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Dental microwear texture and anthropoid diets.

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 147:551–579 (2012)
Dental Microwear Texture and Anthropoid Diets
Robert S. Scott,1* Mark F. Teaford,2 and Peter S. Ungar3
1
Department of Anthropology, Rutgers, The State University of New Jersey, New Brunswick, NJ 08901
Department of Physical Therapy, School of Health Sciences, High Point University, High Point, NC 27262
3
Department of Anthropology, University of Arkansas, Fayetteville, AR 72701
2
KEY WORDS
dietary variability; food mechanical properties; dental anthropology; primate
ABSTRACT
Dental microwear has long been used as
evidence concerning the diets of extinct species. Here,
we present a comparative baseline series of dental microwear textures for a sample of 21 anthropoid primate
species displaying interspecific and intraspecific dietary
variability. Four dental microwear texture variables
(complexity, anisotropy, textural fill volume, and heterogeneity) were computed based on scale-sensitive fractal
analysis and high-resolution three-dimensional renderings of microwear surfaces collected using a white-light
confocal profiler. The purpose of this analysis was to
assess the extent to which these variables reflect varia-
tion in diet. Significant contrasts between species with
diets known to include foods with differing material
properties are clearly evident for all four microwear texture variables. In particular, species that consume more
tough foods, such as leaves, tended to have high levels of
anisotropy and low texture complexity. The converse was
true for species including hard and brittle items in their
diets either as staples or as fallback foods. These results
reaffirm the utility of dental microwear texture analysis
as an important tool in making dietary inferences based
on fossil primate samples. Am J Phys Anthropol
147:551–579, 2012. V 2012 Wiley Periodicals, Inc.
The primate radiation is characterized by diverse dietary strategies, and the study of living primate diets provides one key for interpreting fossil hominin diets. Other
clues have come from analyses of masticatory anatomy
and adaptations in their comparative context (Strait et
al., 2009; Grine et al., 2010; and references therein) as
well as inferences based on topics as disparate as stable
isotopes (e.g., Sponheimer et al., 2006) and genetics (e.g.,
Perry et al., 2007). Another line of evidence is provided
by microscopic wear preserved on fossil teeth, which can
be used to infer the material properties of foods consumed just prior to death. A comparative baseline of primate dental microwear surfaces paired with the study of
primate diets in the wild has great potential as an aid to
the reconstruction of food preferences and subsistence
strategies in fossil species, and might be a powerful complement to dietary inferences that flow from other lines
of evidence.
However, recent research on dental microwear and primate diets has made two points increasingly clear: 1)
extant primate diets are complex, flexible, and variable;
and 2) dental microwear is also variable and presents
intrinsic obstacles with respect to repeatable quantification of microwear surfaces. Although a link between
observations of dental microwear on occlusal wear facets
and general diet categories has long been substantiated
(Teaford, 1988a; Ungar et al., 2008b), workers still argue
that dental microwear has not yet lived up to its full
potential (Teaford, 2007; Ungar et al., 2008b). Grine et
al. (2002) pointed to high levels of observer measurement error in dental microwear feature analyses, even
when employing scanning electron microscopy for imaging surfaces. Another significant difficulty in pushing
dental microwear to its potential is the limited nature of
most studies of primate diets in the wild. Methods of
data collection vary dramatically from study to study,
and very few describe dietary preferences and strategies
in terms of both food material properties and dietary
variability on various geographic and temporal scales
(e.g., microhabitat, regional, altitudinal, seasonal, phenological; Teaford and Glander, 1991, 1996; Teaford et al.,
2006; see Teaford and Robinson, 1989). For instance,
Conklin-Brittain et al. (2000) reviewed the literature on
ape diets and found dramatic variability in diets among
common chimpanzees, with reports from 24 studies
evincing a range of percent fruit consumed of 19–99%.
These studies also rarely mention the variety of fruit
parts eaten and their fracture properties, which vary
from soft and tough, to hard and brittle (Dominy et al.,
2008; Norconk et al., 2009; see Vogel et al., 2009 for
some of the rare exceptions this statement; Vogel et al.,
2008; Wright et al., 2009). We would expect very different dental microwear signals to result from a diet of 19%
hard fruit endocarp (on one extreme) compared to one of
99% soft fruit mesocarp (on another).
Of further interest, behavioral observations of primates in the wild increasingly demonstrate that summarytype characterizations of masticatory adaptations are often not well matched with actual food preferences. For
example, Lophocebus albigena, with its relatively thick
enamel and other craniodental specializations, was long
C 2012
V
WILEY PERIODICALS, INC.
C
Additional Supporting Information may be found in the online
version of this article.
Grant sponsors: US National Science Foundation, LSB Leakey
Foundation.
*Correspondence to: Robert S. Scott, Department of Anthropology,
131 George Street, RAB 306, New Brunswick, NJ 08901-1414, USA.
E-mail: robertsc@rci.rutgers.edu
Received 31 May 2011; accepted 27 November 2011
DOI 10.1002/ajpa.22007
Published online 13 February 2012 in Wiley Online Library
(wileyonlinelibrary.com).
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R.S. SCOTT ET AL.
thought to be a dedicated hard-object feeder, but behavioral research combined with mechanical testing of food
properties indicates that L. albigena is more aptly
described as a hard-food fallback feeder, taking such
resources on occasion rather than regularly (Lambert et
al., 2004). This would also appear to be mirrored in
observations of L. albigena microwear (Scott et al., 2005,
2006; Ungar, 2009) and contrast with recent information
on Cercocebus atys, a truly dedicated hard object feeder
(McGraw et al., 2010; Daegling et al., 2011).
Here, we address two issues: 1) the extent to which
dental microwear corresponds with reported primate
diets (microwear-diet specificity), and 2) the types of dietary inferences that may benefit most from microwear
analyses as compared to what might be learned from
functional anatomy. To do so, we rely on the largest comparative baseline of high-resolution dental microwear
surfaces assembled to date and a review of current literature on the dietary preference, strategy, flexibility,
and—when available—food material properties for primate species in the sample.
The observation that dental microwear can be associated with diet and jaw movements dates back more than
50 years (Butler, 1952; Mills, 1955; Baker et al., 1959;
Dahlberg and Kinzey, 1962; Walker, 1976). Walker
(1981), Rensberger (1978), Ryan (1979), and Grine (1977)
adopted the scanning electron microscope (SEM) as an
instrument capable of observing microwear with sufficient resolution and, most critically, depth of field for the
inference of mammalian diets. Soon thereafter, Grine
(1981, 1986) published inferences on South African australopith diets based on the proportions of microwear
features identified as either pits or scratches on SEM
photomicrographs, and Walker, Gordon (1984, 1988),
Teaford, and their coworkers began documenting differences in dental microwear related to diet in modern
taxa. However, despite innumerable subsequent studies,
sample sizes have generally remained small due to the
time-consuming nature of digitization of microwear features on photomicrographs, even with the introduction of
semiautomated methods to assist observers in identifying microwear features (Ungar et al., 1991). Moreover,
the inherent subjectivity of feature identification is likely
an important source of high interobserver errors
reported for such studies (Grine et al., 2002). Limitations
like changing apparent microwear geometry due to shadowing effects (essentially, data loss associated with the
representation of 3D surfaces in two dimensions with
SEM images) have long been recognized (Gordon, 1988).
Thus, the study of the associations between dental
microwear and diet, while longstanding, has been limited by methodological constraints.
Recently, alternative approaches have been proposed
to resolve some of these difficulties. Some workers have
advocated a return to variations on low-magnification
light microscopy (Solounias and Semprebon, 2002; Godfrey et al., 2004; Semprebon et al., 2004; Green et al.,
2005; Nelson et al., 2005; Green, 2009; Rivals et al.,
2009; Williams and Patterson, 2010) or low-magnification light photomicroscopy (Merceron et al., 2004,
2005a,b) as low-cost methods capable of generating
larger sample sizes. However, two separate research
groups have been unable to replicate the results of such
studies (Scott et al., 2008; Mihlbachler et al., 2010),
which calls into question both the repeatability of results
and the ability to compare results between studies.
There are also problems in recognizing postmortem wear
American Journal of Physical Anthropology
with the low magnification techniques (Teaford et al.,
2008; Grine et al., in press). Another alternative, dental
microwear texture analysis, is based on the use of a confocal white-light profiler and is capable of generating
large samples of microwear surfaces and repeatable
measurements (Scott et al., 2005, 2006, 2009; Merceron
et al., 2006, 2009, 2010; Ungar and Scott, 2007, 2009;
Ungar et al., 2007, 2008a,b, 2010b,c; Krueger et al.,
2008; Prideaux et al., 2009; El-Zaatari, 2010; Krueger
and Ungar, 2010; Schubert et al., 2010; Schulz et al.,
2010). This method relies on three-dimensional coordinates collected at high resolution from microwear surfaces identified by the investigator together with objective
variables describing surface textures using tiling and
profiling algorithms based on principles from fractal geometry (see especially Scott et al., 2006). Here, we characterize dental microwear quantitatively using this relatively new approach.
An empirical relationship between molar microwear
and diet has been consistently reported in the literature,
no matter which method of data acquisition has been
used. Molar wear facets of field-trapped or wild-shot
individuals reported to consume hard foods on a regular
basis have been shown repeatedly to display higher frequencies of microscopic pitting, particularly, large pits
(Teaford and Walker, 1984; Teaford, 1985, 1988a; Teaford
and Robinson, 1989; Teaford and Runestad, 1992; Strait,
1993) and more recently more complex microwear textures (Scott et al., 2006). Similarly, more folivorous, grazing, or tough flesh-based diets have been associated with
striated microwear (Teaford and Walker, 1984; Teaford,
1988a; Hayek et al., 1991; Solounias and Moelleken,
1992a,b, 1994; Solounias and Hayek, 1993; MacFadden
et al., 1999) and anisotropic microwear textures (Scott et
al., 2006; Ungar et al., 2007, 2010b; Prideaux et al.,
2009; Schubert et al., 2010). This may result from both
masticatory mechanics and/or abrasives including phytoliths (Gordon, 1984; Lucas and Teaford, 1995; Teaford
and Lytle, 1996; Danielson and Reinhard, 1998; Mainland, 1998, 2003; Gugel et al., 2001; Silcox and Teaford,
2002; Teaford et al., 2006). In addition to the hardness
and toughness of foods as influences on microwear, exogenous grit has been well implicated in the formation of
microwear (e.g., Ungar et al., 1995; Teaford and Lytle,
1996; Silcox and Teaford, 2002; Nystrom et al., 2004).
The well-documented empirical relationship between
food fracture properties and dental microwear patterns
can be explained with a simple causal model. Observed
patterns of microwear are caused by differences in the
angle of approach of opposing occlusal facets. In turn,
these angles of approach are dictated by food hardness
and toughness. Thus, hard foods are typically masticated
between opposing teeth with a normal angle of approach
into occlusion [‘‘crushing’’ in the framework of Kay and
Hiiemae (1974)]. Conversely, tough foods are often triturated when opposing surfaces slide past one another,
given an angle of approach more parallel to the facets
themselves (‘‘shearing’’ when the orientation of approach
into and out of centric occlusion is fairly constrained,
and ‘‘grinding’’ when not). In each case, the actual wear
causing particles are the same: phytoliths or other silicabased structures in the plants themselves (Gordon, 1984;
Ungar, 1994; Lucas and Teaford, 1995; Teaford and
Lytle, 1996; Danielson and Reinhard, 1998; Mainland,
1998, 2003; Gugel et al., 2001; Silcox and Teaford, 2002;
Teaford et al., 2006) or exogenous grit (Ungar et al.,
1995; Teaford and Lytle, 1996; Silcox and Teaford, 2002;
553
DENTAL MICROWEAR TEXTURE AND ANTHROPOID DIETS
Nystrom et al., 2004). The key point is that the ultimate
cause of the microwear is usually small abrasives in or
on foods, with differences in pattern resulting from influences of food mechanical properties on occlusion.
An alternate mode of microwear causation, adhesive
wear, has been described by Teaford et al. (see especially
Teaford and Runestad, 1992). Tooth-to-tooth contact generating very small true contact areas and very high
loads at these points might lead to tiny welds between
opposing prisms and consequent ‘‘plucking’’ of prisms
(Walker, 1980, 1984) or micro-fractures at contact points.
Either mode might result in small pits.
In the case of shearing tough foods (graze, mature
leaves, tough flesh), the angle of approach of opposing facets is low and the direction of approach may be fairly consistent. Microwear fabrics resulting from this process are
predicted to be anisotropic and composed primarily of parallel and subparallel scratches. These scratches are
formed as wear particles like phytoliths and exogenous
grit are dragged across the occlusal surface.
Crushing hard foods is accomplished by generating
greater compressive forces as occlusal surfaces contact
each other with a higher angle of approach. The microwear that results is composed of multiple overlapping
pits as abrasives in or on a food item cause microflaking
of the occlusal facet oftentimes using existing points of
weakness. Such microwear surfaces are likely to be complex in the methodology of Scott et al. (2005).
Grinding or milling of tough foods can also be characterized by low angles of approach between opposing facets, but the directionality of approach may be less consistent. Thus, grinding or milling likely would result in
less anisotropic microwear textures that are also not
complex (see Ungar et al., 2010c).
The basic parameters of this model of microwear causation (recently summarized by Ungar, 2011) have been
developed and confirmed over the past 50 years. The
framework outlined by Kay and Hiiemae (1974) offered a
useful functional perspective, numerous studies using the
SEM to observe microwear have supported it empirically
(see Teaford, 1988a), and experimental studies have elaborated on it (e.g., Teaford and Oyen, 1989b; Teaford and
Runestad, 1992; Ungar, 1994; Ungar et al., 1995).
Prior studies have proceeded through both experimental work and quantitative assessment of museum collections. Here, we take the quantitative approach applying
new methods to larger samples. It is important to note
from the outset that an ideal study would proceed with
samples where field observations of actual diets before
sampling are available (see Materials and Methods).
Unfortunately, available museum samples do not typically come with this form of metadata, and studies of
live animals have been limited by the extreme effort
required to study and capture or keep them.
MATERIALS AND METHODS
Samples, preparation, and data collection
This study presents data on molar microwear textures
of 21 species (22 taxa total) of anthropoid primates
(Table 1). Alpha taxonomy generally follows that of the
IUCN Red List of Threatened Species 2009.2. The Semnopithecus entellus sample and Trachypithecus cristatus
sample each follow the taxonomy used for these same
specimens in Rafferty et al. (2002) and Scott et al.
(2006), although current IUCN designations could split
TABLE 1. Anthropoid primate comparative sample
Taxon
5CERC
Colobus guereza
Colobus polykomos
Procolobus badius
Lophocebus albigena
Cercocebus atys
3PAP
Papio cynocephalus
Papio ursinus
Theropithecus gelada
3HOM
Pan troglodytes
Gorilla gorilla
Gorilla beringei
6CEB
Alouatta palliata
Ateles belzebuth
Ateles hybridus
Cebus xanthosternos
Cebus nigritus robustus
Cebus nigritus x libidinosus
5CAT
Semnopithecus entellus
Trachypithecus cristatus
Presbytis rubicunda
Macaca fascicularis
Pongo pygmaeus
N
Museum
23
29
16
23
55
NMNH
SMNK
SMNK
UMN (17); NMNH (6)
SMNK
27
12
12
UMN(17); KNM (10)
NMNH
FMNH (8); HERC (4)
17
15
16
CMNH
AMNH (8); CMNH (7)
NMNH
31
10
8
9
14
7
NMNH
NMNH
NMNH
NMNH
NMNH
NMNH
8
12
12
20
15
BMNH (5); NMNH (3)
NMNH
NMNH
NMNH
SAPM
Museum abbreviations are: NMNH, National Museum of Natural History, Washington DC, USA; SMNK, Staatliches Museum
für Naturkunde Karlsruhe, Germany; UMN, Department of Anthropology, University of Minnesota, Minneapolis, Minnesota,
USA; KNM, National Museum of Kenya, Nairobi, Kenya;
FMNH, The Field Museum, Chicago, Illinois, USA; HERC,
Human Evolution Research Center, Berkeley, California, USA;
CMNH, Cleveland Museum of Natural History, Cleveland, Ohio,
USA; AMNH, American Museum of Natural History, New York,
New York, USA; BMNH, Natural History Museum, London,
UK; SAPM, Staatssammlung für Anthropologie und Paläeoanatomie München, Germany. When species include specimens
from more than one collection, the number of specimens from
each collection is indicated in parentheses.
these further. These data are compared with what is
known about the diets of these taxa.
The total sample includes 391 wild-shot specimens for
which high-resolution replicas of M2s (mostly mandibular) were made. The original specimens were cleaned
with acetone- or alcohol-soaked cotton swabs, and vinyl
impressions were made using President’s Jet Regular
Body Dental Impression Material (Coltene-Whaledent).
Casts were subsequently poured using Epotek 301 epoxy
resin and hardener (Epoxy Technologies). ‘‘Phase II’’ facets (9 or x; Kay, 1977) on the resulting casts were
scanned using a Sensofar Pll white-light scanning confocal profiler (Solarius, Sunnyvale, CA) with a 1003 objective, following the procedures outlined by Scott et al.
(2006). This resulted in a 3D point cloud with a lateral
sampling interval of 0.18 lm and a vertical resolution of
0.005 lm for each scan. We collected data for four adjoining fields to sample a total area of 276 3 204 lm. Only
those surfaces that clearly preserved antemortem microwear [following criteria of Teaford (1988b) and King et
al. (1999)] were included in the analysis, and artifacts,
such as adherent dust particles, were excluded by
thresholding, erase operators, and slope-filtering as necessary. Scans were then leveled using Solarmap Universal software (Solarius Development, Sunnyvale, CA).
American Journal of Physical Anthropology
554
R.S. SCOTT ET AL.
Dental microwear texture parameters
Four dental microwear texture parameters described
by Scott et al. (2006) were calculated using the scalesensitive fractal analysis programs Toothfrax and Sfrax
(Surfract, www.surfract.com). These four parameters
are: area-scale fractal complexity (Asfc), exact proportion
length-scale anisotropy of relief at the 1.8-lm scale
(epLsar1.8lm), heterogeneity of area-scale fractal complexity (HAsfc81cells), and textural fill volume (Tfv).
Asfc describes the fractal complexity of microwear
surfaces, and complexity has been associated with food
hardness (Scott et al., 2005, 2006; Schubert et al., 2010;
Ungar et al., 2010c). The anisotropy of microwear texture (here measured by epLsar1.8lm) has been linked to
food toughness, and high anisotropy is found for surfaces that appear to be dominated by parallel striations
(Scott et al., 2005, 2006; Prideaux et al., 2009; Schubert et
al., 2010). Heterogeneity (here measured by HAsfc81cells)
describes the degree of within-field-of-view variation in
microwear across different scales, and can potentially be
related to factors such as the size and variability in wearcausing particles (Scott et al., 2006). In this case, textural
fill volume (Tfv) is calculated as the difference between fill
volume resulting from square cuboids with 2 lm2 square
sides and fill volume resulting from square cuboids with
10 lm2 square sides (see Scott et al., 2006), so higher values should reflect high incidences of features broadly of
the finer scale. Tfv should be greater for surfaces with
larger, deeper, and more symmetrical areas of wear (i.e.,
heavily pitted surfaces) as more filling elements are likely
to fit in such areas.
The descriptive terms for the microwear texture parameters in this study are preferred over variable acronyms. Thus, complexity refers to Asfc, anisotropy refers
to epLsar1.8lm, heterogeneity refers to HAsfc81cells, and
textural fill volume is used in preference to Tfv.
Statistical analyses
An ideal test for the relationship between dental
microwear and diet would match data on wear facet texture with field observations of foods consumed prior to
molding teeth (e.g., Teaford and Glander, 1991, 1996;
Nystrom et al., 2004). Indeed, given the likelihood of a
‘‘Last Supper’’ effect on dental microwear (Grine, 1986),
only data on foods consumed in the last few days, weeks,
or perhaps months prior to dental molding would generally be relevant. However, the exact length of the ‘‘Last
Supper’’ period should depend on the properties of the
foods and abrasives brought into contact with the teeth.
For instance, individual microwear features in some
modern human populations can turnover very slowly,
given clean and processed foods with limited abrasives
likely to scratch teeth (Teaford and Tylenda, 1991). By
contrast, people living in abrasive environments (e.g.,
Molnar, 1983), or wild-caught nonhuman primates that
consume phytolith-rich foods (e.g., Teaford and Glander,
1991, 1996) often exhibit much faster rates of tooth
wear, and thus could potentially show marked microwear changes in a matter of days. Similarly, deep pits
left by especially large abrasives could potentially last
longer on dental facets than shallower features (Noble
and Teaford, 1995).
It is also true that measurements of the material properties of the actual foods consumed during the period of
field observation would be needed to realize this ideal
American Journal of Physical Anthropology
case. Thus, in the ideal situation, microwear textures for
groups of species with similar diet material properties
would be compared.
However, the wild-shot museum specimens available
for most studies, including this one, are not linked with
days of behavioral feeding observations and analyses of
the mechanical properties of these foods. In fact, for
many species, no studies of food material properties
have been made. Behavioral studies of diets are also not
available for all taxa and are unavailable for many populations. For example, eight specimens of Ateles hybridus
hybridus, the variegated spider monkey, from Zulia, Venezuela preserved antemortem microwear. However, we
are aware of no published data on the diet of A. hybridus
other than a short report that Ateles hybridus brunnea
in Colombia ‘‘. . .follow the dietary patterns of all other
spider monkeys as they rely heavily on fruits’’ (Link and
Morales Jimenez, 2007). To further complicate the issue,
when several behavioral studies have been made of
diets, what often becomes clear is that, assuming methods of behavioral data collection are the same, there is
substantial dietary variability within species on various
geographic and temporal scales (e.g., microhabitat, regional, altitudinal, seasonal, phenological, and idiosyncratic; see for instance Conklin-Brittain et al., 2000). A
simple table of ‘‘species-specific diets’’ would be a naive
oversimplification of primate diets.
Simply seeking out significant differences between
pairs of species for which microwear texture data are
available pairs this risk of oversimplification of primate
diet with the risk of data dredging—randomly finding
spurious statistical significance. However, the available
dietary data from field studies are so sparse as to make
the use of taxonomy a necessary proxy for diet. To minimize the risks of oversimplification and data dredging,
we proceeded in three ways.
First, the diet of each species included in this study
was described using the available literature, and predictions regarding microwear texture parameters were
made a priori on the basis of this review. Efforts were
made to note scales of dietary variability (geographic
and temporal), especially in relation to locations of specimen collection, and particular attention was paid to
ranges of food types consumed between studies as well
as to any data available on food material properties.
Equal efforts were made to predict when differences in
microwear textures were not expected as well as when
differences were expected.
Second, the hypotheses that diet and species and diet
and genus are linked closely enough to result in microwear textures that differ between species and between
genera were tested. Rank-transformed data for the four
microwear texture parameters were compared first among
genera and then among species, with genus or species as
the factor, microwear texture parameters as the dependent variables, and values for each individual as the replicates. This test assesses significance of variation among
the taxa in overall microwear surface texture.
Third, analyses were carried out on a series of five
subsets of the overall comparative data set both at the
species level and at the genus level. These analysis
groupings were designed to contain some taxonomic and/
or ecogeographic similarity while still encompassing dietary differences. Constraining the analysis in this fashion simplified the development of a priori predictions
concerning microwear textures and reduced the potential
for an inevitable loss of statistical power that would be
DENTAL MICROWEAR TEXTURE AND ANTHROPOID DIETS
caused by corrections for pairwise comparisons across
four different variables between all 22 taxa. For
instance, predicting the microwear textures of Papio cynocephalus in comparison to Theropithecus gelada is more
straightforward than predicting how each may compare
with the African apes. Similarly, the literature on African ape diets makes comparisons among the African
apes more straightforward than comparisons of African
apes to other primates.
The five independently analyzed subsets of the complete
comparative data set or analysis groupings were as follows:
1. Five species of forest-dwelling African cercopithecid
monkey (5CERC). This group includes two mangabeys
(L. albigena and C. atys) and three colobus monkeys
(Colobus guereza, Colobus polykomos, and Procolobus
badius).
2. Three species of mainly terrestrial, open habitat
African papionin monkey (3PAP). This group includes
P. cynocephalus, Papio ursinus, and T. gelada.
3. Three species of African ape (3HOM). This group
includes Pan troglodytes and two species of Gorilla,
Gorilla gorilla, and Gorilla beringei.
4. Six taxa of New World monkey (6CEB). This group
includes Alouatta palliata, two species of Ateles,
Ateles belzebuth, and A. hybridus, and three taxa of
‘‘apelloid’’ Cebus, Cebus xanthosternos, Cebus nigritus
robustus, and wild-shot hybrids of Cebus nigritus 3
libidinosus from Minas Gerais, Brazil.
5. Five species of Asian catarrhine (5CAT). This group
includes Pongo pygmaeus, Macaca fascicularis, and
three colobines, Presbytis rubicunda, Semnopithecus
entellus, and Trachypithecus cristatus.
Statistical analyses were performed for all four microwear texture variables, and for each analysis grouping
following procedures similar to those outlined in previous studies (Ungar et al., 2006, 2008b). All data were
rank-transformed before analysis, because raw microwear data typically violate assumptions associated with
parametric statistical tests (Conover and Iman, 1981).
Single-classification ANOVAs for each variable and
multiple comparisons tests were used to determine the
sources of significant variation. Fisher’s LSD a priori
tests and Tukey’s HSD post hoc tests were run to balance risks of Type I and Type II errors (Cook and Farewell, 1996). In general, comparisons in which Tukey’s
HSD was significant are interpreted as grounds to
reject the null hypothesis of no difference in the microwear texture parameter. Instances where Fisher’s LSD
was not significant are interpreted as grounds to not
reject the null hypothesis of no difference in the microwear texture parameter (Cook and Farewell, 1996).
Cases when Tukey’s HSD was not significant but Fisher’s LSD was significant are interpreted here as marginal, and worthy of further investigation (see Cook
and Farewell, 1996 for a discussion of multiple comparison corrections). Put more simply, the use of both
Tukey’s HSD and Fisher’s LSD tests allows us to partition comparisons into significant, not significant, and
suggestive of significance.
Reported diets
Diets of 5CERC group. The first analysis grouping
(5CERC) includes the two mangabeys, L. albigena and
C. atys, and three colobus monkeys, C. guereza, C. poly-
555
komos, and P. badius. Figure 1 displays some of the
reported range of variation in the annual diets of these
taxa and in general, a gradient from an extreme folivore
(>90% leaves) among at least some C. guereza (see especially Harris and Chapman, 2007) to specialization on
hard fruits found on the forest floor for at least some
populations of C. atys (Bergmüller et al., in prep; Daegling and McGraw, 2007; McGraw and Zuberbuhler,
2008). L. albigena, C. polykomos, and P. badius appear
to grade in between these two species in terms of the
degree to which leaves and seeds are incorporated into
their diets (Fig. 1).
Data on the specific material properties of all foods
eaten by C. atys are not yet published, but major food
items eaten include invertebrates (26% of total feeding)
and fruits of Anthonota fragrans, Sacoglottis gabonensis,
and Dialium aubrevillei (\68% of total feeding). Among
the fruits, those of Anthonota fragrans appear to be preferred (Bergmüller et al., in prep) with C. atys consuming seeds within a 6–12 cm long capsule at all stages of
ripeness (Janmaat et al., 2006). Sacoglottis gabonensis
fruits are ovoid drupes about 4 cm in diameter that contain a hard, hollow stone (Morgan, 2009). The Sacoglottis stone is a stress-limited food and has hardness similar to peach pits, cherry pits, or coconut husks (Williams
et al., 2005; Daegling et al., 2010; McGraw et al., 2011).
Sacoglottis stones are available on the forest floor to C.
atys throughout the year, but appear to be eaten only as
Anthonota becomes unavailable (Bergmüller et al., in
prep). Sacoglottis consumption ranged from 6% of feeding time (March) to 50% of feeding time (August) during
the study of Bergmüller et al. (in prep). McGraw et al.
(2010) report that Sacoglottis stones are the most preferred foods for Tai Forest C. atys (52% of annual diet).
In addition to consuming the stones of Sacoglottis, C.
atys eats the pulp of ripening Sacoglottis drupes during
peak fruiting (Bergmüller et al., in prep). C. atys spent
less time feeding on the small fruits of Dialium aubrevillei than on Sacoglottis or Anthonota throughout the
study period (March–August) of Bergmüller et al. (in
prep). The dependence of C. atys on Sacoglottis stones
suggests that C. atys might best be described as a habitual hard-food feeder.
L. albigena has long been viewed as a dedicated hardfood feeder (Chalmers, 1968; Jones and Sabater-Pi,
1968). However, behavioral research combined with mechanical testing of food properties indicates that L. albigena is more aptly described as a facultative hard-food
fallback feeder, taking such resources on occasion and as
needed rather than preferentially (Lambert et al., 2004).
Although colobine monkeys are widely described as
‘‘leaf-eating monkeys,’’ field studies have made it increasingly clear that seeds often play a large role in colobine
diets (Davies et al., 1999; Steenbeek and van Schaik,
2001; Dela, 2007; Guo et al., 2007). Indeed, it has been
argued (Chivers, 1994; Kay and Davies, 1994; Merceron
et al., 2009) that seed predation may have resulted in
selection for guts exapted for folivory. With leaves typically characterized as tough (especially when mature)
and seeds being hard or tough (Lucas et al., 2009),
some colobines may routinely eat foods that are tough
and some that are hard or ones that are both hard and
tough. This situation may confound expectations regarding dental microwear of colobines and has been proposed
to influence masticatory morphological variation among
African and Asian colobines (Koyabu and Endo, 2009,
2010).
American Journal of Physical Anthropology
556
R.S. SCOTT ET AL.
Fig. 1. Dietary variation among groups of mangabeys and African colobus monkeys. Diets are by percent feeding time and food
type. Data are from Bergmüller et al. (in prep), Ham (1994), Poulsen et al. (2001), Lambert et al. (2004), Dasilva (1994), Davies et
al. (1999), Maisels et al. (1994), Marsh (1981), Poulsen et al. (2002), Fashing (2001), and Harris and Chapman (2007).
Fig. 2. Dietary variation in populations of baboons and geladas. Diets are by percent feeding time and food type. Data are from
Dunbar (1988), Norton et al. (1987), Barton (1989), Dunbar and Dunbar (1974), and Bentley-Condit (2009).
American Journal of Physical Anthropology
DENTAL MICROWEAR TEXTURE AND ANTHROPOID DIETS
Of the three colobines studied here, C. polykomos, P.
badius, and C. guereza, C. guereza appears to be the
closest to what might be described as a specialized folivore. For instance, in a study of eight C. guereza groups
in Kibale National Forest, Uganda four groups ate more
than 90% leaves while the least folivorous group ate
78.52% leaves, 17.72% fruits, and only 1.29% seeds (data
are percent-time feeding; Harris and Chapman, 2007).
The most folivorous groups ate from 23 to 50% mature
(likely tougher) leaves, while the lowest percentage of
time spent feeding on mature leaves was 12% (Harris
and Chapman, 2007). In contrast, Fashing (2001)
reported lower levels of folivory for C. guereza in the
Kakamega Forest, Kenya (48–57% leaves) and suggested
that fruits were actually preferred. Fashing (2001) also
noted that C. guereza from a range of sites appears to
have generally lower dietary diversity than other
colobine species (including P. badius). The dental sample
of C. guereza studied here were derived from the Mount
Kenya environs, and no studies are published on
the diet of this population; thus, the degree of folivory
represented in the sample is at present unknown.
For the purposes of making predictions concerning
expected microwear textures, the sample is considered
as that of a specialized folivore that consumes seeds only
infrequently.
Published reports indicate that P. badius relies on a
diet more heavily focused on seed eating. For instance,
P. badius badius on Tiwai Island, Sierra Leone ate 52%
leaves and 25% seeds (Davies et al., 1999). Similarly,
populations of P. badius temminckii have a diet with a
significant proportion of seeds, in the 18–19% range
(Starin, 1991). Colobus polykomos appears to have a diet
very similar to that of P. badius: 57% leaves and 33%
seeds (Dasilva, 1989, 1994; Davies et al., 1999). Thus, P.
badius and C. polykomos can be described as habitual
leaf and seed eaters. If the seeds consumed are tough or
hard (or both), remains to be quantified. Qualitative
descriptions have characterized them as tough (Davies
et al., 1999). However, Pentaclethra macrophylla seeds
reported as constituting 13% of C. polykomos diet by Davies et al. (1999) are described as ‘‘persistent,’’ ‘‘hard and
woody’’ and as having a ‘‘hard’’ seed coat (Ehiagbonare
and Onyibe, 2008).
It is important to emphasize that while studies like
that of Koyabu and Endo (2009) assume hard seeds in
some African colobine diets, the mechanical properties of
seeds eaten have not been measured. It is possible that
the diets of P. badius and C. polykomos include or do not
include substantial quantities of hard seeds. Until such
time as data on the hardness of seeds known to be eaten
by these species are available, the consumption of the
seeds and pods of P. macrophylla by C. polykomos offers
the best evidence for durophagy by an African colobine.
Based on the dietary descriptions for this analysis
grouping (5CERC), we predict that the obligate hardfood eater, C. atys, should have the highest values for
dental microwear complexity followed by L. albigena, the
facultative-hard-food fallback feeder. We expect the specialized folivore, C. guereza, to have minimal values for
complexity and the highest values for anisotropy. We
expect C. polykomos and P. badius to have more intermediate values for anisotropy and complexity. It is possible
that C. polykomos might have greater values for
complexity than P. badius, if seeds eaten by P. badius
are less mechanically challenging. But in either case, we
expect C. guereza to have lower values for heterogeneity
557
than P. badius and C. polykomos. We expect textural fill
volume to parallel the results for complexity, with C.
atys having the greatest textural fill volume and C. guereza having the lowest.
Diets of 3PAP group. The second analysis grouping
consists of three mainly terrestrial, relatively open-habitat African papionins: P. cynocephalus, P. ursinus, and T.
gelada. Behavioral observations of extant Papio indicate
a diet that is, if nothing else, flexible and variable
(Dunbar, 1988; Whiten et al., 1991; Altmann, 1998;
Bentley-Condit, 2009). Food resources such as fruits and
underground storage organs (USOs) tend to be consumed
to varying degrees from population to population and
species to species (Fig. 2). Temporal variation in the consumption of different food resources is also evident in
Papio. In contrast, Theropithecus is known to have a
less variable diet typically composed of 90% grass
(Dunbar and Dunbar, 1974), with a preference for grass
blades when available (Iwamoto, 1993; see Fig. 2).
P. ursinus is known to consume USOs, which have figured prominently in various hypotheses of hominin
diets. Thus, it would be useful to identify a microwear
texture signal correlated with USO consumption. However, various populations of P. cynocephalus also consume USOs (Fig. 2), and the appropriate framework for
identifying microwear correlates of USO consumption
requires comparison of populations of Papio known to
eat quantities of USOs with those that do not (Daegling
and Grine, 1999). Moreover, the physical properties and
abrasiveness of USOs are variable (Dominy et al., 2008).
Thus, the main comparison possible here is between the
two Papio species, which are best considered dietary
generalists, and T.gelada, which can be described as a
specialized grass eater (Dunbar and Dunbar, 1974).
Based on this understanding of Papio and Theropithecus diets, we predict that T. gelada will have less complex microwear, lower textural fill volume, less heterogeneous microwear, and more anisotropic microwear
textures than P. cynocephalus and P. ursinus. Any differences between P. ursinus and P. cynocephalus might be
due to USO eating by P. ursinus, but it remains possible
that the P. cynocephalus sample used here included individuals that also ate quantities of USOs, or that each
species ate different types of USOs, so results will be
interpreted with caution.
Diets of 3HOM group. The third analysis grouping
includes P. troglodytes and two species of Gorilla, G. gorilla, and G. beringei. The first behavioral studies of gorillas in the wild focused on mountain gorillas, G. beringei
from the high Virungas (which is the provenience of the
specimens studied here), where fleshy fruits are relatively
sparse (e.g., Schaller, 1963; Fossey and Harcourt, 1977;
Watts, 1984). Thus, gorillas were initially thought to be
primarily folivorous, with those assumptions being
accepted in the morphological literature. Subsequent
work showed that lowland gorillas (G. gorilla) had a
much more variable diet that included significant
amounts of fruit (Sabater-Pi, 1977; Tutin and Fernandez,
1985; Nishihara, 1995; Remis, 1997; Rogers et al., 2004).
The consensus now seems to be that, while mountain
gorillas consume more fleshy fruits when these are available (Ganas et al., 2004; Rothman et al., 2008), the diets
of higher altitude populations, including the Karisoke
individuals examined in this study, are limited by a lack
of regular access to such foods (Rogers et al., 2004). By
contrast, lowland gorillas more frequently consume
American Journal of Physical Anthropology
558
R.S. SCOTT ET AL.
preferred soft fruit and fall back on terrestrial herbs,
leaves, pith, and even termites when favored foods are
not available (Yamagiwa et al., 1996; Doran et al., 2002;
Cipolletta et al., 2007; Masi, 2008; Doran-Sheehy et al.,
2009).
The common chimpanzee, P. troglodytes, has been studied at several heavily forested sites (Hladik, 1977b;
Wrangham, 1977; Nishida and Uehara, 1983; Goodall,
1986; Tutin et al., 1991, 1997; Wrangham et al., 1991;
Newton-Fisher, 1999; Hunt and McGrew, 2002; Tweheyo
et al., 2004; Morgan and Sanz, 2006) and also at some
more open localities (Suzuki, 1969; McGrew et al., 1981,
1988; Moore, 1992, 1994; Hunt and McGrew, 2002;
Pruetz, 2006; Copeland, 2009). Across this range of habitats, however, chimps prefer soft fruits as a mainstay in
their diet, even increasing foraging ranges during times
of fruit scarcity to pursue them (Wrangham et al., 1998).
Still, while the fruit component of their diet may provide
nutritional constancy across habitats (Hohmann et al.,
2010), chimps will consume a wide range of other foods,
most notably, leaves, pith, oil palm, terrestrial herbaceous
vegetation, and animal matter, at various times of the
year (Wrangham et al., 1991, 1998; McGrew, 1992; Tutin
et al., 1997; Yamakoshi, 1998; Basabose, 2002; Humle
and Matsuzawa, 2004; Deblauwe and Janssens, 2008).
Based on these differences in diet, we expect gorillas
to exhibit less complexity and heterogeneity in their
microwear textures, and more anisotropy than in common chimpanzees. However, we also expect lowland and
mountain gorillas (especially G. beringei from higher elevations) to exhibit more subtle differences in microwear
texture, with the latter having more microwear surface
texture anisotropy and perhaps less complexity and heterogeneity than the former.
Diets of 6CEB group. The fourth analysis grouping
includes A. palliata, A. belzebuth, A. hybridus, and three
taxa of ‘‘apelloid’’ capuchins. A. palliata is most accurately described as a folivore and frugivore. Chapman
(1988) noted a diet of 49% leaves and 28.5% fruit for A.
palliata in Santa Rosa National Park, Costa Rica. A
review of A. palliata diets in Los Tuxtlas, Mexico
revealed a range of 26.6–87.3% leaves and 12.7–59%
fruit (Cristobal-Azkarate and Arroyo-Rodriguez, 2007).
Norconk et al. (2009) report a genus-wide average 54%
leaves for Alouatta, including mature leaves. Some data
on food properties are available for two species of
Alouatta, A. seniculus from Turtle Mountain, Guyana
and A. palliata from Costa Rica and Nicaragua. Norconk
et al. (2009) report average food toughness (R) of 1,111 J/
m2 for A. seniculus and describe it as a frequent consumer of tough leaves that was also capable of breaching
not only ‘‘exceedingly tough’’ but also rare seed coats of
Catostemma fragrans. Recent studies of A. palliata in
Costa Rica and Nicaragua documented lower average
toughness values (300–900 J/m2), but with significant
variations between locations on the leaves (Teaford et
al., 2006). A recent study of A. palliata in Nicaragua
(Raguet-Schofield, 2010) scored sex and age specific average dietary toughness based on time spent feeding and
mean toughness (R) for commonly eaten mature leaves.
Average toughness (R) for these leaves ranged between
349 and 794 J/m2. We consider it likely that our sample
of A. palliata consumed tough leaves in significant quantity. However, we also consider the exploitation of
diverse resources likely and expect that fruits were also
eaten frequently.
American Journal of Physical Anthropology
What is most important here is how howler monkeys
compare to the other taxa in our sample in terms of food
material properties. For example, how does Alouatta
compare to Ateles, the spider monkeys? Ateles has long
been considered a genus of highly frugivorous primate.
Di Fiore et al. (2008) reviewed spider monkey diets and
reported an annual mean time spent feeding on fruit of
77% across studies of Ateles geoffroyi, A. paniscus, A.
belzebuth, and A. chamek. Percent time spent feeding on
fruits ranged from 39 to 94% and percent time feeding
on leaves ranged from 6 to 55% for several studies of
A. geoffroyi in Mesoamerica (Mexico, Guatemala, Costa
Rica, El Salvador, and Panama; Gonzalez-Zamora et al.,
2009). A. belzebuth consumption of leaves would appear
to rise as high as around 25% of feeding time at some
times, but annually averages from 7 to 13% of feeding
time with fruit and mainly ripe fruit remaining the dominant part of A. belzebuth diets (Dew, 2005; Suarez,
2006; Felton et al., 2008).
Study of diet in A. hybridus (also in our sample) is as
yet minimal. According to observations from a forest
fragment at San Juan del Carere, Colombia, A. hybridus
averaged 53% of feeding time on fruits and 27% of feeding time on leaves (Aldana Saavedra, 2009). At Serrania
de Las Quinchas, Colombia A. hybridus appeared to rely
even more on fruits (Guerrero and Link, 2007; Link and
Morales Jimenez, 2007). What seems quite clear is that
compared to any species of Alouatta, Ateles spp. appear
to consume more fruit flesh, and likely experience a
much less mechanically challenging diet. Not surprisingly, Ateles is broadly acknowledged to be an important
Neotropical seed-disperser (Russo et al., 2005; Link and
Di Fiore, 2006). Ateles paniscus had a mean dietary
toughness of 839 J/m2 and a maximum dietary toughness of 2,139 J/m2 (Norconk et al., 2009). This contrasts
with mean dietary toughness of 1,111 J/m2 (as noted earlier) and maximum dietary toughness of 7,902 J/m2 for
A. seniculus at the same site (Norconk et al., 2009).
Our sample includes three taxa of tufted capuchins,
the ‘‘apelloids’’ Cebus xanthosternos, C. nigritus robustus,
and hybrids of C. nigritus and C. libidinosus (see
Rylands and Mittermeier, 2009 for taxonomic notes).
These have traditionally been thought to be capable of
processing very hard objects such as palm nuts (e.g., Terborgh and Janson, 1983), and Wright (2005) regarded
craniodental characters of this group as derived features
potentially permitting the processing of more stress-limited foods. Work on the diets of tufted capuchins has
focused on Cebus apella (Wright, 2005; Norconk et al.,
2009; Wright et al., 2009) and C. libidinosus (Chalk et
al., 2008; Wright et al., 2009). Findings of these studies
demonstrate mastication of tougher foods by both C.
libidinosus (maximum toughness 5 10,350 J/m2) and
Cebus apella (maximum toughness 5 10,909 J/m2) compared to the wedge-capped (nonapelloid) capuchin, Cebus
olivaceus (maximum toughness 5 2,792 J/m2). It is also
worth noting that these studies found a tremendous
range in food toughness for the tufted capuchins. Of
course, an added complication in this behavioral data set
is that C. libidinosus (Fragaszy et al., 2004; Visalberghi
et al., 2008) and more recently C. xanthosternos (Canale
et al., 2009) use stone tools while on the ground to
exploit particularly hard foods like palm nuts. Thus,
while they are capable of eating a wide range of foods in
a variety of different ways, available data suggest that
the tufted capuchins may be considered hard-food fallback feeders.
DENTAL MICROWEAR TEXTURE AND ANTHROPOID DIETS
The available literature suggests the following concerning the New World monkeys in our sample. First,
both species of Ateles appear to have the least mechanically challenging diets and, compared to the other
species, should thus have decreased values for complexity, anisotropy, and textural fill volume. Consumption of tough and mature leaves is expected to result
in higher anisotropy values for Alouatta compared to
the rest of the sample in this group. The Ateles species
may have the least variable diets in the group in
terms of material properties, while both Alouatta and
Ateles probably had a smaller range of food toughness
compared to Cebus. Thus, Ateles may have the lowest
values for heterogeneity among the New World monkeys, with Cebus having the greatest. The three species of Cebus are also expected to have at least some
specimens that display very elevated values for complexity linked to recent consumption of resources like
palm nuts.
Diets of 5CAT group. The fifth analysis grouping
includes P. pygmaeus, M. fascicularis, and three colobines, P. rubicunda, S. entellus, and T. cristatus.
Although none of these taxa have been subject to the
extensive, long-term study of some of the African apes,
they are still known well enough to yield certain expectations for microwear analysis. Orangutans are perhaps
the best known of this group and have traditionally been
recognized as frugivores, albeit with marked seasonal
changes in diet at certain sites (MacKinnon, 1974; Rodman, 1977). Recent work has shown that, when faced
with seasonal fluctuations in fruit availability, those diet
changes can include more time spent feeding on insects,
unripe fruit, leaves, or bark (Knott, 1998; Fox et al.,
2004; Wich et al., 2006; Vogel et al., 2009; Kanamori et
al., 2010). A rough estimate of annual averages for different foods would include 60–70% fruit, 10–20%
leaves, 5–20% bark, and 0–10% insects, depending on
the site and season(s) of data collection (Wich et al.,
2006). Orangutans may preferentially seek out soft, ripe
fruit when possible (Leighton, 1993; Constantino et al.,
2009) and they are certainly capable of processing
extremely hard seeds if necessary (Lucas et al., 1994;
Constantino et al., 2009). However, seeds eaten as fallback foods are also surprisingly tough (Vogel et al., 2008,
2009). The same could be said about bark that is processed at certain times of the year—it can be soft (Fox et
al., 2004), but it is often very tough (Vogel et al., 2008).
Macaca fascicularis is one of the more common primates used in laboratory studies, yet its diet in the wild
has received less attention than that of the orangutan.
As with most macaques, it has often been portrayed as
an omnivore (Kurland, 1973; Poirier and Smith, 1974;
Hock and Sasekumar, 1979), but if given a choice, it
would probably prefer soft fruit (Rodman, 1978; Wheatley, 1978, 1980; Sussman and Tattersall, 1981; Berenstain, 1986; Lucas and Corlett, 1991; Son, 2003). Estimates of time spent feeding on different items include
67% fruits, 17% leaves, 9% flowers, and 4% insects
(Yeager, 1996). Long-tailed macaques eat many of the
same fruits as sympatric orangutans (Ungar, 1995). Corlett and Lucas (1990) noted that M. fascicularis rarely
break seeds, and Lucas and Teaford (1994) noted that
some leaves in the diet do contain significant amounts of
silica. As a case in point, Ungar (1995) has noted, while
P. pygmaeus consumes the ripe, hardened fruits of
Gnetum cf. latifollum at Ketambe, M. fascicularis is only
able to eat softer, unripened ones.
559
The three Asian colobines are generally thought to fall
along a continuum from fairly dedicated leaf-eating (T.
cristatus), through seed-eating (P. rubicunda), to a variable diet including significant amounts of time spent
feeding terrestrially (S. entellus). Trachypithecus cristatus is the least well studied of the three, with the only
published data being either anecdotal reports (Hock and
Sasekumar, 1979; Kool, 1986), or longer term studies of
what was then thought to be a subspecies of T. cristatus
but is now thought to be a different species, T. auratus
(Brotoisworo and Dirgayusa, 1991; Bennett and Davies,
1994). The net result is that we can say nothing more
than Caton did in 1999—that is, that T. cristatus probably consumes a significant amount of leaves (i.e., 55–
80%), and some fruit and flowers (Caton, 1999). By contrast, P. rubicunda was the focus of pioneering work by
Davies, and also Supriatna et al., in the 1980s, which
really began to change our perspectives on the diets of
langurs. In essence, this species is ‘‘not an obligate folivore’’ and instead consumes high proportions of seeds
and fruits (30–35% of each; Davies, 1984, 1991;
Supriatna et al., 1986). The leaves that it does eat tend
to be immature and readily digestible (Davies et al.,
1988). Unfortunately, there has been some confusion in
the literature about the seeds consumed by P. rubicunda.
They are generally not hard and tough (as suggested by
Koyabu and Endo, 2010), but instead, pliant and tough
(Lucas and Teaford, 1994). Not unexpectedly, S. entellus,
with its wide range of habitats, has a wide range of
reported diets. However, leaves and fruit are always the
main components, ranging from 45 to 67% and 20 to
45%, respectively (Hladik, 1977a; Oppenheimer, 1978;
Srivastava, 1989; Newton, 1992; Koenig and Borries,
2001; Sayers and Norconk, 2008). Within those broad
categories, gray langurs seem to prefer young leaves,
flowers, and seeds rather than mature leaves, but at certain times of the year, mature leaves may still dominate
feeding times (Koenig and Borries, 2001; Sayers and
Norconk, 2008). Interestingly, fallback foods vary significantly between habitats, with lowland groups including
more insects, while highland groups include more USOs
and bark (Sayers and Norconk, 2008). Of course, underlying all of these diet differences is the fact that S. entellus is generally regarded as the most terrestrial colobine
(Dunbar and Badam, 1998; Dunbar et al., 2004).
Based on these diet differences, we might expect P.
pygmaeus, or perhaps M. fascicularis, to exhibit the
most complex and heterogeneous microwear textures,
assuming that specimens of either or both had access to
more resistant foods in the weeks before collection. By
contrast, the colobines would be expected to show less
complexity and heterogeneity, and perhaps more anisotropy, especially if P. rubicunda was indeed consuming
tough seeds rather than hard ones. The unknown in this
would be the impact of terrestrial feeding on S. entellus,
which might exhibit reduced or elevated heterogeneity if
either a limited range of terrestrial abrasives or a wide
range of them, were dominating microwear textures.
RESULTS
Two MANOVA tests with all four microwear texture
variables were carried out: first with genus as the factor
or grouping variable, and second with species as the factor or grouping variable. There was significant variation
in microwear texture for both genera (P \ 0.001,
Wilks’ k 5 0.351, F 5 7.47, df 5 60, 1,454) and species
American Journal of Physical Anthropology
560
R.S. SCOTT ET AL.
(P \ 0.0001, Wilks’ k 5 0.297, F 5 6.20, df 5 84, 1,448).
One possibility is that these significant results could be
driven by only a single texture variable so ANOVA’s for
each variable were performed by genus and then by
species. In all cases, these comparisons were significant
(P [ 0.0001; see Table 2).
5CERC group
Significant contrasts were spread across all four dental
microwear texture variables for the 5CERC analysis in
both the generic and species level analyses (Table 3). For
the genus-level analysis, Colobus had significantly lower
mean complexity than Cercocebus (P \ 0.001, Tukey’s
HSD) and Lophocebus (P 5 0.029, Fisher’s LSD). For anisotropy, it was the genus Cercocebus that differed from
the other genera. Cercocebus had lower anisotropy
than Colobus (P \ 0.001, Tukey’s HSD) and Procolobus
(P \ 0.001, Tukey’s HSD), and potentially lower anisotropy than Lophocebus (P 5 0.034, Fisher’s LSD).
Lophocebus also had potentially lower anisotropy
than Procolobus (P 5 0.021, Fisher’s LSD). Results for
textural fill volume were similar to the complexity
results, with Colobus again appearing distinct by virtue
of lower mean textural fill volume compared to Cercocebus (P 5 0.008, Tukey’s HSD) and Lophocebus (P \
0.001, Tukey’s HSD). Lower mean texture fill volume for
Procolobus compared to Lophocebus could not be rejected
(P 5 0.048, Fisher’s LSD). Lophocebus had more heterogeneous microwear than Colobus (P 5 0.02, Tukey’s
HSD) and possibly Cercocebus (P 5 0.023, Fisher’s LSD).
The species level analysis indicates differences
between the two Colobus species in complexity (P \
0.0001, Tukey’s HSD). Colobus guereza represents an
extreme low for complexity and was also significantly
lower in complexity compared to C. atys, L. albigena (P
\ 0.001, Tukey’s HSD) and P. badius (P \ 0.002, Tukey’s
HSD). Thus, with respect to complexity, it is the low values for C. guereza that are significant (Table 3; Fig. 3).
Colobus guereza and P. badius had the highest means
and C. atys the lowest mean for microwear texture anisotropy. C. atys had significantly lower mean anisotropy
compared to all three colobine species (P \ 0.01, Tukey’s
HSD) and differed from L. albigena in anisotropy by
Fisher’s LSD (P 5 0.035), but not by Tukey’s HSD (P 5
0.206). Thus, while low complexity seems to differentiate
C. guereza, low anisotropy appears to distinguish C.
atys. This is shown in Figure 4, wherein the histogram
of anisotropy for C. atys is distinct from those for the
other four cercopithecoids. The C. atys sample displays a
concentration of low anisotropy scores (\ 0.0045) and
very few higher anisotropy scores ([ 0.0055).
Results for textural fill volume for the most part
paralleled those for complexity (Table 3). Again, it
appears to be C. guereza that was distinguished from
the other four cercopithecoids with lower textural fill
TABLE 2. Statistical analysis of four dental microwear texture variables by genus and species
A. MANOVA
Between genera
Wilks’ Lambda
Pillai Trace
Hotelling-Lawley
Between species
Wilks’ Lambda
Pillai Trace
Hotelling-Lawley
B. ANOVAs
Test statistic
F
df
P
0.351
0.858
1.319
7.47
6.83
8.15
60, 1,454
60, 1,500
60, 1138.4
\ 0.001
\ 0.001
\ 0.001
0.297
0.975
1.569
6.20
5.66
6.81
84, 1,448
84, 1,476
84, 1193.9
\ 0.001
\ 0.001
\ 0.001
Variable
F
df
p
Complexity (Asfc)
Anisotropy (epLsar1.8lm)
Textural fill volume (Tfv)
Heterogeneity (Hasfc81)
16.02
7.19
6.88
7.01
15,
15,
15,
15,
375
375
375
375
\ 0.001
\ 0.001
\ 0.001
\ 0.001
Complexity (Asfc)
Anisotropy (epLsar1.8lm)
Textural fill volume (Tfv)
Heterogeneity (Hasfc81)
13.52
5.62
5.89
5.80
21,
21,
21,
21,
369
369
369
369
\ 0.001
\ 0.001
\ 0.001
\ 0.001
Between genera
Between species
TABLE 3. Statistical analysis of 5CERC with pairwise comparisons
A. ANOVAs
Variable
F
df
Complexity (Asfc)
Anisotropy (epLsar1.8lm)
Textural fill volume (Tfv)
Heterogeneity (Hasfc81)
8.20
10.85
7.18
3.23
3,
3,
3,
3,
142
142
142
142
\ 0.001
\ 0.001
\ 0.001
0.022
Complexity (Asfc)
Anisotropy (epLsar1.8lm)
Textural fill volume (Tfv)
Heterogeneity (Hasfc81)
10.95
8.10
6.10
2.99
4,
4,
4,
4,
141
141
141
141
\ 0.001
\ 0.001
\ 0.001
0.021
Between genera
Between species
American Journal of Physical Anthropology
P
TABLE 3. (Continued)
P
B. Pairwise comparisons between genera
Complexity (Asfc)
Tukey’s HSD
Fisher’s LSD
Cercocebus
Cercocebus
Cercocebus
Colobus
Colobus
Lophocebus
v.
v.
v.
v.
v.
v.
Colobus
Lophocebus
Procolobus
Lophocebus
Procolobus
Procolobus
\ 0.001
0.363
0.464
0.121
0.227
1
\ 0.001
0.106
0.148
0.029
0.059
0.977
Cercocebus
Cercocebus
Cercocebus
Colobus
Colobus
Lophocebus
v.
v.
v.
v.
v.
v.
Colobus
Lophocebus
Procolobus
Lophocebus
Procolobus
Procolobus
\ 0.001
0.14
\ 0.001
0.405
0.568
0.091
0
0.034
\ 0.001
0.122
0.199
0.021
Cercocebus
Cercocebus
Cercocebus
Colobus
Colobus
Lophocebus
v.
v.
v.
v.
v.
v.
Colobus
Lophocebus
Procolobus
Lophocebus
Procolobus
Procolobus
0.008
0.222
0.929
\ 0.001
0.407
0.191
0.002
0.057
0.543
\ 0.001
0.123
0.048
Cercocebus
Cercocebus
Cercocebus
Colobus
Colobus
Lophocebus
v.
v.
v.
v.
v.
v.
Colobus
Lophocebus
Procolobus
Lophocebus
Procolobus
Procolobus
0.856
0.1
0.649
0.02
0.325
0.885
0.427
0.023
0.246
0.004
0.092
0.466
Anisotropy (epLsar1.8lm)
Textural fill volume (Tfv)
Heterogeneity (Hasfc81)
P
C. Pairwise comparisons between species
Complexity (Asfc)
Tukey’s HSD
Fisher’s LSD
Cercocebus atys
Cercocebus atys
Cercocebus atys
Cercocebus atys
Colobus guereza
Colobus guereza
Colobus guereza
Colobus polykomos
Colobus polykomos
Lophocebus albigena
v.
v.
v.
v.
v.
v.
v.
v.
v.
v.
Colobus guereza
Colobus polykomos
Lophocebus albigena
Procolobus badius
Colobus polykomos
Lophocebus albigena
Procolobus badius
Lophocebus albigena
Procolobus badius
Procolobus badius
\ 0.001
0.177
0.425
0.541
\ 0.001
\ 0.001
0.002
0.998
0.999
1
\ 0.001
0.029
0.089
0.127
\ 0.001
\ 0.001
\ 0.001
0.773
0.82
0.976
Cercocebus atys
Cercocebus atys
Cercocebus atys
Cercocebus atys
Colobus guereza
Colobus guereza
Colobus guereza
Colobus polykomos
Colobus polykomos
Lophocebus albigena
v.
v.
v.
v.
v.
v.
v.
v.
v.
v.
Colobus guereza
Colobus polykomos
Lophocebus albigena
Procolobus badius
Colobus polykomos
Lophocebus albigena
Procolobus badius
Lophocebus albigena
Procolobus badius
Procolobus badius
0.001
0.001
0.206
\ 0.001
0.999
0.605
0.845
0.698
0.708
0.138
\ 0.001
0
0.035
\ 0.001
0.82
0.153
0.309
0.2
0.205
0.022
Cercocebus atys
Cercocebus atys
Cercocebus atys
Cercocebus atys
Colobus guereza
Colobus guereza
Colobus guereza
Colobus polykomos
Colobus polykomos
Lophocebus albigena
v.
v.
v.
v.
v.
v.
v.
v.
v.
v.
Colobus guereza
Colobus polykomos
Lophocebus albigena
Procolobus badius
Colobus polykomos
Lophocebus albigena
Procolobus badius
Lophocebus albigena
Procolobus badius
Procolobus badius
0.004
0.355
0.303
0.973
0.485
\ 0.001
0.201
0.011
0.934
0.264
0.001
0.069
0.056
0.541
0.108
\ 0.001
0.034
0.002
0.431
0.047
Cercocebus atys
Cercocebus atys
Cercocebus atys
Cercocebus atys
Colobus guereza
Colobus guereza
Colobus guereza
Colobus polykomos
Colobus polykomos
Lophocebus albigena
v.
v.
v.
v.
v.
v.
v.
v.
v.
v.
Colobus guereza
Colobus polykomos
Lophocebus albigena
Procolobus badius
Colobus polykomos
Lophocebus albigena
Procolobus badius
Lophocebus albigena
Procolobus badius
Procolobus badius
0.531
1
0.145
0.768
0.579
0.01
0.179
0.292
0.865
0.949
0.124
0.905
0.023
0.244
0.143
0.001
0.029
0.053
0.329
0.464
Anisotropy (epLsar1.8lm)
Textural fill volume (Tfv)
Heterogeneity (Hasfc81)
Values for P that are significant at a 5 0.05 are shown in bold print.
562
R.S. SCOTT ET AL.
Fig. 3. Histograms showing relative frequencies of microwear texture complexity levels for the five species in the 5CERC
group.
volume than C. atys and L. albigena (P 5 0.004 and
P \ 0.0001, Tukey’s HSD) and P. badius (P 5 0.034,
Fisher’s LSD). The mean textural fill volume for C.
guereza was also lower than the mean for C. polykomos, but this difference was not significant. Colobus
polykomos had the second lowest textural fill volume
next to C. guereza and differed significantly from L.
albigena, which had the highest textural fill volume
(P 5 0.011).
Colobus guereza had the lowest heterogeneity of all
five cercopithecoids and was significantly lower in heterogeneity compared to L. albigena (P 5 0.01, Tukey’s
HSD) and potentially P. badius (P 5 0.029, Fisher’s
American Journal of Physical Anthropology
LSD). L. albigena had the highest heterogeneity in the
5CERC analysis grouping and potentially also differed
from C. atys (P 5 0.023, Fisher’s LSD).
3PAP group
Three of the four microwear texture variables tested for
the 3PAP analysis grouping evinced significant variation
between taxa (Table 4). These variables were complexity,
anisotropy, and heterogeneity. Textural fill volume did not
show significant variation. In each case, T. gelada differed
from the two Papio samples and thus the genus and species level analyses were entirely congruent.
DENTAL MICROWEAR TEXTURE AND ANTHROPOID DIETS
563
Fig. 4. Histograms showing relative frequencies of microwear texture anisotropy levels for the five species in the 5CERC
group.
T. gelada had significantly lower complexity than both
P. cynocephalus and P. ursinus (P \ 0.001, Tukey’s
HSD). Similarly, T. gelada had significantly higher anisotropy than both P. cynocephalus and P. ursinus (P \
0.001, Tukey’s HSD). With respect to microwear heterogeneity, T. gelada had a significantly lower mean than P.
cynocephalus (P \ 0.001, Tukey’s HSD). The comparison
between T. gelada and P. ursinus was more equivocal
and significant only by Fisher’s LSD (P 5 0.028).
0.025; Table 5). Anisotropy was higher and heterogeneity
lower for Gorilla compared to Pan. Complexity and textural fill volume did not differ significantly between Gorilla and Pan. The species level comparison for the African apes in which the Gorilla sample was split into G.
gorilla and G. beringei resulted in no significant microwear contrasts.
3HOM group
All four microwear texture variables showed significant variation at the genus and species levels (Table 6).
No unequivocal significant differences were found
between either the two Ateles species or the three taxa
of ‘‘apelloid’’ capuchins. Thus, the most pertinent analy-
The genus-level comparison of Pan to Gorilla showed
significance for two of the four microwear texture variables: anisotropy (P 5 0.032) and heterogeneity (P 5
6CEB group
American Journal of Physical Anthropology
564
R.S. SCOTT ET AL.
TABLE 4. Statistical analysis of 3PAP with pairwise comparisons
A. ANOVAs
Variable
F
df
P
Between genera
Complexity (Asfc)
Anisotropy (epLsar1.8lm)
Textural fill volume (Tfv)
Heterogeneity (Hasfc81)
43.22
24.56
0.002
14.96
1,
1,
1,
1,
49
49
49
49
\ 0.001
\ 0.001
0.965
\ 0.001
Complexity (Asfc)
Anisotropy (epLsar1.8lm)
Textural fill volume (Tfv)
Heterogeneity (Hasfc81)
21.17
12.21
2.78
8.87
2,
2,
2,
2,
48
48
48
48
\ 0.001
\ 0.001
0.072
0.001
Between species
P
B. Pairwise comparisons between species
Tukey’s HSD
Fisher’s LSD
Complexity (Asfc)
Papio cynocephalus
Papio cynocephalus
Papio ursinus
v.
v.
v.
Papio ursinus
Theropithecus gelada
Theropithecus gelada
0.998
\ 0.001
\ 0.001
0.948
\ 0.001
\ 0.001
Papio cynocephalus
Papio cynocephalus
Papio ursinus
v.
v.
v.
Papio ursinus
Theropithecus gelada
Theropithecus gelada
0.877
\ 0.001
\ 0.001
0.628
\ 0.001
\ 0.001
Papio cynocephalus
Papio cynocephalus
Papio ursinus
v.
v.
v.
Papio ursinus
Theropithecus gelada
Theropithecus gelada
0.284
\ 0.001
0.07
0.131
\ 0.001
0.028
Anisotropy (epLsar1.8lm)
Heterogeneity (Hasfc81)
Values for P that are significant at a 5 0.05 are shown in bold print.
TABLE 5. Statistical analysis of 3HOM
ANOVAs
Variable
F
df
P
Complexity (Asfc)
Anisotropy (epLsar1.8lm)
Textural fill volume (Tfv)
Heterogeneity (Hasfc81)
1.73
4.88
0.009
5.332
1,
1,
1,
1,
46
46
46
46
0.195
0.032
0.924
0.025
Complexity (Asfc)
Anisotropy (epLsar1.8lm)
Textural fill volume (Tfv)
Heterogeneity (Hasfc81)
0.992
2.41
0.023
2.61
2,
2,
2,
2,
45
45
45
45
0.379
0.102
0.977
0.084
Between genera
Between species
Values for P that are significant at a 5 0.05 are shown in bold
print.
0.05, Tukey’s HSD) and possibly Ateles (P \ 0.05, Fisher’s LSD) had less heterogeneous microwear than Cebus.
Species-level comparisons are shown in Table 6 and
these confirm the following:
1. A. palliata is distinguished from the other five species
by significantly lower complexity (P \ 0.001, Tukey’s
HSD).
2. A. palliata is also generally distinguished from the
other species by higher anisotropy at least according
to Fisher’s LSD for each comparison.
3. Ateles and Alouatta tend to have lower textural fill
volumes than Cebus.
4. A. hybridus appears to have the lowest heterogeneity
in the 6CEB group.
5CAT group
sis might be the generic-level comparison between
Ateles, Alouatta, and Cebus.
The means for complexity, anisotropy, and textural fill
volume for Ateles were all intermediate between those
for ‘‘apelloid’’ capuchins and Alouatta. For complexity, all
three contrasts were significant. Complexity of Cebus
microwear was significantly greater than complexity of
Ateles microwear (P \ 0.014, Tukey’s HSD), which was
in turn significantly greater than complexity of Alouatta
microwear (P \ 0.001, Tukey’s HSD). High anisotropy
distinguished Alouatta, where contrasts with Cebus (P \
0.001) and Ateles (P 5 0.001) were both significant
according to Tukey’s HSD. Ateles and Cebus did not have
significantly different means for anisotropy. Cebus differed significantly from Alouatta and Ateles due to
greater textural fill volume (P \ 0.001, Tukey’s HSD).
Finally, with respect to heterogeneity, Alouatta (P \
American Journal of Physical Anthropology
The genus- and species-level analyses for the 5CAT
group were identical as all five taxa were distinct at the
generic level. The anisotropy texture variable did not
differ across the five taxa, but the other three variables
did (Table 7).
Complexity and textural fill volume results were similar. In both cases, M. fascicularis had the highest values,
and it was M. fascicularis that tended to be separated
from the other species when there were significant
results. According to Tukey’s HSD, M. fascicularis had
significantly higher complexity compared to all three
Asian colobines: T. cristatus (P \ 0.001), S. entellus (P 5
0.001), and P. rubicunda (P 5 0.024). Some similar differences were evident for textural fill volume where M.
fascicularis was distinguished from S. entellus (P 5
0.031, Tukey’s HSD) and P. rubicunda (P 5 0.027,
Tukey’s HSD).
565
DENTAL MICROWEAR TEXTURE AND ANTHROPOID DIETS
TABLE 6. Statistical analysis of 6CEB with pairwise comparisons
A. ANOVAs
Variable
F
df
P
Between genera
Complexity (Asfc)
Anisotropy (epLsar1.8lm)
Textural fill volume (Tfv)
Heterogeneity (Hasfc81)
74.15
13.98
22.59
4.15
2,
2,
2,
2,
76
76
76
76
\ 0.001
\ 0.001
\0.001
0.02
Complexity (Asfc)
Anisotropy (epLsar1.8lm)
Textural fill volume (Tfv)
Heterogeneity (Hasfc81)
32.97
7.58
10.32
3.75
5,
5,
5,
5,
73
73
73
73
\ 0.001
\ 0.001
\ 0.001
0.004
Between species
P
B. Pairwise comparisons between genera
Tukey’s HSD
Fisher’s LSD
Complexity (Asfc)
Alouatta
Alouatta
Ateles
v.
v.
v.
Ateles
Cebus
Cebus
\ 0.001
\ 0.001
0.014
\ 0.001
\ 0.001
0.005
Alouatta
Alouatta
Ateles
v.
v.
v.
Ateles
Cebus
Cebus
0.001
0
0.809
0
0
0.537
Alouatta
Alouatta
Ateles
v.
v.
v.
Ateles
Cebus
Cebus
0.234
\ 0.001
\ 0.001
0.105
\ 0.001
\ 0.001
Alouatta
Alouatta
Ateles
v.
v.
v.
Ateles
Cebus
Cebus
0.991
0.026
0.086
0.897
0.01
0.034
Anisotropy (epLsar1.8lm)
Textural fill volume (Tfv)
Heterogeneity (Hasfc81)
P
C. Pairwise comparisons between species
Tukey’s HSD
Fisher’s LSD
Complexity (Asfc)
Alouatta palliata
Alouatta palliata
Alouatta palliata
Alouatta palliata
Alouatta palliata
Ateles belzebuth
Ateles belzebuth
Ateles belzebuth
Ateles belzebuth
Ateles hybridus
Ateles hybridus
Ateles hybridus
Cebus nigritus robustus
Cebus nigritus robustus
Cebus nigritus x libidinosus
Anisotropy (epLsar1.8lm)
Alouatta palliata
Alouatta palliata
Alouatta palliata
Alouatta palliata
Alouatta palliata
Ateles belzebuth
Ateles belzebuth
Ateles belzebuth
Ateles belzebuth
Ateles hybridus
Ateles hybridus
Ateles hybridus
Cebus nigritus robustus
Cebus nigritus robustus
Cebus nigritus x libidinosus
v.
v.
v.
v.
v.
v.
v.
v.
v.
v.
v.
v.
v.
v.
v.
Ateles belzebuth
Ateles hybridus
Cebus nigritus robustus
Cebus nigritus 3 libidinosus
Cebus xanthosternos
Ateles hybridus
Cebus nigritus robustus
Cebus nigritus 3 libidinosus
Cebus xanthosternos
Cebus nigritus robustus
Cebus nigritus 3 libidinosus
Cebus xanthosternos
Cebus nigritus 3 libidinosus
Cebus xanthosternos
Cebus xanthosternos
0
0
0
0
0
0.996
0.232
0.006
0.92
0.637
0.039
0.998
0.409
0.876
0.09
0
0
0
0
0
0.609
0.028
0
0.325
0.127
0.003
0.665
0.061
0.271
0.009
v.
v.
v.
v.
v.
v.
v.
v.
v.
v.
v.
v.
v.
v.
v.
Ateles belzebuth
Ateles hybridus
Cebus nigritus robustus
Cebus nigritus 3 libidinosus
Cebus xanthosternos
Ateles hybridus
Cebus nigritus robustus
Cebus nigritus 3 libidinosus
Cebus xanthosternos
Cebus nigritus robustus
Cebus nigritus 3 libidinosus
Cebus xanthosternos
Cebus nigritus 3 libidinosus
Cebus xanthosternos
Cebus xanthosternos
0.198
0.005
0.001
0
0.354
0.755
0.84
0.18
1
0.999
0.91
0.664
0.691
0.749
0.139
0.023
0
0
0
0.05
0.18
0.237
0.02
0.848
0.739
0.312
0.137
0.149
0.177
0.015
American Journal of Physical Anthropology
566
R.S. SCOTT ET AL.
TABLE 6. (Continued)
P
C. Pairwise comparisons between species
Textural fill volume (Tfv)
Alouatta palliata
Alouatta palliata
Alouatta palliata
Alouatta palliata
Alouatta palliata
Ateles belzebuth
Ateles belzebuth
Ateles belzebuth
Ateles belzebuth
Ateles hybridus
Ateles hybridus
Ateles hybridus
Cebus nigritus robustus
Cebus nigritus robustus
Cebus nigritus x libidinosus
Heterogeneity (Hasfc81)
Alouatta palliata
Alouatta palliata
Alouatta palliata
Alouatta palliata
Alouatta palliata
Ateles belzebuth
Ateles belzebuth
Ateles belzebuth
Ateles belzebuth
Ateles hybridus
Ateles hybridus
Ateles hybridus
Cebus nigritus robustus
Cebus nigritus robustus
Cebus nigritus x libidinosus
Tukey’s HSD
Fisher’s LSD
v.
v.
v.
v.
v.
v.
v.
v.
v.
v.
v.
v.
v.
v.
v.
Ateles belzebuth
Ateles hybridus
Cebus nigritus robustus
Cebus nigritus 3 libidinosus
Cebus xanthosternos
Ateles hybridus
Cebus nigritus robustus
Cebus nigritus 3 libidinosus
Cebus xanthosternos
Cebus nigritus robustus
Cebus nigritus 3 libidinosus
Cebus xanthosternos
Cebus nigritus 3 libidinosus
Cebus xanthosternos
Cebus xanthosternos
0.348
0.996
0
0
0.028
0.871
0.09
0.063
0.915
0.005
0.005
0.327
0.99
0.651
0.439
0.048
0.619
0
0
0.002
0.266
0.009
0.006
0.318
0
0
0.044
0.542
0.132
0.068
v.
v.
v.
v.
v.
v.
v.
v.
v.
v.
v.
v.
v.
v.
v.
Ateles belzebuth
Ateles hybridus
Cebus nigritus robustus
Cebus nigritus 3 libidinosus
Cebus xanthosternos
Ateles hybridus
Cebus nigritus robustus
Cebus nigritus 3 libidinosus
Cebus xanthosternos
Cebus nigritus robustus
Cebus nigritus 3 libidinosus
Cebus xanthosternos
Cebus nigritus 3 libidinosus
Cebus xanthosternos
Cebus xanthosternos
0.594
0.588
0.092
0.161
0.989
0.113
0.985
0.952
0.973
0.014
0.024
0.466
0.999
0.687
0.638
0.111
0.11
0.009
0.018
0.533
0.012
0.506
0.387
0.45
0.001
0.002
0.074
0.744
0.147
0.127
Values for P that are significant at a 5 0.05 are shown in bold print.
P. pygmaeus appears to have microwear that was intermediate between M. fascicularis and the Asian colobines in terms of complexity and textural fill volume,
although differences were only suggestive. However,
according to Fisher’s LSD, P. pygmaeus had significantly
more complex microwear than S. entellus (P 5 0.017),
and T. cristatus (P 5 0.014) and lower textural fill volume compared to M. fascicularis (P 5 0.021).
Microwear heterogeneity displayed a different pattern
than complexity and textural fill volume. Instead of
another contrast between the Asian colobines and M.
fascicularis, S. entellus tended to have the lowest heterogeneity compared to the other four species in the analysis. In three cases, differences were significant by
Tukey’s HSD: P. rubicunda (P \ 0.001), P. pygmaeus
(P 5 0.035), and M. fascicularis (P 5 0.012). The comparison between S. entellus and T. cristatus was only significant by Fisher’s LSD (P 50.009).
wear has been unclear. Here, microwear texture comparisons, using the largest comparative primate collection yet sampled, confirm this essential relationship
and suggest as much as 70% of the variance in microwear texture variables can be explained by species designation (1—Wilks’ k 5 0.70 in the species level analysis). Moreover, the importance of understanding the mechanical properties of foods consumed is highlighted by
the results for each of our analysis groupings. In general, these results emphasize the intrinsic variability of
primate microwear (see Fig. 5), the necessity of large
samples, the greater ease with which dietary extremes
may be recognized, and current limitations on the depth
of dietary reconstructions that can be offered for fossil
species. Insight into additional possibilities and limitations of dental microwear analyses are evident from a
consideration of each of the dental microwear texture
variables considered here.
DISCUSSION
Complexity
This study grows out of more than 30 years of
research on dental microwear that has repeatedly confirmed a relationship between food consumed and dental microwear. Prior studies have sometimes been limited by issues of observer errors (Grine et al., 2002;
Scott et al., 2008; Mihlbachler et al., 2010) and by the
limits of published diet information. Thus, the ultimate
precision of dietary reconstructions provided by micro-
Although both genus- and species-level analyses were
performed for the 5CERC analysis grouping, the significant difference in complexity between C. guereza and C.
polykomos shows that the species level analysis is most
relevant. This difference in complexity appears to
be driven by the extremely low complexity values for C.
guereza. The predicted means for complexity for 5CERC in
order from low to high were: C. guereza ? P. badius ?
American Journal of Physical Anthropology
567
DENTAL MICROWEAR TEXTURE AND ANTHROPOID DIETS
TABLE 7. Statistical analysis of 5CAT with pairwise comparisons
A. ANOVAs
Variable
F
Complexity (Asfc)
Anisotropy (epLsar1.8lm)
Textural fill volume (Tfv)
Heterogeneity (Hasfc81)
7.18
1.28
3.59
4.46
df
P
Between speciesa
3,
3,
3,
3,
\ 0.001
0.288
0.011
0.003
142
142
142
142
P
B. Pairwise comparisons between speciesa
Complexity (Asfc)
Macaca fascicularis
Macaca fascicularis
Macaca fascicularis
Macaca fascicularis
Pongo pygmaeus
Pongo pygmaeus
Pongo pygmaeus
Presbytis rubicunda
Presbytis rubicunda
Semnopithecus entellus
Textural fill volume (Tfv)
Macaca fascicularis
Macaca fascicularis
Macaca fascicularis
Macaca fascicularis
Pongo pygmaeus
Pongo pygmaeus
Pongo pygmaeus
Presbytis rubicunda
Presbytis rubicunda
Semnopithecus entellus
Heterogeneity (Hasfc81)
Macaca fascicularis
Macaca fascicularis
Macaca fascicularis
Macaca fascicularis
Pongo pygmaeus
Pongo pygmaeus
Pongo pygmaeus
Presbytis rubicunda
Presbytis rubicunda
Semnopithecus entellus
Tukey’s HSD
Fisher’s LSD
v.
v.
v.
v.
v.
v.
v.
v.
v.
v.
Pongo pygmaeus
Presbytis rubicunda
Semnopithecus entellus
Trachypithecus cristatus
Presbytis rubicunda
Semnopithecus entellus
Trachypithecus cristatus
Semnopithecus entellus
Trachypithecus cristatus
Trachypithecus cristatus
0.36
0.024
0.001
\ 0.001
0.697
0.118
0.099
0.724
0.77
1
0.07
0.003
\ 0.001
\ 0.001
0.201
0.017
0.014
0.217
0.248
0.84
v.
v.
v.
v.
v.
v.
v.
v.
v.
v.
Pongo pygmaeus
Presbytis rubicunda
Semnopithecus entellus
Trachypithecus cristatus
Presbytis rubicunda
Semnopithecus entellus
Trachypithecus cristatus
Semnopithecus entellus
Trachypithecus cristatus
Trachypithecus cristatus
0.14
0.027
0.031
0.475
0.932
0.843
0.984
0.998
0.719
0.609
0.021
0.003
0.004
0.105
0.431
0.31
0.597
0.758
0.214
0.157
v.
v.
v.
v.
v.
v.
v.
v.
v.
v.
Pongo pygmaeus
Presbytis rubicunda
Semnopithecus entellus
Trachypithecus cristatus
Presbytis rubicunda
Semnopithecus entellus
Trachypithecus cristatus
Semnopithecus entellus
Trachypithecus cristatus
Trachypithecus cristatus
0.998
0.657
0.012
0.991
0.543
0.035
1
0.001
0.488
0.068
0.771
0.18
0.001
0.648
0.129
0.004
0.862
\ 0.001
0.109
0.009
Values for P that are significant at a 5 0.05 are shown in bold print.
All species belonged to different genera and therefore the genus and species level analyses were the same.
a
C. polykomos ? L. albigena ? C. atys. The observed pattern was: C. guereza ? P. badius ? C. polykomos ? L.
albigena ? C. atys (see Fig. 3). Thus, there appears to be
broad accord between the predicted and observed patterns.
With that said though, it is only C. guereza, with its
consistently low complexity, which differed significantly
from the other members of this group. Although the
maximum complexity value for C. guereza was 6.52,
this was the only C. guereza specimen to have complexity greater than 2. Indeed, the next highest complexity
score was 1.90. Thus, out of 23 individuals, only one (or
4.3%, with a binomial 95% confidence interval of 0–
12.7%, see Table 8) could be characterized as having
high microwear complexity. This particular result is in
exact accord with our predictions based on studies of
diet in the three colobine species included here. Only C.
guereza appears to be potentially specialized as a folivore. The other two colobines likely consume a diet of
at least 25% seeds.
On the other end of the complexity spectrum is C.
atys. C. atys had significantly higher complexity than C.
guereza as already noted and also possibly significantly
higher complexity than C. polykomos. However, predicted differences between C. atys and L. albigena were
not found (but see Daegling et al., 2011). Thus, while
microwear predictions based on diet were supported by a
broadly consistent pattern, they were not always
reflected by significant results. It may be that the presence of some harder foods above a certain threshold
amount may result in more complex microwear, or it
may be that mixed samples of museum specimens do not
adequately represent the animals upon which diet differences in the literature are based.
The inclusion of seeds in their diets at rates of 25% for
P. badius (Davies et al., 1999) and 33% for C. polykomos
(Dasilva, 1989, 1994; Davies et al., 1999) may correspond
quite well with a tendency toward more complex microwear in these two species. For instance, if complexity
scores greater than two are once again considered as
‘‘complex,’’ then about 1/3 (31.0 and 31.3%, respectively)
of all the P. badius and C. polykomos might be characterized as having complex microwear. The hypothesis that
greater hardness of seeds in comparison to leaves generates microwear complexity is supported if C. polykomos
American Journal of Physical Anthropology
568
R.S. SCOTT ET AL.
Fig. 5. Photosimulation montages of selected specimens known to preserve antemortem microwear. Each montage is comprised
of photosimulations derived from 3D point clouds for four adjacent fields representing a total of 276 3 204 lm of each original occlusal surface. Specimens shown of (a) Theropithecus gelada (5FMNH 8174), (b) Alouatta palliata (5NMNH 363164), and (c) Gorilla beringei (5NMNH 545027) have anisotropic microwear texture with values of anisotropy above the 0.0050 cutpoint. Specimens
of (d) Cercocebus atys (5SMNK 5644), (e) Cebus nigritus robustus (5NMNH 518290), and (f) Pan troglodytes (5CMNH B2034—
upper M2) have complex microwear texture with values of complexity above the 2.00 cutpoint. SMNK 5885 (g) and SAPM 198174
(i), specimens of Colobus polykomos and Pongo pygmaeus respectively, have complex and anisotropic microwear texture. NMNH
406670 (h) is an example of Ateles belzebuth with neither complex nor anisotropic microwear texture.
and P. badius do eat hard seeds. At least for C. polykomos, the seeds of P. macrophylla are one candidate for
such a food.
An alternative explanation for higher complexity in P.
badius and C. polykomos compared to C. guereza might
be adhesive wear (see Teaford and Runestad, 1992) in P.
badius and C. polykomos. Potentially tough, woody seeds
and seed pods might lead to increased tooth on tooth
contact and generation of smaller pits.
Although the exact mechanical properties of African
colobine diets need study, a clear correspondence
between the percent of specimens with complex microwear and the percent of seeds in their diet seems supportable. The two binomial 95% confidence limits for the
percent of specimens with complexity greater than two
are: 8.5–54.0% for P. badius with N 5 16 and 14.2–
47.9% for C. polykomos with N 5 29. As it is likely that
the animals studied here actually consumed somewhere
between 10 and 50% seeds, a best case interpretation of
our results might be that the confidence limits on
‘‘complex’’ microwear do indeed represent a realistic expectation for the microwear patterns of colobine monkeys
consuming seeds (tough or hard) at rates somewhere
between 10 and 50%.
Analysis of complexity for the other groups largely
yields interpretations similar to those based on the
5CERC analysis. Thus, complexity differed between Papio
and Theropithecus as expected with much lower complexity for Theropithecus. P. ursinus could not be distinguished from the other two species and no microwear signature could be linked to USO consumption. Similar comAmerican Journal of Physical Anthropology
plexity results were also evident for the 6CEB group. The
generic contrast was particularly notable with a clear
trend from Cebus (most complex microwear and hard
diet) to Ateles (moderately complex microwear/less challenging and more frugivorous diet) to Alouatta (much less
complex microwear and tough folivorous diet).
As expected, M. fascicularis and P. pygmaeus had
more complex microwear surfaces than the three colobines in the 5CAT group. However, it is M. fascicularis
that was distinguished by significantly higher complexity and not P. pygmaeus. Based on this pattern, it is
hard to argue that these P. pygmaeus ate extremely
hard or tough foods in the time before death. Instead,
microwear texture complexity for P. pygmaeus seems to
indicate an ape that seeks out ripe fleshy fruit as
opposed to hard objects. Of course, since both M. fascicularis and P. pygmaeus have variable diets, another
option could be that the microwear analysis was based
on M. fascicularis that consumed hard objects in the
time immediately before death and P. pygmaeus that
did not.
As for the African apes, significant differences in complexity between Pan and Gorilla and indeed between the
two Gorilla species were expected (with G. beringei predicted to have the lowest complexity). This was not the
case, suggesting that the reported overlap observed for
African ape diets in terms of fruit and leaves (ConklinBrittain et al., 2000) may be large enough that microwear differences for complexity are not observable (but
see below for possibly utility of complexity as an adjunct
to anisotropy in the African apes).
569
DENTAL MICROWEAR TEXTURE AND ANTHROPOID DIETS
TABLE 8. Percent specimens with complex dental microwear texture
Asymptotic 95% confidence limits
Taxon
5CERC
Colobus guereza
Colobus polykomos
Procolobus badius
Lophocebus albigena
Cercocebus atys
3PAP
Papio cynocephalus
Papio ursinus
Theropithecus gelada
3HOM
Pan troglodytes
Gorilla gorilla
Gorilla beringei
6CEB
Alouatta palliata
Ateles belzebuth
Ateles hybridus
Cebus xanthosternos
Cebus nigritus robustus
Cebus nigritus x libidinosus
5CAT
Semnopithecus entellus
Trachypithecus cristatus
Presbytis rubicunda
Macaca fascicularis
Pongo pygmaeus
a
N
% Complexa
Lower limit (%)
Upper limit (%)
23
29
16
23
55
4.3
31.0
31.3
39.1
54.5
0.0
14.2
8.5
19.2
41.4
12.7
47.9
54.0
59.1
67.7
27
12
12
48.1
50.0
0.0
29.3
21.7
–
67.0
78.3
–
17
15
16
52.9
40.0
18.8
29.2
15.2
0.0
76.7
64.8
37.9
31
10
8
9
14
7
0.0
40.0
37.5
33.3
71.4
100.0
–
9.6
4.0
2.5
47.8
–
–
70.4
71.0
64.1
95.1
–
8
12
12
20
15
0.0
8.3
8.3
40.0
20.0
–
0.0
0.0
18.5
0.0
–
24.0
24.0
61.5
40.2
Complex specimens are defined here as all specimens with Asfc exceeding a complexity cutpoint of 2.00.
Anisotropy
As with complexity, our results for anisotropy were
mostly in accord with our predictions. This is seen most
clearly by high anisotropy values for C. guereza and low
anisotropy values for C. atys. However, there is a subtle
and interesting difference between predictions and findings. We predicted that folivorous primates would tend
to have more anisotropic microwear. What actually
seems to be the case is that the most nonfolivorous species in the group tend to have the lowest probability of
having anisotropic microwear. The equation seems to be
more one of no tough leaves in the diet means no anisotropy as opposed to tough leaves means anisotropy.
The key to understanding these results might be to
model resultant wear patterns as the result of processes
of both wear addition and subtraction at variable rates.
Thus, tough foods may lead to the slow addition and subtraction of parallel striae and generate anisotropy. Hard
foods may lead to the rapid addition and subtraction of
features, and the creation of large deep features, summing to a complex microwear texture. If both hard and
tough foods are consumed in some proportion, then the
resultant wear pattern will potentially depend as much
on the differential rates of wear subtraction and addition
as the frequency of consumption of different foods. In
this case, significant differences between C. atys and the
other forest-dwelling cercopithecids may be driven by either more complete subtraction of microwear striae due
to more rapid and complete microwear turnover from
hard foods (Teaford and Oyen, 1989b) or by minimal
addition of microwear striae from less commonly consumed tough foods or by both. Perhaps only in the case
of C. guereza were few enough harder foods (presumably
seeds) consumed for subtraction of a tough food anisot-
ropy signal to become a minimal contributor to resultant
dental microwear texture.
It is worth exploring the transformation of anisotropy
scores to a nominal scale where textures are either anisotropic or not. Here, we propose an anisotropy cutpoint
of 0.0050 analogous to that already discussed for complexity. The 0.0050 cutpoint falls conveniently between
the median anisotropy values of browsers and grazers
from as diverse groups as ruminants and macropodids
(Ungar et al., 2007; Prideaux et al., 2009). Results and
95% confidence intervals arising from the application of
this cutpoint are shown in Table 9. Considered in this
fashion, 14.9–16.7% of C. atys specimens would have anisotropic microwear while 19.2–59.1% of C. guereza specimens would have anisotropic microwear. If indeed the C.
guereza sample studied here consumed 80% or more
tough leaves (as suggested in the literature), our results
would imply that even infrequent consumption of some
hard foods may act to obliterate or complicate anisotropic textures.
A more meaningful application enabled by nominalizing both complexity and anisotropy in this fashion can
be seen in Figure 6. Here, the proportions of anisotropic
and complex microwear signatures are plotted against
each other. The result is a useful map of microwear texture signals for our entire database as well as other fossil and extant species taken from the literature. Two
properties of this plot argue for its heuristic value: 1) a
robust negative linear trend and 2) species with different
diets occupy distinct spaces on the plot.
This latter point is especially evident when it comes to
the African apes. As noted above, there were no significant differences in complexity in the comparisons among
the African apes. Neither generic nor species level analyses were significant. The only significant differences
American Journal of Physical Anthropology
570
R.S. SCOTT ET AL.
TABLE 9. Percent specimens with anisotropic dental microwear texture
Asymptotic 95% confidence limits
Taxon
5CERC
Colobus guereza
Colobus polykomos
Procolobus badius
Lophocebus albigena
Cercocebus atys
3PAP
Papio cynocephalus
Papio ursinus
Theropithecus gelada
3HOM
Pan troglodytes
Gorilla gorilla
Gorilla beringei
6CEB
Alouatta palliata
Ateles belzebuth
Ateles hybridus
Cebus xanthosternos
Cebus nigritus robustus
Cebus nigritus x libidinosus
5CAT
Semnopithecus entellus
Trachypithecus cristatus
Presbytis rubicunda
Macaca fascicularis
Pongo pygmaeus
a
N
% Anisotropica
Lower limit (%)
Upper limit (%)
23
29
16
23
55
39.1
37.9
50.0
34.8
9.1
19.2
20.3
25.5
15.3
1.5
59.1
55.6
74.5
54.2
16.7
27
12
12
11.1
8.3
75.0
0.0
0.0
50.5
23.0
24.0
99.5
17
15
16
5.9
20.0
31.3
0.0
0.0
8.5
17.1
40.2
54.0
31
10
8
9
14
7
64.5
30.0
12.5
55.6
21.4
0.0
47.7
1.6
0.0
23.1
0.0
–
81.4
58.4
35.4
88.0
42.9
–
8
12
12
20
15
37.5
41.7
41.7
25.0
26.7
4.0
13.8
13.8
6.0
4.3
71.0
69.6
69.6
44.0
49.0
Anisotropic specimens are defined here as all specimens with epLsar1.8lm exceeding an anisotropy cutpoint of 0.0050.
found were in the generic level analysis between Pan
and Gorilla for anisotropy and heterogeneity. Although
tests of anisotropy and heterogeneity approach significance in this species level comparison (P 5 0.102 and
0.084 respectively) the direction of any differences
between G. beringei and G. gorilla was opposite what is
expected given diets reported in the literature (especially given that the specimens studied here were from
the high Virungas). For example, G. beringei had lower
mean values for anisotropy compared with G. gorilla.
However, if both complexity and anisotropy are nominalized for the African apes, the resulting plot (see Fig.
6c) is very consistent with expectations based on reports
of diets of these three species: the more folivorous G.
beringei has more anisotropic and fewer complex specimens compared to the other two species. P. troglodytes
fills the other extreme (more complex, less anisotropic)
and G. gorilla displays the expected intermediate
signal.
The 3PAP, 6CEB, and 5CAT analyses all produced
results consistent with our interpretations of an anisotropy microwear signal as the result of tough food consumption with a low frequency of hard foods. The grasseater Theropithecus is distinguished by high anisotropy
(significantly different than Papio) as is folivorous A.
palliata, and the folivorous Asian colobines. These distinctions can all be seen in Figure 6.
One notable observation concerns C. xanthosternos.
Although this species could not be distinguished significantly from the other ‘‘apelloid’’ Cebus, as can be seen in
Figure 6, many of the specimens in this sample recorded
high anisotropy. This particular situation deserves more
investigation and is interesting in light of recent reports of
tool use in the wild by C. xanthosternos (Canale et al., 2009).
American Journal of Physical Anthropology
Textural fill volume
There is no evidence that primate molar microwear
textural fill volume is as useful as complexity in distinguishing between species with different diets. Thus, in
general, textural fill volume differed less often between
pairs of species than complexity. For instance, the
3HOM and 3PAP data sets had no significant results for
textural fill volume.
When it comes to the 5CERC group, significant differences in textural fill volume tend to coincide with contrasts already evident for complexity. Large textural fill
volumes tend to be associated with high complexity.
Potentially, the most interesting divergence between
the textural fill volume and complexity results is that
L. albigena had a mean textural fill volume that was as
high, if not higher than that for C. atys. It is possible
that the high complexity observed for L. albigena
results from larger features and that observed for C.
atys arises from wear features at a greater variety of
scales.
The textural fill volume results for the 5CAT and
6CEB analyses also paralleled those for complexity.
Alouatta stood out with low textural fill volume for the
6CEB comparisons and M. fascicularis stood out with
high textural fill volume for in the 5CAT analysis. These
results serve to confirm what the results for complexity
already show.
In sum, our results seem to be consistent with two
ideas. First, the more microwear there is, the greater
the textural fill volume. In particular, more abrasives,
and especially larger ones should excavate more surface—creating deeper and/or larger features. A second
idea might be characterized as a ‘‘square peg round hole’’
situation or rather more like square peg versus skinny
DENTAL MICROWEAR TEXTURE AND ANTHROPOID DIETS
571
Fig. 6. Bubble plots of percent of specimens with complex microwear textures versus percent of specimens with anisotropic
microwear textures for studied species. Bubble widths are proportional to sample sizes. Species are plotted according to analysis
group: (a) 5CERC group, (b) 3PAP group, (c) 3HOM group, (d) 6CEB group, and (e) 5CAT group. Fossil hominins (Scott et al.,
2005; Ungar et al., 2008; Ungar et al., 2010), extant bovids (Ungar et al., 2007), and extant carnivores (Schubert et al., 2010) are
plotted with selected primates (f).
long deep scratch. Since the filling volumes are square
on one side, they will fit best into pits as opposed to
scratches. Larger pits likely allow more filling elements
to fit into them more easily than into scratches (especially narrower ones).
The data presented here suggest that textural fill volume may be best used as a supplement to complexity for
primate molar microwear. However, the correlation
between complexity and textural fill volume reported in
Scott et al. (2006) was not extremely high. Thus, it does
appear that complexity and textural fill volume are not
redundant measures. Future experimental work could
help illuminate the differences between these two measures of microwear texture.
Heterogeneity
Heterogeneity may reflect size and variability of wearinducing particles (Scott et al., 2006). Potentially more
heterogeneous microwear could result from larger wearinducing particles as large features (especially pits) are
added in a more random fashion. Alternatively, scratches
(especially longer ones) may affect more homogeneous
microwear in as much as they affect multiple subregions
of the same facets. These ideas seem supported by
results for the 5CERC group. First, L. albigena evinces
high heterogeneity and high textural fill volume consistent with the notion of some large pits introducing
greater heterogeneity. Second, low heterogeneity in
American Journal of Physical Anthropology
572
R.S. SCOTT ET AL.
C. guereza is consistent with long scratches affecting
multiple subregions and yielding a more homogeneously
worn surface.
Another possible relationship between the heterogeneity variable and diet is simply that heterogeneous microwear is the result of a more heterogeneous or varying
diet. This idea receives some support from the analysis
of the 5CERC group where C. guereza has the least heterogeneous microwear as well as probably the most consistent and least variable diet (i.e., more frequent folivory). However, it is not really possible with this dataset
to determine if low C. guereza heterogeneity is the
intrinsic result of wear-inducing particle size, a scratch
length effect, less dietary variability, or a combination of
all of these.
Theropithecus gelada has arguably the most consistent
and homogeneous diet of all the species in our sample.
Indeed, it represents something of an exception among
primates that as a group tend toward dietary catholicism. Thus, if microwear heterogeneity responds to dietary variability, it is expected that T. gelada should have
among the lowest scores for heterogeneity. This is, in
fact, the case: T. gelada has the lowest heterogeneity
with a median of 0.585.
Minimal T.gelada heterogeneity scores can be interpreted as evidence for a direct heterogeneity to dietary
variability correspondence. However, this interpretation
is made problematic because grass consumption by T.
gelada means that the scratch effect and particle size
explanations for heterogeneity also can be applied. As
shown in Figure 1, species of Papio tend toward quite
variable diets. It might be expected that the two species
of Papio in this study would have quite high scores for
microwear heterogeneity, if it is indeed greater dietary
variability leading to heterogeneous microwear. In this
case the results are mixed, P. cynocephalus does have
high microwear heterogeneity (median HAsfc 5 0.923),
but P. ursinus has lower heterogeneity (median HAsfc 5
0.689). Moreover, the difference between P. ursinus and
T. gelada in heterogeneity was significant only by Fisher’s LSD. Thus, the case that T. gelada has very homogeneous microwear simply due to low dietary variability
must be viewed with some caution. In particular, the
effects of small wear-inducing particles and the predominance of longer scratches affecting multiple wear subregions could also explain low heterogeneity in T. gelada.
Thus, heterogeneity is possibly influenced by diet type
and/or dietary breadth.
Heterogeneity differed significantly between Pan and
Gorilla, with Pan having higher heterogeneity. Here
again the dietary breadth, scratch length effect, and particle size effects are all possible explanations for this difference.
One piece of evidence potentially running counter to
the scratch length explanation for low heterogeneity can
be found in the 6CEB analysis. In this case, A. hybridus
had lower heterogeneity than A. palliata. If predominance of scratches leads to low heterogeneity and, if like
other Ateles, this species or population was largely frugivorous, this result would be unexpected. However,
given the paucity of real behavioral data on diet in A.
hybridus, perhaps this group was simply more folivorous. Again, more behavioral data and microwear data
are needed to sort through these alternatives.
It would be a mistake to overstate these results. The
interpretation suggested above should be viewed as a
best case and some caveats apply. First, the cutpoint of
American Journal of Physical Anthropology
complexity greater than two to identify specimens with
complex microwear is somewhat arbitrary. However, a
complexity cutpoint of two is not without support from
other diverse groups. For example, Ungar et al. (2007)
compared some extant grazing and bovid species. The
grazing bovid with the highest mean complexity was
Oryx gazella at 1.99. The browsing bovid with the lowest
mean complexity was Sylvicapra grimmia at 2.17. Similarly, Prideaux et al. (2009) found mean complexities of
1.117 for the grazing kangaroo Macropus giganteus and
6.118 for the browser Wallabia bicolor. Thus, if an arbitrary cutoff between ‘‘complex’’ and ‘‘not complex’’ microwear is selected—two is at least reasonable.
A second caveat follows from the observation that
microwear textures are quite variable. This is unsurprising given that primate diets are, in fact, variable. It is
the unusual case where primate diets are more monotonous. Moreover, variability may be increased by the phenomenon of the ‘‘Last Supper’’ effect whereby perhaps as
little as 1 week or less of dietary history might be
reflected in microwear. Thus, larger sample sizes are
clearly preferred. The colobine species here are represented by samples of 16, 23, and 29. The broad binomial
95% confidence intervals discussed above for these three
colobines show that even with relatively large samples,
uncertainty persists. We suggest that larger samples are
critical for us to be confident that we are sampling variation inherent in primate microwear samples. It is also
important to recognize that extreme cases, such as virtually no individuals with high complexity, might still be
recognized at lower sample sizes.
A third caveat relates to the issue of the ‘‘Last Supper’’
phenomenon and the likelihood that different kinds of
microwear texture have differing longevity. Complexity
and textural fill volume are both influenced by the presence of deep features and deep features may persist for
a longer period of time. Findings of both more rapid
turnover of microwear and more rapid tooth wear in the
case of hard diets (Teaford and Oyen, 1989a,b) support
the argument that a noncomplex microwear surface
could be altered very rapidly by minimal time feeding on
hard foods, and that these complex microwear signatures
could then linger as feeding on softer foods resumes
(assuming that abrasion, rather than other wear processes like erosion, is the main source of wear being documented). Thus, all things being equal, a complex microwear surface may well have a longer lifespan than a
noncomplex surface. A single period of predation on hard
seeds or acidic fruit may then leave persistent, complex
microwear and an overestimate of hard food consumption could then be a risk. A failure to find significant differences in complexity between L. albigena and C. atys
could be explained by this phenomenon. Alternatively,
limited control over museum sample provenience related
to availability of specific resources would certainly be a
possibility. Although hard foods may be less frequent in
L. albigena diets, they may reach a high enough threshold that new microwear complexity is often generated
before old microwear complexity is lost. Controlled study
to estimate the lifespan of complex versus noncomplex
microwear, and more control concerning the diets of individuals included in microwear studies will be critical to
improving interpretations.
A fourth caveat noted in the discussion of methodology
should be reemphasized. The specimens analyzed here in
some cases represent mixed samples from phenologically
and ecogeographically varied settings. As a result,
DENTAL MICROWEAR TEXTURE AND ANTHROPOID DIETS
dietary information may not be for the same populations
as those considered here and this can complicate interpretations. The ideal study case would involve measurement of microwear textures where field or laboratory observation of foods eaten, tests of those foods’ properties,
and realized microwear textures could be compared.
Here we are only able to offer taxonomy as a general
proxy for foods consumed and its material properties.
The ideal test could well provide resolution to some of
the issues noted above. Does hard-seed consumption create microwear complexity? How many seeds need to be
consumed? How long might complex microwear textures
last once seed consumption ceases? How do other wear
processes, like erosion, affect microwear textures and
longevity? Answering these questions would clearly be
helpful. For instance, the value of a complexity cutpoint
of two could be evaluated directly.
Synthesis
It is clear that microwear textures vary with diet. It is
also clear that observed textures within-species are quite
variable. We are certain that this reflects variable diets
of primates in general. A practical result is that large
samples (possibly 10 or more) become of particular
import when it comes to drawing conclusions about fossil
species. The truism that ‘‘more fossils are needed’’ then
applies to an even greater degree. This is a cold comfort
to the paleoanthropologist curious about the dietary evolution of our close fossil relatives.
However, it is at least true that, in cases where diets
were less variable, smaller samples may at least give us
new insights. A case in point may be that of P. boisei.
Until recently with the publication of Ungar et al.’s
(2008a) analysis of seven P. boisei specimens, the widely
held presumption would have been that P. boisei was
likely a consumer of hard foods at least as a fallback
resource. Remarkably, none of the seven specimens analyzed revealed microwear complexity that exceeded our
proposed complexity cutpoint of two. Little evidence
would exist then for the consumption of hard foods. This
conclusion is further strengthened by the addition of two
more P. boisei specimens from Olduvai to this sample
(Ungar et al., 2010a; Ungar et al., in press). Both specimens have low complexity. Thus, confidence is relatively
high in this case that hard foods were unlikely to have
constituted a major part of P. boisei’s diet. The data leading to this conclusion can be visualized best in Figure 6
(data from Ungar et al., 2008a), where P. boisei plot far
from any extant primate consuming hard foods. The contrast with P. robustus is considerable.
As noted from the outset, a limitation of museumbased studies is that they do not come with data on
foods eaten by specimens prior to death. Still, much of
the variation in microwear textures can be explained by
species designation (1—Wilks’ k 5 0.70 in the species
level analysis), and this offers good support for links
between diet and microwear texture variables. Future
study in either a field setting or experimental lab setting
where foods eaten are positively known prior to microwear sampling is a necessary next step and will offer a
better understanding of the diet-microwear texture linkage. A recent contribution by Merceron et al. (2010) provides positive results (albeit on small samples), where
microwear texture variables are linked with seasonal
data and gut contents in roe deer. Studies such as these
lead the way for future work.
573
The presentation of microwear texture data in Figure
6 represents a synthesis of much of the work published
on dental microwear textures across mammals, and
allows a general level of confidence to be expressed about
different species based on the size of the available sample and the relative frequency of complex and anisotropic
microwear. The two microwear texture variables that
seem to indicate diet the best are used and the plot is
clearly heuristic—separating browsing and grazing
ruminants, browsing kangaroos from grazing kangaroos,
primates eating hard and tough foods, and even cheetahs from hyenas.
Figure 6 can also be interpreted with the help of the
causal model described in the Introduction. Accordingly,
species eating foods requiring crushing should plot in
the lower right quadrant (complex and isotropic). Species
that shear predominantly tough foods should plot in the
upper left quadrant. Species that mainly grind or mill
tough foods would plot in the lower left quadrant. These
predictions are borne out in Figure 6.
Of course, varying cutpoints for anisotropy and complexity could be more useful for taxa as divergent as say
carnivores, primates, and bovids. This might be expected
if dental morphology and/or masticatory mechanics have
strong influences on microwear texture. Divergent
groups seem at least broadly comparable in Figure 6.
However, controlled feeding of divergent taxa and subsequent evaluation of microwear textures could be used to
elucidate any sort of phase shift in complexity and anisotropy cutpoints.
CONCLUSIONS
The large comparative database of anthropoid dental
microwear textures based on high-resolution threedimensional renderings presented here confirms that
dental microwear textures vary significantly with diet. It
is also clear that just as primate diets are complicated
and variable so too is dental microwear. Dental microwear complexity and anisotropy appear to be particularly useful, but dental microwear heterogeneity and textural fill volume also vary with diet. Although large sample sizes are important, dental microwear textures can
provide very powerful insights into the diets of fossil primates. Adopting a complexity and anisotropy cutpoint
allowing for nominalization of these data yields the most
useful (for the purpose of dietary inference) visualization
of dental microwear variability across extant and extinct
species to date.
LITERATURE CITED
Aldana Saavedra JP. 2009. Feeding ecology and seed dispersal
by Ateles hybridus, Alouatta seniculus and Cebus albifrons in
a fragmented area at San Juan del Carare, Colombia: ecology
of a monkey community in a fragment. Master’s thesis. Uppsala: Swedish Biodiversity Centre.
Altmann SA. 1998. Foraging for survival: yearling baboons in
Africa. Chicago: University of Chicago Press.
Baker G, Jones L, Wardrop I. 1959. Cause of wear in sheeps’
teeth. Nature 184:1583–1584.
Barton R. 1989. Foraging strategies, diet and competition in
olive baboons. Ph.D. Dissertation. University of St. Andrews.
Basabose AK. 2002. Diet composition of chimpanzees inhabiting
the montane forest of Kahuzi, Democratic Republic of Congo.
Am J Primatol 58:1–12.
Bennett E, Davies A. 1994. The ecology of Asian colobines. In:
Davies A, Oates J, editors. Colobine monkeys: their ecology,
American Journal of Physical Anthropology
574
R.S. SCOTT ET AL.
behavior and evolution. Cambridge: Cambridge University
Press. p 129–171.
Bentley-Condit VK. 2009. Food choices and habitat use by
the Tana River yellow baboons (Papio cynocephalus): a
preliminary report on five years of data. Am J Primatol
71:432–436.
Berenstain L. 1986. Responses of long-tailed macaques to
drought and fire in Eastern Borneo: a preliminary report. Biotropica 18:257–262.
Brotoisworo E, Dirgayusa I. 1991. Ranging and feeding behaviour of Presbytis cristatus in the Pangandaran Reserve, West
Java, Indonesia. In: Ehara A, Kimura T, Takenaka O, Iwamoto M, editors. Primatology today. Amsterdam: Elsevier. p
115–118.
Butler P. 1952. The milk molars of Perissodactyla, with remarks
on molar occlusion. Proc Zool Soc Lond 121:777–817.
Canale GR, Guidorizzi CE, Kierulff MCM, Gatto C. 2009. First
record of tool use by wild populations of the yellow-breasted
capuchin monkey (Cebus xanthosternos) and new records for
the bearded capuchin (Cebus libidinosus). Am J Primatol
71:366–372.
Caton JM. 1999. Digestive strategy of the Asian colobine genus
Trachypithecus. Primates 40:311–325.
Chalk J, Wright BW, Lucas PW, Verderane MP, Fragaszy D,
Visalberghi E, Izar P, Ottoni EB. 2008. The mechanical properties of foods processed by Cebus libidinosus at Boa Vista,
Brazil. AAPA Meeting, Columbus, OH, April 7–13.
Chalmers N. 1968. Group composition, ecology and daily activities of free living mangabeys in Uganda. Folia Primatologica
8:247–262.
Chapman C. 1988. Patterns of foraging and range use by three
species of neotropical primates. Primates 29:177–194.
Chivers DJ. 1994. Functional anatomy of the gastrointestinal
tract. In: Davies AG, Oates JF, editors. Colobine monkeys:
their ecology, behaviour, and evolution. Cambridge: Cambridge University Press. p 205–227.
Cipolletta C, Spagnoletti N, Todd A, Robbins M, Cohen H,
Pacyna S. 2007. Termite feeding by western lowland gorillas
(Gorilla gorilla gorilla) at Bai-Hokou, Central African Republic. Int J Primatol 28:457–476.
Conklin-Brittain N, Knott C, Wrangham R. 2000. The feeding
ecology of apes. The apes: challenges for the 21st century.
Brookfield, IL: Chicago Zoological Society. p 167–174.
Conover W, Iman R. 1981. Rank transformations as a bridge
between parametric and nonparametric statistics. Am Stat
35:124–129.
Constantino PJ, Lucas PW, Lee JJW, Lawn BR. 2009. The influence of fallback foods on great ape tooth enamel. Am J Phys
Anthropol 140:653–660.
Cook RJ, Farewell VT. 1996. Multiplicity considerations in the
design and analysis of clinical trials. J R Stat Soc A 159:93–
110.
Copeland SR. 2009. Potential hominin plant foods in northern
Tanzania: semi-arid savannas versus savanna chimpanzee
sites. J Hum Evol 57:365–378.
Corlett RT, Lucas PW. 1990. Alternative seed-handling strategies in primates: seed-spitting by long-tailed macaques
(Macaca fascicularis). Oecologia 82:166–171.
Cristobal-Azkarate J, Arroyo-Rodriguez V. 2007. Diet and activity pattern of howler monkeys (Alouatta palliata) in Los Tuxtlas, Mexico: effects of habitat fragmentation and implications
for conservation. Am J Primatol 69:1013–1029.
Daegling DJ, Grine FE. 1999. Terrestrial foraging and dental
microwear in Papio ursinus. Primates 40:559–572.
Daegling DJ, McGraw WS. 2007. Functional morphology of the
mangabey mandibular corpus: relationship to dental specializations and feeding behavior. Am J Phys Anthropol 134:50–
62.
Daegling DJ, McGraw WS, Ungar PS, Pampush JD, Vick AE,
Bitty EA. 2011. Hard-object feeding in sooty mangabeys (Cercocebus atys) and interpretation of early hominin feeding ecology. PLoS ONE 6(8): e23095. doi:10.1371/journal.pone.0023095.
Daegling DJ, McGraw WS, Vick AE, Rapoff AJ, Bitty A, Paacho
R. 2010. Masticatory effort and dietary hardness in sooty
American Journal of Physical Anthropology
mangabeys (Cercocebus atys) from Tai Forest, Ivory Coast.
Am J Phys Anthropol 50:90.
Dahlberg A, Kinzey W. 1962. Étude microscopique de l’abrasion
et de l’attrition sur la surface des dents. Bull Gr Int Rech Sci
Stomatol 5:242–251.
Danielson DR, Reinhard KJ. 1998. Human dental microwear
caused by calcium oxalate phytoliths in prehistoric diet of the
lower Pecos region, Texas. Am J Phys Anthropol 107:297–304.
Dasilva GL. 1989. The ecology of the western black and white
colobus (Colobus polykomos Zimmerman 1780) on a riverine
island in south-eastern Sierra Leone. PhD Dissertation, University of Oxford.
Dasilva GL. 1994. Diet of Colobus polykomos on Tiwai Island:
selection of food in relation to its seasonal abundance and
nutritional quality. Int J Primatol 15:655–680.
Davies AG. 1984. An ecological study of the red leaf monkey
(Presbytis rubicunda) in the dipterocarp forest of Northern
Borneo. PhD Dissertation, Cambridge University.
Davies G. 1991. Seed-eating by red leaf monkeys (Presbytis
rubicunda) in dipterocarp forest of Northern Borneo. Int J
Primatol 12:119–144.
Davies A, Bennett E, Waterman P. 1988. Food selection by two
Southeast Asian colobine monkeys (Presbytis rubicunda and
Presbytis melalophos) in relation to plant chemistry. Biol J
Linn Soc 34:33–56.
Davies AG, Oates JF, Dasilva GL. 1999. Patterns of frugivory in
three West African colobine monkeys. Int J Primatol 20:327–
357.
Deblauwe I, Janssens GPJ. 2008. New insights in insect prey
choice by chimpanzees and gorillas in southeast Cameroon:
the role of nutritional value. Am J Phys Anthropol 135:42–55.
Dela JDS. 2007. Seasonal food use strategies of Semnopithecus
vetulus nestor, at Panadura and Piliyandala, Sri Lanka. Int J
Primatol 28:607–626.
Dew JL. 2005. Foraging, food choice, and food processing by
sympatric ripe-fruit specialists: Lagothrix lagotricha poeppigii
and Ateles belzebuth belzebuth. Int J Primatol 26:1107–1135.
Di Fiore A, Link A, Dew JL. 2008. Diets of wild spider monkeys.
In: Campbell CJ, editor. Spider monkeys: behavior, ecology
and evolution of the genus Ateles. Cambridge, UK: Cambridge
University Press. p 81–137.
Dominy NJ, Vogel ER, Yeakel JD, Constantino P, Lucas PW.
2008. Mechanical properties of plant underground storage
organs and implications for dietary models of early hominins.
Evol Biol 35:159–175.
Doran DM, McNeilage A, Greer D, Bocian C, Mehlman P, Shah
N. 2002. Western lowland gorilla diet and resource availability: new evidence, cross-site comparisons, and reflections on
indirect sampling methods. Am J Primatol 58:91–116.
Doran-Sheehy D, Mongo P, Lodwick J, Conklin-Brittain NL.
2009. Male and female western gorilla diet: preferred foods,
use of fallback resources, and implications for ape versus old
world monkey foraging strategies. Am J Phys Anthropol
140:727–738.
Dunbar DC, Badam GL. 1998. Development of posture and locomotion in free-ranging primates. Neurosci Biobehav Rev
22:541–546.
Dunbar DC, Badam GL, Hallgrimsson B, Vieilledent S. 2004.
Stabilization and mobility of the head and trunk in wild monkeys during terrestrial and flat-surface walks and gallops.
J Exp Biol 207:1027–1042.
Dunbar RIM. 1988. Primate social systems. Ithaca, NY: Cornell
University Press.
Dunbar RIM, Dunbar EP. 1974. Ecological relations and niche
separation between sympatric terrestrial primates in Ethiopia. Folia Primatol 21:36–60.
Ehiagbonare J, Onyibe H. 2008. Regeneration studies on Pentaclethra macrophylla Bth. Sci Res Essay 3:531–536.
El-Zaatari S. 2010. Occlusal microwear texture analysis and the
diets of historical/prehistoric hunter-gatherers. Int J Osteoarchaeol 20:67–87.
Fashing PJ. 2001. Feeding ecology of guerezas in the Kakamega
Forest, Kenya: the importance of Moraceae fruit in their diet.
Int J Primatol 22:579–609.
DENTAL MICROWEAR TEXTURE AND ANTHROPOID DIETS
Felton AM, Felton A, Wood JT, Lindenmayer DB. 2008. Diet
and feeding ecology of Ateles chamek in a Bolivian semihumid
forest: the importance of Ficus as a staple food resource. Int J
Primatol 29:379–403.
Fossey D, Harcourt AH. 1977. Feeding ecology of free-ranging
mountain gorillas (Gorilla gorilla beringei). In: Clutton-Brock
TH, editor. Primate ecology. New York: Academic Press.
p 415–447.
Fox EA, van Schaik CP, Sitompul A, Wright DN. 2004. Intraand interpopulational differences in orangutan (Pongo pygmaeus) activity and diet: implications for the invention of tool
use. Am J Phys Anthropol 125:162–174.
Fragaszy D, Izar P, Visalberghi E, Ottoni EB, De Oliveira MG.
2004. Wild capuchin monkeys (Cebus libidinosus) use anvils
and stone pounding tools. Am J Primatol 64:359–366.
Ganas J, Robbins MM, Nkurunungi JB, Kaplin BA, McNeilage
A. 2004. Dietary variability of mountain gorillas in Bwindi
Impenetrable National Park, Uganda. Int J Primatol 25:
1043–1072.
Godfrey LR, Semprebon GM, Jungers WL, Sutherland MR,
Simons EL, Solounias N. 2004. Dental use wear in extinct
lemurs: evidence of diet and niche differentiation. J Hum
Evol 47:145–169.
Gonzalez-Zamora A, Arroyo-Rodriguez V, Chaves OM, SanchezLopez S, Stoner KE, Riba-Hernandez P. 2009. Diet of spider
monkeys (Ateles geoffroyi) in Mesoamerica: current knowledge
and future directions. Am J Primatol 71:8–20.
Goodall J. 1986. The chimpanzees of Gombe: patterns of behaviour. Cambridge, MA: Harvard University Press.
Gordon KD. 1984. Orientation of occlusal contacts in the chimpanzee, Pan troglodytes verus, deduced from scanning electron-microscopic analysis of dental microwear patterns. Arch
Oral Biol 29:783–787.
Gordon KD. 1988. A review of methodology and quantification
in dental microwear analysis. Scan Microsc 2:1139–1147.
Green JL. 2009. Dental microwear in the orthodentine of the
Xenarthra (Mammalia) and its use in reconstructing the
palaeodiet of extinct taxa: the case study of Nothrotheriops
shastensis (Xenarthra, Tardigrada, Nothrotheriidae). Zool J
Linn Soc 156:201–222.
Green JL, Semprebon GM, Solounias N. 2005. Reconstructing
the palaeodiet of Florida Mammut americanum via low-magnification stereomicroscopy. Palaeogeogr Palaeoclimatol Palaeoecol 223:34–48.
Grine F. 1977. Analysis of early hominid deciduous molar wear
by scanning electron microscopy: a preliminary report. Proc
Elect Microsc Soc S Afr 7:157–158.
Grine F. 1981. Trophic differences between ‘gracile’ and ‘robust’
australopithecines: a scanning electron microscope analysis of
occlusal events. S Afr J Sci 77:203–230.
Grine FE. 1986. Dental evidence for dietary differences in Australopithecus and Paranthropus: a quantitative-analysis of
permanent molar microwear. J Hum Evol 15:783–822.
Grine FE, Judex S, Daegling DJ, Ozcivici E, Ungar PS, Teaford
MF, Sponheimer M, Scott J, Scott RS, Walker A. 2010. Craniofacial biomechanics and functional and dietary inferences
in hominin paleontology. J Hum Evol 58:293–308.
Grine FE, Sponheimer M, Ungar PS, Lee-Thorp J, Teaford
MF. How dental microwear and stable isotopes inform the
paleoecology of extinct hominins. Am J Phys Anthropol,
in press.
Grine FE, Ungar PS, Teaford MF. 2002. Error rates in dental
microwear quantification using scanning electron microscopy.
Scanning 24:144–153.
Guerrero JD, Link A. 2007. Trabajo de grado para optar al
tı́tulo de Ecóloga. Facultad de Estudios Ambientales y
Rurales. Pontificia Universidad Javeriana. Bogotá, D.C.
Gugel IL, Grupe G, Kunzelmann KH. 2001. Simulation of dental microwear: characteristic traces by opal phytoliths give
clues to ancient human dietary behavior. Am J Phys Anthropol 114:124–138.
Guo SG, Li BG, Watanabe K. 2007. Diet and activity budget of
Rhinopithecus roxellana in the Qinling Mountains, China.
Primates 48:268–276.
575
Ham R. 1994. Behaviour and ecology of the greycheeked mangabeys (Cercocebus albigena) in the Lope Reserve, Gabon. Ph.D.
Dissertation. Stirling, UK: University of Stirling.
Harris TR, Chapman CA. 2007. Variation in diet and ranging of
black and white colobus monkeys in Kibale National Park,
Uganda. Primates 48:208–221.
Hayek LAC, Bernor RL, Solounias N, Steigerwald P. 1991. Preliminary studies of hipparionine horse diet as measured by
tooth microwear. Ann Zool Fennici 28:187–200.
Hladik CM. 1977a. A comparative study of the feeding strategies of two sympatric species of leaf monkeys: Presbytis senex
and Presbytis entellus. In: Clutton-Brock TH, editor. Primate
ecology. London: Academic Press. p 333–353.
Hladik CM. 1977b. Chimpanzees of Gombe and the chimpanzees
of Gabon: some comparative data on the diet. In: CluttonBrock TH, editor. Primate ecology. New York: Academic Press.
p 481–501.
Hock LB, Sasekumar A. 1979. A preliminary study on the feeding biology of mangrove forest primates, Kuala Selangor.
Malay Nat J 33:105–112.
Hohmann G, Potts K, N’Guessan A, Fowler A, Mundry R, Ganzhorn JU, Ortmann S. 2010. Plant foods consumed by Pan:
exploring the variation of nutritional ecology across Africa.
Am J Phys Anthropol 141:476–485.
Humle T, Matsuzawa T. 2004. Oil palm use by adjacent communities of chimpanzees at Bossou and Nimba Mountains,
West Africa. Int J Primatol 25:551–581.
Hunt KD, McGrew WC. 2002. Chimpanzees in the dry habitats
of Assirik, Senegal and Semliki Wildlife Reserve, Uganda. In:
Boesch C, Hohmann G, Marchant LF, editors. Behavioral
diversity in chimpanzees and bonobos. New York: Cambridge
University Press. p 35–51.
Iwamoto T. 1993. The ecology of Theropithecus gelada. In:
Jablonski N, editor. Theropithecus: the rise and fall of a primate
genus. Cambridge: Cambridge University Press. p 441–452.
Janmaat KRL, Byrne RW, Zuberbuhler K. 2006. Evidence for a
spatial memory of fruiting states of rainforest trees in wild
mangabeys. Anim Behav 72:797–807.
Jones C, Sabater-Pi J. 1968. Comparative ecology of Cercocebus
albigena (Gray) and Cercocebus torquatus (Kerr) in Rio Muni,
West Africa. Folia Primatol 9:99–113.
Kanamori T, Kuze N, Bernard H, Malim TP, Kohshima S. 2010.
Feeding ecology of Bornean orangutans (Pongo pygmaeus
morio) in Danum Valley, Sabah, Malaysia: a 3-year record
including two mast fruitings. Am J Primatol 72:820–840.
Kay NBK, Davies AG. 1994. Digestive physiology. In: Davies
AG, Oates JF, editors. Colobine monkeys: their ecology, behaviour, and evolution. Cambridge: Cambridge University Press.
p 229–249.
Kay R, Hiiemae K. 1974. Jaw movement and tooth use in recent
and fossil primates. Am J Phys Anthropol 40:227–256.
Kay RF. 1977. The evolution of molar occlusion in Cercopithecidae and early catarrhines. Am J Phys Anthropol 46:327–
352.
King T, Andrews P, Boz B. 1999. Effect of taphonomic processes
on dental microwear. Am J Phys Anthropol 108:359–373.
Knott C. 1998. Changes in orangutan caloric intake, energy balance, and ketones in response to fluctuating fruit availability.
Int J Primatol 19:1061–1079.
Koenig A, Borries C. 2001. Socioecology of Hanuman langurs:
the story of their success. Evol Anthropol 10:122–137.
Kool K. 1986. Ranging and feeding behaviour of the silvered
leaf monkey, Presbytis cristata, at Pangandaran, Jawa Barat,
Indonesia. Primate Rep 14:24.
Koyabu DB, Endo H. 2009. Craniofacial variation and dietary
adaptations of African colobines. J Hum Evol 56:525–536.
Koyabu DB, Endo H. 2010. Craniodental mechanics and diet in
Asian colobines: morphological evidence of mature seed predation and sclerocarpy. Am J Phys Anthropol 142:137–148.
Krueger KL, Scott JR, Kay RF, Ungar PS. 2008. Technical note:
dental microwear textures of ‘‘Phase I’’ and ‘‘Phase II’’ facets.
Am J Phys Anthropol 137:485–490.
Krueger KL, Ungar PS. 2010. Incisor microwear textures of five
bioarcheological groups. Int J Osteoarchaeol 20:549–560.
American Journal of Physical Anthropology
576
R.S. SCOTT ET AL.
Kurland J. 1973. A natural history of kra macaques (Macaca
fascicularis Raffles, 1821) at the Kutai Reserve, Kalimantan
Timur, Indonesia. Primates 14:245–262.
Lambert JE, Chapman CA, Wrangham RW, Conklin-Brittain
NL. 2004. Hardness of cercopithecine foods: implications for
the critical function of enamel thickness in exploiting fallback
foods. Am J Phys Anthropol 125:363–368.
Leighton M. 1993. Modeling dietary selectivity by Bornean
orangutans: evidence for integration of multiple criteria in
fruit selection. Int J Primatol 14:257–313.
Link A, Di Fiore A. 2006. Seed dispersal by spider monkeys and
its importance in the maintenance of Neotropical rain-forest
diversity. J Trop Ecol 22:235–246.
Link A, Morales Jimenez A. 2007. Ecology, social behavior and seed
dispersal patterns of the critically endangered brown spider monkey (Ateles hybridus) at Serrania de Las Quinchas, Colombia.
Fundacion Biodiversa Colombia, http://www.fundacionbiodiversa.
org/pdf/Ateles/EcologyQuinchasReport.pdf.
Lucas PW, Constantino PJ, Chalk J, Ziscovici C, Wright BW, Fragaszy DM, Hill DA, Lee JJW, Chai H, Darvell BW, et al. 2009.
Indentation as a technique to assess the mechanical properties
of fallback foods. Am J Phys Anthropol 140:643–652.
Lucas PW, Corlett RT. 1991. Relationship between the diet of Macaca
fascicularis and forest phenology. Folia Primatol 57:201–215.
Lucas PW, Peters CR, Arrandale SR. 1994. Seed-breaking forces
exerted by orangutans with their teeth in captivity and a new
technique for estimating forces produced in the wild. Am J
Phys Anthropol 94:365–378.
Lucas P, Teaford MF. 1994. The functional morphology of colobine teeth. In: Davies A, Oates J, editors. Colobine monkeys:
their ecology, behaviour and evolution. Cambridge: Cambridge
University Press. p 173–203.
Lucas PW, Teaford MF. 1995. Significance of silica in leaves to
long-tailed macaques (Macaca fascicularis). Folia Primatol
64:30–36.
MacFadden BJ, Solounias N, Cerling TE. 1999. Ancient diets,
ecology, and extinction of 5-million-year-old horses from Florida. Science 283:824–827.
MacKinnon J. 1974. The behavior and ecology of wild orangutans. Anim Behav 22:3–74.
Mainland IL. 1998. Dental microwear and diet in domestic
sheep (Ovis aries) and goats (Capra hircus): distinguishing
grazing and fodder-fed ovicaprids using a quantitative analytical approach. J Archaeol Sci 25:1259–1271.
Mainland IL. 2003. Dental microwear in grazing and browsing
Gotland sheep (Ovis aries) and its implications for dietary
reconstruction. J Archaeol Sci 30:1513–1527.
Maisels F, Gauthierhion A, Gautier JP. 1994. Diets of two sympatric colobines in Zaire – more evidence on seed-eating in
forests on poor soils. Int J Primatol 15:681–701.
Marsh C. 1981. Diet choice among Red Colobus (Colobus badius
rufomitratus) on the Tana River, Kenya. Folia Primatologica
35:147–177.
Masi S. 2008. Seasonal influence on foraging strategies, activity
and energy budgets of western lowland gorillas (Gorilla gorilla gorilla) in Bai-Hokou, Central African Republic. Rome:
University of Rome ‘‘La Sapienza.’’
McGraw WS, Daegling DJ, Vick AL, Bitty A, Paacho R.
2010.
Diet and ingestive behaviors of a hard object feeder: feeding
and foraging of sooty mangabeys (Cercocebus atys) in Tai Forest, Ivory Coast. Am J Phys Anthropol (Suppl 50):167.
McGraw WS, Vick AE, Daegling DJ. 2011. Sex and age differences in the diet and ingestive behaviors of sooty mangabeys
(Cercocebus atys) in the Tai Forest, Ivory Coast. Am J Phys
Anthropol 144:140–153.
McGraw WS, Zuberbuhler K. 2008. Socioecology, predation, and
cognition in a community of West African monkeys. Evol
Anthropol 17:254–266.
McGrew WC. 1992. Chimpanzee material culture: implications
for human evolution. Cambridge; New York: Cambridge University Press.
McGrew WC, Baldwin PJ, Tutin CEG. 1981. Chimpanzees in a
hot, dry and open habitat: Mt. Assirik, Senegal, West Africa.
J Hum Evol 10:227–244.
American Journal of Physical Anthropology
McGrew WC, Baldwin PJ, Tutin CEG. 1988. Diet of wild chimpanzees (Pan troglodytes verus) at Mt. Assirik, Senegal. I.
Composition. Am J Primatol 16:213–226.
Merceron G, Blondel C, De Bonis L, Koufos GD, Viriot L. 2005a.
A new method of dental microwear analysis: application to
extant primates and Ouranopithecus macedoniensis (Late
Miocene of Greece). Palaios 20:551–561.
Merceron G, de Bonis L, Viriot L, Blondel C. 2005b. Dental
microwear of the late Miocene bovids of northern Greece: Vallesian/Turolian environmental changes and disappearance of
Ouranopithecus macedoniensis? Bull De La Soc Geol De
France 176:475–484.
Merceron G, Escarguel G, Angibault JM, Verheyden-Tixier H.
2010. Can dental microwear textures record inter-individual
dietary variations? PLoS One 5:9.
Merceron G, Scott J, Scott RS, Geraads D, Spassov N, Ungar
PS. 2009. Folivory or fruit/seed predation for Mesopithecus,
an earliest colobine from the late Miocene of Eurasia? J Hum
Evol 57:732–738.
Merceron G, Taylor S, Scott R, Chaimanee Y, Jaeger JJ. 2006.
Dietary characterization of the hominoid Khoratpithecus (Miocene of Thailand): evidence from dental topographic and microwear texture analyses. Naturwissenschaften 93:329–333.
Merceron G, Viriot L, Blondel C. 2004. Tooth microwear pattern
in roe deer (Capreolus capreolus L.) from Chize (Western
France) and relation to food composition. Small Ruminant
Res 53:125–132.
Mihlbachler M, Beatty B, Caldera-Siu A, Chan D, Lee R. 2010.
Exploring the influence of observer bias in dental microwear
analysis. Soc Vertebr Paleontol 70th Anniversary Meeting
Program and Abstracts, Pittsburgh.
Mills J. 1955. Ideal dental occlusion in primates. Dent Pract
6:47–51.
Molnar S, McKee J, Molnar I, Przybeck T. 1983. Tooth wear
rates among contemporary Australian Aborigines. J Dent Res
62:562–565.
Moore J. 1992. ‘‘Savanna’’ chimpanzees. In: Nishida T, McGrew
WC, Marler P, Pickford M, de Waal FBM, editors. Topics in
primatology, Vol. 1: Human origins. Tokyo: University of
Tokyo Press. p 99–118.
Moore J. 1994. Plants of the Tongwe East Forest Reserve
(Ugalla), Tanzania. Tropics 3:333–340.
Morgan BJ. 2009. Sacoglottis gabonensis: a keystone fruit for
forest elephants in the Reserve de Faune du Petit Loango,
Gabon. Afr J Ecol 47:154–163.
Morgan D, Sanz C. 2006. Chimpanzee feeding ecology and comparisons with sympatric gorillas in the Goulaugo Triangle,
Republic of Congo. In: Hohmann G, Robbins MM, Boesch C,
editors. Feeding ecology in apes and other primates; ecological, physiological and behavioural aspects. Cambridge: Cambridge University Press. p 97–122.
Nelson S, Badgley C, Zakem E. 2005. Microwear in modern squirrels in relation to diet. Palaeontol Electr 8;14A:15p, http://
palaeo-electronica.org/paleo/2005_1/nelson14/issue1_05.htm.
Newton P. 1992. Feeding and ranging patterns of forest hanuman langurs (Presbytis entellus). Int J Primatol 13:245–285.
Newton-Fisher NE. 1999. The diet of chimpanzees in the
Budongo Forest Reserve, Uganda. Afr J Ecol 37:344–354.
Nishida T, Uehara S. 1983. Natural diet of chimpanzees (Pan
troglodytes schweinfurthii): long-term record from the Mahale
Mountains, Tanzania. Afr Study Monogr 3:109–130.
Nishihara T. 1995. Feeding ecology of western lowland gorillas
in the Nouabalé-Ndoki National Park, northern Congo. Primates 36:151–168.
Noble V, Teaford MF. 1995. Dental microwear in Caucasian
American Homo sapiens: preliminary results. Am J Phys
Anthropol (Suppl 20):162.
Norconk MA, Wright BW, Conklin-Brittain NL, Vinyard CJ.
2009. Mechanical and nutritional properties of food as factors
in Platyrrhine dietary adaptations. In: Garber PA, Estrada A,
Bicca-Marques JC, Heymann EW, Strier KB, editors. South
American primates: comparative perspectives in the study of
behavior, ecology, and conservation. New York: Springer.
p 279–319.
DENTAL MICROWEAR TEXTURE AND ANTHROPOID DIETS
Norton GW, Rhine RJ, Wynn GW, Wynn RD. 1987. Baboon diet:
a five-year study of stability and variability in the plant feeding and habitat of the yellow baboons (Papio cynocephalus) of
Mikumi National Park, Tanzania. Folia Primatologica 48:78–
120.
Nystrom P, Phillips-Conroy JE, Jolly CJ. 2004. Dental microwear in anubis and hybrid baboons (Papio hamadryas, sensu
lato) living in Awash National Park, Ethiopia. Am J Phys
Anthropol 125:279–291.
Oppenheimer J. 1978. Aspects of the diet of the Hanuman
langur. In: Chivers D, Herbert J, editors. Recent advances
in primatology, Vol. 1: Behaviour. London: Academic Press.
p 337–342.
Perry GH, Dominy NJ, Claw KG, Lee AS, Fiegler H, Redon R,
Werner J, Villanea FA, Mountain JL, Misra R, et al. 2007.
Diet and the evolution of human amylase gene copy number
variation. Nat Genet 39:1256–1260.
Poirier F, Smith E. 1974. The crab-eating macaques (Macaca
fascicularis) of Angaur Island, Palau, Micronesia. Folia Primatol 22:258–306.
Poulsen JR, Clark CJ, Smith TB. 2001. Seasonal variation in
the feeding ecology of the grey-cheeked mangabey (Lophocebus albigena) in Cameroon. Am J Phys Anthropol 54:91–
105.
Poulsen JR, Clark CJ, Connor EF, Smith TB. 2002. Differential
resource use by primates and hornbills: Implications for seed
dispersal. Ecology 83:228–240.
Prideaux GJ, Ayliffe LK, DeSantis LRG, Schubert BW, Murray
PF, Gagan MK, Cerling TE. 2009. Extinction implications of a
chenopod browse diet for a giant Pleistocene kangaroo. Proc
Natl Acad Sci USA 106:11646–11650.
Pruetz JD. 2006. Feeding ecology of savanna chimpanzees (Pan
troglodytes verus) at Fongoli, Senegal. In: Hohmann G, Robbins MM, Boesch C, editors. Feeding ecology in apes and
other primates: ecological, physiological and behavioural
aspects. Cambridge: Cambridge University Press. p 326–364.
Rafferty KL, Teaford MF, Jungers WL. 2002. Molar microwear
of subfossil lemurs: improving the resolution of dietary inferences. J Hum Evol 43:645–657.
Raguet-Schofield ML. 2010. The ontogeny of feeding behavior of
Nicaraguan mantled howler monkeys (Alouatta palliata). Ph.D.
dissertation, University of Illinois at Urbana-Champaign.
Remis MJ. 1997. Western lowland gorillas (Gorilla gorilla gorilla) as seasonal frugivores: use of variable resources. Am J
Primatol 43:87–109.
Rensberger J. 1978. Scanning electron microscopy of wear and
occlusal events in some small herbivores. In: Butler P, Joysey
K, editors. Development, function, and evolution of teeth.
New York: Academic Press. p 415–438.
Rivals F, Schulz E, Kaiser TM. 2009. Late and middle Pleistocene ungulates dietary diversity in Western Europe indicate
variations of Neanderthal paleoenvironments through time
and space. Quat Sci Rev 28:3388–3400.
Rodman P. 1977. Feeding behavior of orangutans in the Kutai
Reserve, East Kalimantan. In: Clutton-Brock T, editor. Primate ecology. London: Academic Press. p 383–413.
Rodman P. 1978. Diets, densities and distributions of Bornean
primates. In: Montgomery G, editor. The ecology of arboreal
folivores. Washington, DC: Smithsonian Institution Press. p
465–478.
Rogers ME, Abernethy K, Bermejo M, Cipolletta C, Doran D,
McFarland K, Nishihara T, Remis M, Tutin CEG. 2004. Western
gorilla diet: a synthesis from six sites. Am J Primatol 64:173–192.
Rothman JM, Dierenfeld ES, Hintz HF, Pell AN. 2008. Nutritional quality of gorilla diets: consequences of age, sex, and
season. Oecologia 155:111–122.
Russo SE, Campbell CJ, Dew JL, Stevenson PR, Suarez SA.
2005. A multi-forest comparison of dietary preferences and
seed dispersal by Ateles spp. Int J Primatol 26:1017–1037.
Ryan A. 1979. Wear striation direction on primate teeth: a scanning electron microscope examination. Am J Phys Anthropol
50:155–168.
Rylands AB, Mittermeier RA. 2009. The diversity of the New
World primates (Platyrrhini): an annotated taxonomy. In:
577
Garber PA, Estrada A, Bicca-Marques JC, Heymann EK,
Strier KB, editors. South American primates: comparative
perspectives in the study of behavior, ecology, and conservation. New York: Springer. p 23–54.
Sabater-Pi J. 1977. Contribution to the study of alimentation of
lowland gorillas in the natural state in Rio Muni, Republic of
Equatorial Guinea (W. Africa). Primates 18:183–204.
Sayers K, Norconk MA. 2008. Himalayan Semnopithecus entellus at Langtang National Park, Nepal: diet, activity patterns,
and resources. Int J Primatol 29:509–530.
Schaller G. 1963. The mountain gorilla: ecology and behavior.
Chicago: University of Chicago Press.
Schubert BW, Ungar PS, DeSantis LRG. 2010. Carnassial
microwear and dietary behaviour in large carnivorans. J Zool
280:257–263.
Schulz E, Calandra I, Kaiser TM. 2010. Applying tribology to
teeth of hoofed mammals. Scanning 32:162–182.
Scott JR, Godfrey LR, Jungers WL, Scott RS, Simons EL, Teaford MF, Ungar PS, Walker A. 2009. Dental microwear texture analysis of two families of subfossil lemurs from Madagascar. J Hum Evol 56:405–416.
Scott R, Schubert B, Grine F, Teaford MF. 2008. Low magnification microwear: questions of precision and repeatability.
J Vertebr Paleontol 28:139A.
Scott RS, Ungar PS, Bergstrom TS, Brown CA, Childs BE, Teaford MF, Walker A. 2006. Dental microwear texture analysis:
technical considerations. J Hum Evol 51:339–349.
Scott RS, Ungar PS, Bergstrom TS, Brown CA, Grine FE, Teaford MF, Walker A. 2005. Dental microwear texture analysis
shows within-species diet variability in fossil hominins. Nature 436:693–695.
Semprebon GM, Godfrey LR, Solounias N, Sutherland MR,
Jungers WL. 2004. Can low-magnification stereomicroscopy
reveal diet? J Hum Evol 47:115–144.
Silcox MT, Teaford MF. 2002. The diet of worms: an analysis of
mole dental microwear. J Mammal 83:804–814.
Solounias N, Hayek LAC. 1993. New methods of tooth microwear analysis and application to dietary determination of two
extinct antelopes. J Zool 229:421–445.
Solounias N, Moelleken S. 1992a. Tooth microwear analyses of
Eotragus sansaniensis (Mammalia: Ruminantia), one of the
oldest known bovids. J Vert Paleontol 12:113–121.
Solounias N, Moelleken SMC. 1992b. Dietary adaptations of two
goat ancestors and evolutionary considerations. Geobios
25:797–809.
Solounias N, Moelleken S. 1994. Dietary differences between
two archaic ruminant species from Sansan, France. Hist Biol
7:203–220.
Solounias N, Semprebon G. 2002. Advances in the reconstruction of ungulate ecomorphology with application to early fossil
equids. Am Mus Novitates 3366:1–49.
Son V. 2003. Diet of Macaca fascicularis in a mangrove forest,
Vietnam. Lab Prim News 42:1–5.
Sponheimer M, Passey BH, de Ruiter DJ, Guatelli-Steinberg D,
Cerling TE, Lee-Thorp JA. 2006. Isotopic evidence for dietary
variability in the early hominin Paranthropus robustus. Science 314:980–982.
Srivastava A. 1989. Feeding ecology and behaviour of Hanuman
langur, Presbytis entellus. PhD Thesis. University of Jodhpur.
Jodhpur, India.
Starin ED. 1991. Socioecology of the red colobus monkey in the
Gambia with particular reference to female-male differences
and transfer patterns. PhD Dissertation, City University of
New York.
Steenbeek R, van Schaik CP. 2001. Competition and group size
in Thomas’s langurs (Presbytis thomasi): the folivore paradox
revisited. Behav Ecol Sociobiol 49:100–110.
Strait DS, Weber GW, Neubauer S, Chalk J, Richmond BG,
Lucas PW, Spencer MA, Schrein C, Dechow PC, Ross CF, et al.
2009. The feeding biomechanics and dietary ecology of Australopithecus africanus. Proc Natl Acad Sci USA 106:2124–2129.
Strait SG. 1993. Molar microwear in extant small-bodied faunivorous mammals: an analysis of feature density and pit frequency. Am J Phys Anthropol 92:63–79.
American Journal of Physical Anthropology
578
R.S. SCOTT ET AL.
Suarez SA. 2006. Diet and travel costs for spider monkeys in a
nonseasonal, hyperdiverse environment. Int J Primatol
27:411–436.
Supriatna J, Manullang BO, Soekara E. 1986. Group composition, home range, and diet of the maroon leaf monkey (Presbytis rubicunda) at Tanjung Puting Reserve, Central Kalimantan, Indonesia. Primates 27:185–190.
Sussman R, Tattersall I. 1981. Behavior and ecology of Macaca
fascicularis in Mauritius: a preliminary study. Primates
22:192–205.
Suzuki A. 1969. An ecological study of chimpanzees in a
savanna woodland. Primates 10:103–148.
Teaford MF, Grine F, Schubert B, Ungar PS. 2008. Low magnification dental microwear: the problem of postmortem artefacts.
J Vert Paleontol 28:151A.
Teaford MF, Glander K. 1996. Dental microwear and diet in a
wild population of mantled howlers (Alouatta palliata). In:
Norconk M, Rosenberger A, Garber P, editors. Adaptive radiations of Neotropical primates. New York: Plenum Press.
p 433–449.
Teaford MF. 1985. Molar microwear and diet in the genus
Cebus. Am J Phys Anthropol 66:363–370.
Teaford MF. 1988a. A review of dental microwear and diet in
modern mammals. Scan Microsc 2:1149–1166.
Teaford MF. 1988b. Scanning electron-microscope diagnosis of
wear patterns versus artifacts on fossil teeth. Scan Microsc
2:1167–1175.
Teaford MF. 2007. What do we know and not know about dental
microwear and diet? In: Ungar PS, editor. Evolution of the
human diet: the known, the unknown and the unknowable.
New York: Oxford University Press. p 106–131.
Teaford MF, Glander KE. 1991. Dental microwear in live, wildtrapped Alouatta palliata from Costa Rica. Am J Phys
Anthropol 85:313–319.
Teaford MF, Lucas PW, Ungar PS, Glander KE. 2006. Mechanical defenses in leaves eaten by Costa Rican howling monkeys
(Alouatta palliata). Am J Phys Anthropol 129:99–104.
Teaford MF, Lytle JD. 1996. Diet-induced changes in rates of
human tooth microwear: a case study involving stone-ground
maize. Am J Phys Anthropol 100:143–147.
Teaford MF, Oyen OJ. 1989a. Differences in the rate of molar
wear between monkeys raised on different diets. J Dent Res
68:1513–1518.
Teaford MF, Oyen OJ. 1989b. In vivo and in vitro turnover in
dental microwear. Am J Phys Anthropol 80:447–460.
Teaford MF, Robinson JG. 1989. Seasonal or ecological differences in diet and molar microwear in Cebus nigrivittatus. Am J
Phys Anthropol 80:391–401.
Teaford MF, Runestad JA. 1992. Dental microwear and diet in
Venezuelan primates. Am J Phys Anthropol 88:347–364.
Teaford MF, Tylenda CA. 1991. A new approach to the study of
tooth wear. J Dent Res 70:204–207.
Teaford MF, Walker A. 1984. Quantitative differences in dental
microwear between primate species with different diets and a
comment on the presumed diet of Sivapithecus. Am J Phys
Anthropol 64:191–200.
Terborgh J, Janson C. 1983. The ecology of primates in southeastern Peru. Natl Geogr Soc Res Rep 15:655–662.
Tutin CEG, Fernandez M. 1985. Foods consumed by sympatric
populations of Gorilla g. gorilla and Pan t. troglodytes in Gabon: some preliminary data. Int J Primatol 6:27–43.
Tutin CEG, Fernandez M, Rogers ME, Williamson EA, McGrew
WC. 1991. Foraging profiles of sympatric lowland gorillas and
chimpanzees in the Lope Reserve, Gabon. Philos Trans R Soc
Lond B Biol Sci 334:179–186.
Tutin CEG, Ham RM, White LJT, Harrison MJS. 1997. The primate community of the Lope Reserve, Gabon: diets, responses
to fruit scarcity, and effects on biomass. Am J Primatol 42:1–24.
Tweheyo M, Lye KA, Weladji RB. 2004. Chimpanzee diet and
habitat selection in the Budongo Forest Reserve, Uganda.
Forest Ecol Manag 188:267–278.
Ungar PS. 2011. Dental microwear analysis. Beer’N’Bones 6:9–13.
Ungar PS. 1994. Incisor microwear of Sumatran anthropoid primates. Am J Phys Anthropol 94:339–363.
American Journal of Physical Anthropology
Ungar PS. 1995. Fruit preferences of four sympatric primate
species at Ketambe, Northern Sumatra, Indonesia. Int J Primatol 16:221–245.
Ungar PS. 2009. Tooth form and function: insights into adaptation through the analysis of dental microwear. Front Oral
Biol 13:38–43.
Ungar PS, Scott R. 2007. Microwear texture analysis: microwear as applied to fossil primates and human ancestors. J
Morphol 268:1143.
Ungar PS, Scott R. 2009. Dental evidence for diets of early
Homo. In: Grine F, Fleagle JG, Leakey R, editors. The first
humans. Dordrecht: Springer. p 121–134.
Ungar PS, Grine FE, Teaford MF. 2006. Diet in early Homo: a
review of the evidence and a new model of adaptive versatility. Annu Rev Anthropol 35:209–228.
Ungar PS, Grine F, Teaford MF. 2008a. Dental microwear and
diet of the Plio-Pleistocene hominin Paranthropus boisei.
PLoS One 3:e2044.
Ungar PS, Scott R, Scott J, Teaford MF. 2008b. Dental microwear analysis: historical perspectives and new approaches. In:
Irish JD, Nelson GC, editors. Technique and application in
dental anthropology. Cambridge; New York: Cambridge University Press. p 389–425.
Ungar PS, Krueger KL, Blumenschine RJ, Njau J, Scott RS.
Dental microwear texture analysis of hominins recovered by
the Olduvai Landscape Paleoanthropology Project, 1995-2007.
J Hum Evol, http://www.ncbi.nlm.nih.gov/pubmed/21784504.
Ungar PS, Krueger KL, Blumenschine RJ, Scott RS, Njau JK.
2010a. Dental microwear texture analysis of newly discovered
hominins from Olduvai Gorge. Am J Phys Anthropol (Suppl
50):232.
Ungar PS, Merceron G, Scott RS. 2007. Dental microwear texture analysis of Varswater bovids and early Pliocene paleoenvironments of Langebaanweg, Western Cape Province, South
Africa. J Mamm Evol 14:163–181.
Ungar PS, Scott JR, Schubert BW, Stynder DD. 2010b. Carnivoran dental microwear textures: comparability of carnassial
facets and functional differentiation of postcanine teeth.
Mammalia 74:219–224.
Ungar PS, Scott RS, Grine FE, Teaford MF. 2010c. Molar microwear textures and the diets of Australopithecus anamensis
and Australopithecus afarensis. Philos Trans R Soc Lond B
Biol Sci 365:3345–3354.
Ungar PS, Simon J-C, Cooper JW. 1991. A semiautomated
image analysis procedure for the quantification of dental
microwear. Scanning 13:31–36.
Ungar PS, Teaford MF, Glander KE, Pastor RF. 1995.
Dust accumulation in the canopy: a potential cause of
dental microwear in primates. Am J Phys Anthropol 97:93–99.
Visalberghi E, Sabbatini G, Spagnoletti N, Andrade FRD, Ottoni
E, Izar P, Fragaszy D. 2008. Physical properties of palm fruits
processed with tools by wild bearded capuchins (Cebus libidinosus). Am J Primatol 70:884–891.
Vogel ER, Haag L, Mitra-Setia T, van Schaik CP, Dominy NJ.
2009. Foraging and ranging behavior during a fallback episode: Hylobates albibarbis and Pongo pygmaeus wurmbii compared. Am J Phys Anthropol 140:716–726.
Vogel ER, van Woerden JT, Lucas PW, Atmoko SSU, van
Schaik CP, Dominy NJ. 2008. Functional ecology and evolution of hominoid molar enamel thickness: Pan troglodytes
schweinfurthii and Pongo pygmaeus wurmbii. J Hum Evol
55:60–74.
Walker A. 1980. Functional anatomy and taphonomy. In: Behrensmeyer A, Hill A, editors. Fossils in the making. Chicago:
University of Chicago Press. p 182–196.
Walker A. 1981. Dietary hypotheses and human evolution.
Philos Trans R Soc Lond B Biol Sci 292:57–64.
Walker A. 1984. Mechanisms of honing in the male baboon canine. Am J Phys Anthropol 65:47–60.
Walker P. 1976. Wear striations on the incisors of cercopithecoid
monkeys as an index of diet and habitat preference. Am J
Phys Anthropol 45:299–308.
Watts DP. 1984. Composition and variability of mountain gorilla
diets in the Central Virungas. Am J Primatol 7:323–356.
DENTAL MICROWEAR TEXTURE AND ANTHROPOID DIETS
Wheatley B. 1978. The behavior and ecology of the crab-eating
macaque (Macaca fascicularis) in the Kutai Reserve, East
Kalimantan, Indonesia. PhD Dissertation, University of California, Davis.
Wheatley B. 1980. Feeding and ranging of East Bornea Macaca
fascicularis. In: Lindburg D, editor. The macaques: studies in
ecology, behavior and evolution. New York: Van Nostran Reinhold. p 215–246.
Whiten A, Byrne RW, Barton RA, Waterman PG, Henzi SP.
1991. Dietary and foraging strategies of baboons. Philos Trans
R Soc Lond B Biol Sci 334:187–197.
Wich SA, Utami-Atmoko SS, Setia TM, Djoyosudharmo S,
Geurts ML. 2006. Dietary and energetic responses of Pongo
abelii to fruit availability fluctuations. Int J Primatol
27:1535–1550.
Williams FL, Patterson JW. 2010. Reconstructing the paleoecology of Taung, South Africa from low-magnification of dental
microwear features in fossil primates. Palaios 25:439–448.
Williams SH, Wright BW, Den Truong V, Daubert CR, Vinyard
CJ. 2005. Mechanical properties of foods used in experimental
studies of primate masticatory function. Am J Primatol
67:329–346.
Wrangham RW. 1977. Feeding behavior of chimpanzees in
Gombe National Park, Tanzania. In: Clutton-Brock TH,
editor. Primate ecology. New York: Academic Press. p
504–538.
579
Wrangham RW, Conklin NL, Chapman CA, Hunt KD. 1991. The
Significance of fibrous foods for Kibale Forest chimpanzees.
Philos Trans R Soc Lond B Biol Sci 334:171–178.
Wrangham RW, Conklin-Brittain NL, Hunt KD. 1998. Dietary
response of chimpanzees and cercopithecines to seasonal variation in fruit abundance. I. Antifeedants. Int J Primatol
19:949–970.
Wright BW. 2005. Craniodental biomechanics and dietary toughness in the genus Cebus. J Hum Evol 48:473–492.
Wright BW, Wright KA, Chalk J, Verderane MP, Fragaszy D,
Visalberghi E, Izar P, Ottoni EB, Constantino P, Vinyard C.
2009. Fallback foraging as a way of life: using dietary toughness to compare the fallback signal among capuchins and
implications for interpreting morphological variation. Am J
Phys Anthropol 140:687–699.
Yamagiwa J, Maruhashi T, Yumoto T, Mwanza N. 1996. Dietary
and ranging overlap in sympatric gorillas and chimpanzees in
Kahuzi-Biega National Park, Zaire. In: McGrew WC, Marchant LF, Nishida T, editors. Great ape societies. Cambridge:
Cambridge University Press. p 82–98.
Yamakoshi G. 1998. Dietary responses to fruit scarcity of wild
chimpanzees at Bossou, Guinea: possible implications for ecological importance of tool use. Am J Phys Anthropol 106:283–295.
Yeager CP. 1996. Feeding ecology of the long-tailed macaque
(Macaca fascicularis) in Kalimantan Tengah, Indonesia. Int J
Primatol 17:51–62.
American Journal of Physical Anthropology
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