioning. Microwear evidence
from SEM and texture analysis both suggest that A. majori diet
included harder foods than A. edwardsi and probably incorporated
more hard objects (Rafferty et al., 2002).
Dietary differences between some of the archaeolemurids were
also suggested by a study of d13C measurements on collagen from
bones of the Archaeolemuridae, particularly between Archaeolemur
and Hadropithecus (Godfrey et al., 2005). Studies of stable isotopes
have been conducted on extant lemurs, successfully distinguishing
differences in habitats between closely related species (Schoe-
ninger et al., 1998; McGee and Vaughn, 2006; Loudon et al., 2007).
These studies suggest that such data can effectively reconstruct
past environments of fossil taxa, and therefore, potential sources of
dietary variation. d13C values for Hadropithecus imply a diet richer
in C4and/or Crassulacean acid metabolism (CAM) plants and/or
invertebrates that feed on C4or CAM plants. A more recent analysis
including more specimens proposed obligate CAM and C4plant
consumption for Hadropithecus (Godfrey et al., 2008). A. majori had
stable carbon isotope values corresponding to a diet mixed diet of
C3and C4or CAM plants, with CAM plants being likely for southern
Madagascar, where arid habitats are more common (Godfrey et al.,
Fig. 3. Bivariate plot of anisotropy and complexity for the two families. Individual
point values for each specimen have been plotted rather than means. Open symbols
represent archaeolemurids (B¼A. cf. edwardsi, ,¼A. edwardsi, D¼A. majori, > ¼H.
stenognathus) and closed symbols indicate megaladapids (C ¼M. edwardsi, -¼M.
grandidieri, : ¼M. madagascariensis).
Descriptive microwear texture statistics for Archaeolemuridae and Megaladapidae.
Asfc epLsarTfvFtfv Smc Hasfc (9)
A. cf. edwardsi
J.R. Scott et al. / Journal of Human Evolution 56 (2009) 405–416411
2005). The values for A. edwardsi were consistent with a diet
dominated by C3 plants, which are associated with mosaic or
forested habitats. Coprolite analysis for A. edwardsi suggests a diet
of frugivory and omnivory for A. edwardsi (Vasey et al., in
The sample size of Hadropithecus stenognathus is small (n¼5)
and any differences between it and the larger samples of other taxa
should be taken as suggestive at best. The microwear of H. sten-
ognathus was similar to that of A. majori, with high values for Tfv,
Ftfv, and Smc. Fisher’s test results indicate that Hadropithecus had
significantly higher values for anisotropy and heterogeneity than
did A. edwardsi and A. cf. edwardsi. Along with the other archae-
olemurids, the microwear signature of Hadropithecus is consistent
with that of a mixed feeder, although with the highest values for
A. Multivariate Nested Analysis of Variance
Between species nested within families
B. Nested ANOVAs
Between species within families
C. Matrices of pairwise differences (within family comparisons)c
A. cf. edwardsi
A. majori 13.85*
A. cf. edwardsi
H. stenognathus 10.76
A. cf. edwardsi
A. edwardsi A. majoriM. edwardsi
M. madagascariensis 13.24*
A. edwardsiA. majori M. edwardsi
M. madagascariensis 12.15*
A. edwardsiA. majori M. edwardsi
M. madagascariensis 6.399
A. cf. edwardsi
A. edwardsiA. majoriM. edwardsi
M. madagascariensis 15.14*
A. cf. edwardsi
A. edwardsiA. majoriM. edwardsi
aAll analyses on ranked data.
bP values reported as 0.000, while effectively zero probabilites, represent actual values of less than 0.001.
c* significant with Fisher’s Least Significance Test; ** significant with Tukeys HSD Multiple Comparisons Test.
J.R. Scott et al. / Journal of Human Evolution 56 (2009) 405–416412
volume among the studied taxa, it is likely that hard objects were
a more frequent part of the diet for Hadropithecus than for the other
included subfossils. If this is the case, the hard object feeding
adaptations reflected in Hadropithecus could have evolved to allow
them to fall back on harder foods when preferred resources were
scarce. However, it is also possible that the higher anisotropy values
reported for H. stenognathus and A. majori could imply a reliance on
tough foods that require more repetitive tooth-food-tooth move-
ments. Isotope analysis also suggests that Hadropithecus ate more
leaves and other plant material, while Archaeolemur ate more fruit
and animal products (Godfrey et al., 2008; Ryan et al., 2008).
The results of the present study support a reconstruction of the
archaeolemurids as at least occasional or facultative hard-object
feeders, as has previously been suggested by both Rafferty et al.
(2002) and Godfrey et al. (2004). The microwear texture analysis
results also appear to reflect ecogeographic differences within the
genus, as earlier hypothesized by both Godfrey et al. (1997) and
Rafferty et al. (2002). As for the specialized morphological adap-
tations in Archaeolemur, it is important to note that adaptations for
tough or hard-object processing may not have been necessary to
process all its foods. In other words, Archaeolemur may have had
the capability to process such hard or tough foods, but not always
Rafferty et al. (2002) argued that the dental microwear of
Archaeolemur indicated an eclectic diet with no distinctive signa-
tures. Some individuals were documented to have larger features
than others, suggesting to the authors ecogeographic variation in
diet or the use of hard objects as fallback resources. Godfrey et al.
(2004) found that the dental microwear of Archaeolemur most
closely resembled that of Cebus apella, a primate that, while
utilizing a variety of resources, has anatomical specializations that
it regularly uses for hard-object processing. It was suggested that,
as in Cebus, the morphological specializations of Archaeolemur such
as extremely thick and heavily decussated enamel, might have also
been used to supplement a variable diet. The results of the current
study support both conclusions and suggest that the archae-
olemurids probably had a variable diet that included hard-objects
in addition to other resources. The microwear texture data suggest
complex surfaces with a mosaic of layered features of various sizes.
The textural variable data for the archaeolemurids overlap with the
lower rangesof data reported for C. apella but are concentratednear
values more similar to those reported for Lophocebus albigena,
a generalist primate that consumes hard objects as fallback items.
This suggests that while the archaeolemurids did utilize some
hard-objects, they may have done so less frequently than did Cebus.
Studies of primate dentition and diet have suggested correla-
tions between morphological features, including tooth shape and
enamel thickness, with the ability of a species to utilize certain
resources (Lucas, 1979; Lucas and Peters, 2000). The application of
dental morphological analysis to the study of dietary preferences in
the subfossil lemurs has suggested that taxa had specialized
adaptations, such as the fast-wearing premolar shearing blade
found in Archaeolemur (Tattersall 1973, 1982) and the high molar
shearing crests and loss of upper incisors in Megaladapis (Thenius,
1953), allowing them to take advantage of hard or tough resources,
However, these seemingly specialized adaptations do not tell us
ones taken only on occasion. As described by Liem (1980), species
that seem to be very specialized in terms of morphological or
behavioral adaptations can, in reality, be ecological generalists. In
some cases, the resources that organisms seem specialized to
phenomenon has become known as Liem’s Paradox (Robinson and
Wilson, 1998). For example, a species may have specialized
adaptations to allow the consumption of hard or tough fallback
foods when less mechanically challenging preferred foods are
unavailable. The preferred items may not require any specialized
processing (e.g., young leaves or fruit flesh), and therefore may not
select for specializedmorphology.
morphology can tell us something about what an animal is capable
of eating, it does not necessarily give us insights into its food pref-
erences, or how often it ate foods with given fracture properties.
Primate diets are highly variable and they depend on preferred
resource availability and the occasional use of fallback resources.
Differences between taxa are often obscured by the fact that
primates assigned to different diet categories in the popular liter-
ature often eat similar foodsde.g., gorillas have traditionally been
described as folivores, while chimpanzees are known as frugivores.
However, Ungar et al. (2008) found overlap in dental microwear
signatures between the two species. In fact, gorillas have been
reported to consume 73% of the same species eaten by sympatric
chimpanzees at Lope ´, Gabon (Tutin and Fernandez,1985). Thus, the
lack of clear differences described by Ungar et al. (2008) in central
dietary tendencies between chimpanzees and gorillas is not
Primates tend to prefer high energy foods, such as ripe fruits,
that do not require specialization to process (Remis, 1997; Remis
et al., 2001; Marshall and Wrangham, 2007). Fallback foods such as
hard seeds or tough leaves may require morphological specializa-
tions to process efficiently, and so it seems that dental morphology
should actually be more reflective of fallback resource use than
preferred diet (Robinson and Wilson, 1998). A study of the dental
morphology and diet of five lemur species by Yamashita (1998b)
revealed that the hardest and toughest resources consumed were
fallback foods and that these were more tightly correlated with the
dental adaptations found in the lemurs than were the most
commonly consumed resources.
Reports on the amount of dietary overlap between living lemurs
have yielded different results. Many examples of dietary variation
and fallback resource use have been reported for lemurs (e.g., Strait
andOverdorff,1996; Yamashita,1996,1998a,b; Simmen et al., 2003)
and several species of generalist lemurs are known, including
Lemur catta. A recent study of lemur seed dispersal at Ranomafana
suggests that there is a lack of dietary overlap between species
(Wright, 2008). Varecia variegata, Eulemur fulvus, Eulemur rubri-
venter, and Propithecus edwardsi were reported to not overlap in
many of the fruits consumed. Yamashita (2002) also found little
overlap in resources selected between Lemur catta and Propithecus
verreauxi verreauxi at Beza Mahafaly Special Reserve but did find
that these species utilized foods with similar mechanical proper-
ties. This suggests that in some habitats lemurs may not overlap in
specific foods, but does not mean that they limit themselves to only
a few food types or that they always choose foods with the same
Individual microwear features on a tooth surface are themselves
ultimately worn away and replaced by others. The ‘‘lifespan’’ of
a feature depends on its depth. This is known as the ‘‘Last Supper
Effect’’ and indicates that microwear features on the enamel surface
only reflect feeding activity in the days or weeks prior to death
(Grine, 1986). Most primate species exploit a variety of resources
with varying fracture properties and abrasives. As a result, it is likely
that even species with different central dietary tendencies will
overlap in their microwear patterning. But then again, some may
also vary dramatically at one period and not the next. Thus, it is only
when larger samples sizes are used, preferably taken from speci-
mens that were collected at different times of the year, that the
biggerpicture ofspecializationanddietaryoverlapbeginsto emerge.
This suggests that to understand dietary adaptations and
behaviors of primates, a measure other than the central microwear
J.R. Scott et al. / Journal of Human Evolution 56 (2009) 405–416 413
tendency is important. Given the short lifespan of individual
features on the facet, microwear may well give us the opportunity
to examine within species variation in dietary patterns given
sufficient sample sizes (Teaford and Robinson, 1989). A few outlier
specimens, such as is observed for Smc of Archaeolemur, are likelyto
be more informative of differences in dietary behaviors in many
cases (such as fallback food exploitation) than comparisons of
sample means (see Scott et al., 2005 for discussion), assuming the
individuals sampled are representative of group behavior. The
ability to detect subtle differences in within-sample variation may
be a key to realizing the potential of dental microwear analyses.
Even with the demonstration of extensive overlap in microwear
signatures between taxa, this study provides a new set of results
that may help to reconstruct the diets of the archaeolemurids and
megaladapids. Both the microwear and cranial adaptations are
consistent with Megaladapis species focusing on leaves. Interspe-
cific differences in microwear signals suggest that M. edwardsi was
the most folivorous of the genus. The results also imply that while
the megaladapids focused on tough foods such as some leaves,
Archaeolemur at least occasionally ingested harder foods. These
data also suggest thatecogeographic differences might help explain
the apparently differing levels of frugivory and hard-object feeding
in the genus.
1. The microwear textures of archaeolemurids are consistent
with a generalist diet, and they probably relied on softer, weaker
items, such as fruit and perhaps young leaves, and ‘‘fell back’’ on
harder objects during times of ecological stress. Two species within
the archaeolemurids group, Archaeolemur majori and Hadropithecus
stenognathus, have microwear texture signatures consistent with
higher levels of hard-object predation than either Archaeolemur
edwardsi variant. Archaeolemur edwardsi overlapped with the
megaladapids in several variables, suggesting a higher amount of
tough foods in the Archaeolemur diet.
2. Microwear textures of the megaladapids are consistent with
previous reconstructions of the family as primary folivores with
some variation between the taxa. Megaladapis edwardsi has
a microwear texture signature consistent with previous recon-
structions of the species as having been the most dedicated folivore
in the family. Megaladapis grandidieri and Megaladapis mada-
gascariensis both have larger surface features and overall lower
values for anisotropy, consistent with a diet including more hard
objects. It is possible that these two species included some fruit or
hard objects in their diets to supplement the leaves.
We would like to thank the curators at the Acade ´mie Malgache,
the American Museum of Natural History, the British Museum of
Natural History, the Duke University Lemur Center, Oxford
University Natural History Museum, the University of Antananar-
ivo, and the Vienna Naturhistorisches Museum for allowing us to
study the specimens in their care. We would also like to thank the
anonymous reviewers for their helpful comments on an earlier
version of this paper. This research was supported by NSF Grants
SBR-0315157 (to PSU, AW, and MFT), BCS-0129185 (to LRG and
WLJ), and BCS-0237388 (to LRG).
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