8 Dental Adaptations of
African Apes
Mark F. Teaford . Peter S. Ungar
Abstract
Improvements in the primate fossil record, and in methods of data acquisition
and analysis, have set the stage for new insights into the development, function,
and evolution of hominoid teeth. This chapter is a brief review of recent advances.
In essence, genetic analyses are changing our perspectives on the evolution of
morphology, while improved studies of dental development and microstructure
have yielded permanent markers of developmental history and microstructural
differences of functional significance. More realistic perspectives on the physical
properties of foods are yielding new functional interpretations of differences in
tooth size. Finally, landmark‐free analyses of tooth shape and wear are giving
researchers the chance to actually monitor how teeth are used in living primates
and by extrapolation in fossil primates too. Through techniques such as these will
come a better understanding of the intricacies of dental function and a clearer
picture of our past.
8.1
Introduction
People have been fascinated by the similarities between apes and humans ever
since the first reports of apes filtered out of Africa. Linnaeus struggled to incorporate them into his System of Nature, but anatomical studies by Tyson (1699) and
Huxley (1863), among others, forced the world to recognize the striking resemblance between African apes, in particular, and modern humans. Now, with the
ape and human fossil record raising more questions, and technological advances
generating new perspectives on morphology, it is time to take another look at the
teeth of African apes, to see what we do, and do not know about them.
8.2
Dental development
Some of the most revolutionary discoveries in all of morphology have come in the
areas of genetics and dental development, where subtle genetic changes have been
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shown to have major impacts on morphology (Jernvall et al. 2000; Salazar‐
Ciudad et al. 2003). Thus far, studies have been restricted to laboratory animals
such as rodents, but the potential impact on studies of morphological change
in ape and human evolution are immense. With that point in mind, what do we
know about dental development in the African apes? Methods of data collection
have sometimes overlapped and sometimes varied dramatically, but some general
trends are still evident in the literature.
Longitudinal data for nonhuman primates are rare, and this is certainly true
for studies of dental development in apes, where methods of monitoring crown
and root development have generally involved either detailed dissections or
radiographs of different individuals of known ages (Zuckerman 1928; Dean and
Wood 1981; Swindler 1985; Beynon et al. 1991; Conroy and Mahoney 1991;
Winkler 1995; Kuykendall 1996) (although see Anemone et al. 1991 for an exception to this). Net results have included estimates of the timing of tooth calcification and emergence, and patterns of inter‐tooth differences in those events.
Analyses of chimpanzees have been far more common than those of other
apes, due largely to the fact that chimps are often used in laboratory research.
Ultimately, results are frequently compared with those for humans.
Estimates of the timing of tooth and root calcification have yielded not only
some consistent patterns in apes and humans but also some patterns of differences between those groups. Specifically, dental development in apes is completed
much more quickly than in humans, at approximately 11–12 years as compared
with approximately 18–20 years (Nissen and Riesen 1964; Conroy and Mahoney
1991; Kuykendall 1996). Yet apes and humans have fairly similar patterns of cusp
initiation and tooth mineralization (Swindler 1985), and their tooth crowns take
similar times to develop (Dean and Wood 1981; Beynon et al. 1991). Two factors
help clarify this apparent dilemma. First, there are significant differences in the
degree of overlap between the development of certain teeth in apes and humans.
For instance, in humans, each of the permanent molars completes its crown
development before the next molar crown begins to develop. In apes, by contrast,
there is a great deal of overlap in the timing of development of the molars (Reid
et al. 1998; Dean 2000). A second factor helping to explain the faster completion
of dental development in apes is a quicker rate of root growth after crown
completion (Anemone et al. 1991, 1996; Simpson et al. 1992; Kuykendall 1996;
Reid et al. 1998).
Finer‐resolution differences in dental development may ultimately be discernible, both within and between species, e.g., differences between the sexes in
some tooth mineralization stages (Kuykendall 1996) or differences in the formation time of specific molar cusps (Reid et al. 1998). However, additional resolution
Dental adaptations of african apes
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will probably require further refinement of techniques (Winkler 1995; Beynon
et al. 1998; Reid et al. 1998).
The net result of these developmental events is a complex pattern of sequences that can, by itself, be used to gain insights into primate life history
(Smith 1991, 1994). Schultz (1960) recognized a basic distinction between relatively rapid‐ and slow‐growing primates, with the former gaining all of their
permanent molars before the eruption of more anterior permanent teeth. Hominoids are all relatively slow growing, but variations in their sequences of dental
eruption (so‐called tooth sequence polymorphisms) (Garn and Lewis 1963) can
still yield insights. For instance, comparisons of humans and common chimpanzees show that humans have much greater variability in the eruption of their
canines and lower central incisors, whereas chimpanzees show greater variability
in the eruption of their second molars (Smith 1994). Still, if the actual timing of
dental eruption can also be calculated (see > Section 8.5.2 below), then the eruption of most pairs of teeth is highly correlated (Smith 1989), and the eruption of
the first and last permanent teeth are, in turn, highly correlated with other life
history variables.
8.3
Dental microstructure
Dental enamel is formed of hydroxyapatite crystals bundled together into prisms
which are, in turn, often woven together in complex patterns, including radial
enamel and decussating Hunter‐Schreger bands (Martin et al. 1988; Koenigswald
and Clemens 1992; Rensberger 1997; Maas and Dumont 1999). This inherent
complexity has left researchers with a wealth of research possibilities, ranging
from permanent markers of developmental history to structural anisotropy of
functional significance.
8.3.1 Incremental microstructural features
Close examination of enamel prisms has revealed so‐called ‘‘cross‐striations’’
(periodic thickenings) laid down in a circadian fashion (Schour and Hoffman
1939; Massler and Schour 1946; Boyde 1964). This, coupled with surface markers
known as perikymata, has allowed researchers to estimate the amount of time
necessary for crown completion in modern hominoids (Dean and Wood 1981;
Beynon et al. 1998; Reid et al. 1998; Shellis 1998; Dean 2000). But it has also given
insights into tooth formation time and age at death in fossils (Bromage and Dean
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1985; Beynon and Dean 1988; Dean et al. 1993), thereby suggesting that most of
the early hominids had an ‘‘apelike’’ pattern of dental development.
8.3.2 Enamel prism patterns
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Before histological studies of the timing of dental development, researchers felt
that the shape of prisms in prepared tooth‐sections (prism packing patterns)
could be used in phylogenetic studies as certain patterns might be characteristic
of certain taxonomic groups (Shellis and Poole 1977; Gantt 1979, 1983; Xirotiris
and Henke XX). However, subsequent work showed that results were often
dependent on methods of specimen preparation (Boyde et al. 1978; Vrba and
Grine 1978). Detailed analyses of enamel at controlled depths subsequently
suggested that hominoids might exhibit an unusual preponderance of ‘‘type 3’’
enamel (Boyde and Martin 1982; Martin et al. 1988). However, more work is
still necessary to document the range of possibilities within and between large
samples of teeth.
8.3.3 Enamel thickness
One obvious result of the complex process of tooth formation in most mammals
is an enamel cap covering the tooth crown—a cap that can vary rather dramatically in thickness. Studies of molar enamel thickness in hominoids have gradually
progressed from simple linear measurements (Gantt 1977; Kay 1981) to more
complex measures designed to account for differences in body size (Martin 1983,
1985). Given the complexity of crown shape and development, it is perhaps no
wonder that there have been continuing discussions about proper methods of
analysis (Grine 1991, 2002, 2005; Macho and Thackeray 1992; Macho and Berner
1993; Macho 1994; Dumont 1995). However, if one were to use a summary
‘‘measure’’ to characterize molar enamel thickness in hominoids, they could
probably be characterized as follows: Gorilla has relatively thin enamel, Pan and
Pongo range from thin to average thickness depending on tooth type, and Homo
has thick enamel (Shellis et al. 1998). These variations in enamel thickness are
probably due to differences in the duration of crown formation rather than the
rate of enamel production (Beynon et al. 1991).
Of course, along with differences in enamel thickness come questions of the
functional significance of those differences. Given the inherent complexity of
primate foods and diets, it is not surprising that the correlation between enamel
thickness and diet is not a perfect one (Maas and Dumont 1999), nor that the
Dental adaptations of african apes
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physical properties of enamel may vary within the tooth crown and even between
species (Cuy et al. 2002; Teaford et al. 2002). Over the past two decades, conventional wisdom has dictated that thick enamel enabled primates to consume
harder foods (Kay 1981; Dumont 1995). However, that perspective is changing
largely because researchers are finally accepting the idea that enamel complexity,
particularly prism decussation, serves as an admirable crack‐stopping mechanism
(Pfretzschner 1986; Koenigswald et al. 1987; Rensberger 1993, 2000; Maas and
Dumont 1999). Thus it may be that prism decussation is a better correlate of
hard‐object feeding than is enamel thickness (Martin et al. 2003). In either case,
we must remember that thick enamel may be an adaptive response to a variety of
factors (Shellis et al. 1998).
8.4
Tooth size
Measurements of tooth size have been the focus of some classic studies of ape
and human dentitions (Ashton and Zuckerman 1950; Schuman and Brace 1955;
Garn et al. 1965; Pilbeam 1969; Mahler 1973; Johanson 1974; Swindler 1976).
However, while some interspecific and intraspecific differences in tooth size are
undoubtedly associated with differences in body size (Garn et al. 1968; Gingerich
et al. 1982; Conroy 1987), the more intriguing trends are those differing from the
standard assumption that larger animals simply have larger teeth.
For instance, investigators have long known that humans have relatively small
canines compared to modern apes (Gregory 1922). However, among modern
apes, chimpanzees and orangutans have relatively larger incisors than do gorillas
and gibbons (Hylander 1975; Kay and Hylander 1978). As a result, differences
in incisor size may reflect differences in the degree of incisor use in ingestion
(Ungar 1996).
Intraspecific differences in canine size have also been used as indicators of
sexual dimorphism, with gibbons and humans showing relatively little sexual
dimorphism and chimps, bonobos, gorillas, and orangs all showing significantly higher sexual dimorphism (Ashton and Zuckerman 1950; Johanson 1974;
Swindler 1976; Kinzey 1984). This has led to further inferences about differences
in social behavior (Kelley 1986; Plavcan et al. 1995), with, for instance, species
showing high degrees of sexual dimorphism also showing polygynous mating
systems.
However, if analyses of tooth size are going to move from simple correlations
(between morphological and behavioral differences) to explanations of causation,
we need a better appreciation of the complexities of such relationships. In the
1970s, discussions began on the exact nature of the relationship between tooth
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size and body size, with initial studies suggesting close ties between postcanine
tooth area and body metabolism (Pilbeam and Gould 1974; Gould 1975), but
subsequent analyses showing such a relationship to be grossly oversimplified (Kay
1975; Fortelius 1985). The confounding variables apparently come in two forms.
First, analyses of modern primates have shown that the relationship between diet
and food‐processing is extremely complicated (Fortelius 1985; Lucas 2004). Thus,
for example, both the rate of chewing and the physical response of food to
chewing may influence the relationship between tooth size and diet. Second,
analyses of fossil primates have shown that phylogenetic history may also complicate analyses of tooth size (Kay and Ungar 1997; Ungar 2002). For instance,
Miocene apes generally have smaller incisors than modern apes.
So, is there a way to gain new insights from analyses of tooth size? Recent
work by Lucas and coworkers (Lucas et al. 1986; Lucas 2004) suggests that there
may be. In essence, anterior teeth and postcanine teeth are probably responding
to different types of functional demands and thus need to be treated differently.
Anterior tooth size is linked to the size of ingested particles, whereas posterior
tooth size may depend on the deformability of the food, including a variety of
properties like stickiness, particle shape, etc. Thus, perhaps relative differences
in tooth size between incisors and molars in modern apes are giving us more
subtle clues about the dietary differences between species. For instance, the fact
that the gorilla has relatively small incisors compared to its molars may not simply
indicate less reliance on the incisors in ingestion. It may also reflect the fact that
the molars of gorillas often process relatively small food particles that are not very
sticky (Lucas 2004). Clearly, however, more work is needed on the relationship
between tooth size and the properties of foods.
8.5
Dental morphology and wear
As Aristotle noted nearly two‐and‐a‐half millennia ago in De Generatione Animalium, tooth form reflects function. Studies of mammalian dental functional
morphology do not date back quite that far, but they certainly boast a long and
celebrated history nonetheless (Owen 1840; Gregory 1922). Early work on primate
teeth, for example, suggested that their molars evolved to improve mechanical
efficiency for particular masticatory movements (Crompton and Sita‐Lumsden
1970; Kay and Hiiemae 1974). Primates that habitually crush foods have been
noted to possess flat molar surfaces, whereas those that shear and slice have highly
crested teeth (Rosenberger and Kinzey 1976; Seligsohn and Szalay 1978).
As in analyses of tooth size, dental functional morphology has recently begun
to take more of a biomechanical perspective, focusing on relationships between
Dental adaptations of african apes
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tooth shape and the strength, toughness, and deformability of foods (Strait 1993;
Lucas and Teaford 1994; Spears and Crompton 1996; Yamashita 1998; Lucas 2004;
Lucas et al. 2004). Primates that specialize on tough foods (those that are difficult
to fracture), such as insect exoskeletons and mature leaves, generally have
reciprocally concave, highly crested teeth for shearing and slicing. In contrast,
those primates that prefer hard, brittle foods (those that resist initial puncture but
are easy to fracture once a crack has started), such as many seeds, nuts, and palm
fronds, tend to have rounder, flatter molar teeth for processing such items.
8.5.1 Quantifying functional aspects of tooth form
Of course, as we try to decipher more complicated relationships between dental
form and function, quantitative approaches to characterizing tooth shape become essential. Researchers have thus developed several methods for characterizing tooth shape. The most popular of these is Kay’s (1978, 1984) shearing quotient
(SQ) method. The lengths of mesiodistal crests are measured on unworn molars
of several closely related species with similar diets. A least‐squares regression
line is fit to summed crest length and mesiodistal occlusal surface length in
logarithmic space. SQs are computed as residuals or deviations from the regression line. This approach tracks diets of living apes fairly well, as the more
folivorous siamang and gorilla have relatively longer shearing crests than do
extant frugivorous hominoids (Kay 1977; Kay and Ungar 1997).
Spears and Crompton (1996) have suggested an alternative approach, measuring great ape cusp slopes from molar cross‐sections. They found that gorillas
had high‐angled occlusal surfaces, orangutans had gradually sloping surfaces, and
chimpanzees had shallow ‘‘supporting’’ cusps, but steeper ‘‘guiding’’ slopes. These
findings are taken to suggest that orangutans are adapted to reduce a hard/brittle
diet, whereas gorillas can more efficiently fracture small food particles by shear.
Chimpanzees, on the other hand, seem to be better suited to a diet with a wide
range of mechanical properties. Such analyses probably give us more functional
insights than do analyses of molar crown and cusp areas (Wood and Abbott 1983;
Wood and Engelman 1988). However, as emphasized by Uchida (1998), the latter
may still yield insights into a combination of genetic and ecological factors.
8.5.2 Tooth wear analyses
While studies of tooth morphology give glimpses of the complex relationship
between primate tooth shape and diet, most such work has been limited to
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unworn teeth. This is a major limitation because it leads to an incomplete picture
of the form–function relationship. Wear is a normal phenomenon that begins as
soon as a primate’s teeth come into occlusion. Thus, natural selection should also
act on worn teeth, favoring morphologies that wear in a manner that keep them
mechanically efficient for fracturing foods (Kay 1981, 1985; Teaford 1983; Teaford
and Glander 1996; Ungar and Williamson 2000). In essence, since tooth wear
occurs throughout an animal’s lifetime, we are missing a great deal of information
if we exclude worn teeth in our analyses. Another limitation of studies that
depend exclusively on unworn teeth is the lack of sufficient numbers of specimens
for many (especially fossil) taxa. We find it remarkable, for example, that the
entire published sample of early hominids from South Africa boasts less than 10
unworn M2s (the teeth most often used in functional studies).
The tooth wear of apes has occasionally been the focus of work in previous
investigations. Early studies examined the degree of tooth wear in apes and humans in attempts to correlate tough, abrasive diets with the presence of increased
tooth wear (Black 1902; Campbell 1925; Schultz 1935; Ashton and Zuckerman
1950; Welsch 1967). As noted by Wolpoff (1971), however, such interpretations
are complicated by the complexities of diet and mastication, not to mention
methodological difficulties associated with incorporating differences in dental
eruption timing into such analyses.
Some investigators have made more detailed comparisons along the tooth
row, noting, for example, that chimpanzees exhibit heavier incisor wear than do
other apes (Ashton and Zuckerman 1950; Welsch 1967), again suggesting heavier
incisor use in chimpanzees. More recently, Dean et al. (1992) have noted that
later‐erupting molars in chimpanzees and gorillas may actually show heavier wear
than their predecessors, suggesting that occlusal loading is greatest on the last
molar in the tooth row. It is perhaps no wonder then that molars in these species
may also exhibit compensatory eruption as wear progresses (Dean et al. 1992)
similar to that documented for some human populations (Whittaker et al. 1982,
1985).
With the advent of cineradiographic and electromyographic studies of mastication, studies of molar wear facets began to document subtle differences in jaw
movement between primate species, with modern apes generally showing an
increased emphasis on crushing and grinding as compared with some other
catarrhines (Kay 1977; Maier and Schneck 1981). With these suggestions, analyses
of tooth wear took another crucial step toward deciphering the relationship
between dental form and function. If differences in the patterns of wear might
indicate differences in jaw movement, could changes in tooth shape with wear
yield further insights?
Dental adaptations of african apes
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A look through the literature, however, reveals a striking paucity of such
studies. Why? Quite simply, it is not easy to measure tooth shape on worn teeth.
Traditional dental morphometrics depend on measuring distances between landmarks that are quickly obliterated by wear. Smith (1999) attempted to control for
wear using a technique modified from Wood and coauthors (Wood et al. 1983).
Molar occlusal views were captured on video and individual cusp areas were
identified on a computer screen by mouse driven cursor. This allowed calculation
of relative 2D (planometric) areas of cusps on unworn to moderately worn teeth
(as long as cusp boundaries were identifiable). Smith’s results suggest that cusp
proportions do indeed reflect diet to some degree, e.g., chimpanzees are linked
with gibbons rather than gorillas.
Even this approach though is not ideal. First, specimens must still be sufficiently unworn to distinguish individual cusp boundaries, and these disappear
pretty quickly, especially on thin enameled molars, such as those of chimpanzees
and gorillas. More importantly, planometric area studies do not adequately
characterize the third dimension of dental morphology. This is a problem because
mastication occurs in a 3D environment, and two teeth with similar projected 2D
areas may differ greatly in cusp relief.
The ability to collect elevation data is vital to studies of dental functional
morphology. Cheek teeth have been known for the better part of a century to act
as guides for jaw movements (Simpson 1933; Crompton and Sita‐Lumsden 1970;
Hiiemae and Kay 1972). Surface relief is critical to the angle of approach of mandibular and maxillary teeth as facets come into occlusion during mastication.
This in turn determines the biomechanical efficiency with which items of given
mechanical properties are fractured (e.g., whether foods are sheared or crushed).
8.5.3 Dental topographic analysis
What we need is a way to consider worn teeth in 3D studies of dental functional
morphology. This is where dental topographic analysis comes in. Elevation data
representing an occlusal surface are collected using a 3D scanner, and the tooth
is modeled and analyzed using geographic information systems (GIS) software
(Zuccotti et al. 1998; Jernvall and Selänne 1999) (> Figure 8.1). Because dental
topographic analysis does not depend on specific landmarks for measurement,
it is equally useful for measuring unworn and worn teeth.
Some results for studies of living great apes are summarized and combined
here to provide an example. Ungar and coworkers studied dental topography of
Gorilla gorilla gorilla and Pan troglodytes troglodytes (M’Kirera and Ungar 2003;
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. Figure 8.1
Digital elevation model (left) and contour map (right) of a tooth. The contour interval is
25.4 mm, with a field of view corresponding to the area represented by the box
Ungar and M’Kirera 2003; Ungar and Taylor 2005). These taxa were chosen for
analysis because of the modest degree to which they differ in the material properties of the foods they consume. At sites where the two taxa are sympatric, such as
Lopé, Gabon, central African chimpanzees and western lowland gorillas overlap
considerably in their diets, preferring soft, succulent fruits. The two taxa do differ
though, especially at times of fruit scarcity. At such times, gorillas fall back more
on tough, fibrous foods than do chimpanzees (Tutin et al. 1991; Remis 1997).
Average annual food type proportions reported for central African common
chimpanzees include about 70–80% fruit flesh, as compared with 45–55% fruit
flesh for western lowland gorillas (Williamson et al. 1990; Kuroda 1992; Nishihara
1992; Tutin et al. 1997).
Dental topographic analysis of Pongo pygmaeus pygmaeus (Ungar and Taylor
2005) can add further insights into great ape molar form and function. The
Bornean orangutan consumes an enormous variety of foods ranging from hard‐
husked, brittle nuts to soft fruits, to leaves, bark, and insects (MacKinnon 1977;
Rodman 1977; Leighton 1993). While items consumed depend greatly on seasonal availability, average annual fruit to leaf proportions for Pongo pygmaeus
pygmaeus are intermediate between those reported for Pan troglodytes troglodytes
and Gorilla gorilla gorilla, with an average fruit percentage of about 55–65%
reported for the orangutans (MacKinnon 1977; Rodman 1977)—noting caveats
concerning differences in data collection methods (Doran et al. 2002).
Data on average surface slope and occlusal relief are illustrated in > Figures
8.2–8.4. These data are based on variably worn M2s of Pongo pygmaeus pygmaeus
(n ¼ 51), Pan troglodytes troglodytes (n ¼ 54), and Gorilla gorilla gorilla (n ¼ 47).
Methods of data collection are presented in detail elsewhere (Ungar and Williamson
2000; M’Kirera and Ungar 2003; Ungar and M’Kirera 2003). Occlusal surfaces
Dental adaptations of african apes
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. Figure 8.2
Triangulated irregular network representations of surface data for M2s of representative
specimens at wear stage 1 (corresponding to Scott scores 10–14 [Scott 1979]): (a) Gorilla
gorilla gorilla (CMNH B1781), (b) Pongo pygmaeus pygmaeus (SAPM 1981/62)
. Figure 8.3
Comparisons of mean surface slope values for given wear stages. Wear stages correspond
to Scott wear scores as follows: (1) 10–14, (2) 15–19, (3) 20–24 (Scott 1979)
were scanned as point clouds with lateral and vertical resolutions of 25.4 mm using
a laser scanner. Resulting data files were opened as tables in ArcView 3.2 (ESRI
Corp) GIS software, and digitial elevation models were cropped to exclude areas
below the lowest point of the occlusal basin. Average slope between adjacent points
(surface slope) and the ratio of 3D to 2D planometric area (occlusal relief) were
then recorded for each specimen.
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. Figure 8.4
Comparisons of mean surface occlusal relief values for given wear stages. Wear stages
correspond to Scott wear scores as follows: (1) 10–14, (2) 15–19, (3) 20–24 (Scott 1979)
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Results are illustrated in > Figures 8.2–8.4. The species overlapped in three
wear stages (as defined in Ungar 2004). As expected, more worn molar surfaces of
each taxon showed less occlusal relief and shallower slopes. At any given stage of
wear, however, gorillas had the steepest slopes and most occlusal relief, followed
by orangutans. Chimpanzees had the shallowest molar cusps and least occlusal
relief.
This example suggests several things. First, tooth shape changes with wear.
As teeth wear down, cusp slopes and occlusal relief both decline. Such changes
likely affect functional efficiency. Further, apes with varying diets differ in the
shapes of their teeth in ways that reflect the mechanical properties of foods that
they eat. Species adapted to shearing and slicing tough leaves should have more
occlusal relief and steeper sloped cusps than those adapted to crushing and
grinding fruit. Cusp slope and occlusal relief values do mirror leaf‐to‐fruit ratios
quite nicely for the great apes.
Another important point to come from this example is the notion that
differences between species are of the same magnitude at different stages of wear.
In fact, two factor ANOVA results show no significant interaction between species
and wear stage for any of the variables examined (M’Kirera and Ungar 2003;
Ungar and M’Kirera 2003; Ungar 2004; Ungar and Taylor 2005). This basically
means that differences between species remain consistent through the wear sequence. In other words, we can compare chimps, gorillas, and orangutans at any
given wear stage and get the same results. This is important because it means that
species need not be represented by unworn teeth as long as there is a baseline of
comparative data for specimens with similar degrees of wear. This will allow us to
reconstruct the diets of a whole new assortment of fossil taxa that could not be
analyzed in the past for lack of available methods.
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8.5.4 Fallback foods and dental functional morphology
Another point emphasized by this work is the fact that gross differences in dental
functional morphology need not relate to gross differences in preferred foods.
Fecal studies for gorillas and chimpanzees at Lopé, for example, show 60–80%
plant species overlap (Williamson et al. 1990; Tutin and Fernandez 1993). These
apes eat fruits much of the year but diverge at ‘‘crunch times’’ when preferred
fruits are scarce. At such times, gorillas fallback more on leaves and other fibrous
plant parts. The same is true for sympatric mountain gorillas and chimpanzees at
the Bwindi Impenetrable National Park in Uganda (Stanford and Nkurunungi
2003). Differences between gorilla and chimpanzee occlusal morphology described here reflect fallback food choice more than everyday dietary preferences
per se.
Apes have a penchant for succulent, sugar‐rich foods—a legacy of the
ancestral catarrhine dietary adaptation (Ross 2000; Ungar 2005). Differences in
diet between catarrhines often rest largely with the seasonal shift to fallback foods
taken when preferred resources are less available (Rogers et al. 1992; Lambert et al.
2004). In these cases, preferred resources are easy to digest, offer a low cost‐benefit
ratio, and may not result in selective pressures that would tax functional morphology. On the other hand, less desirable but seasonally critical fallback foods
might require some morphological specialization (Robinson and Wilson 1998).
This is not a new idea. Kinzey (1978), for example, noted that while Callicebus
moloch and C. torquatus are both primarily frugivorous, the former has longer
shearing crests for slicing leaves and the latter has larger talonid basins for
crushing insect chitin. He reasoned that dental morphology therefore reflects
adaptations not only to primary foods but also to less frequently eaten but still
critical ones.
8.5.5 Function and phylogeny
As indicated earlier, in discussions of tooth size, another issue to consider when
inferring dietary adaptations from morphology is the effect of phylogeny. Phylogenetic inertia or baggage plays an important role in how adaptations manifest
themselves (Kay and Ungar 1997). We know, for example, that shearing quotients
track diet within cercopithecoids, hominoids, and platyrrhines—folivores have
longer crests than frugivores within each of these higher‐level taxa. On the other
hand, cercopithecoids have relatively longer shearing crests than hominoids, and
hominoids have relatively longer shearing crests than platyrrhines independent of
diet (Kay and Covert 1984).
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Because phylogeny determines the starting point for morphology, care must
be taken when considering an extant baseline series to which an extinct species
should be compared. One approach has involved considering ranges. For example, Early Miocene apes tend to have less well‐developed shearing crests than do
extant hominoids—though their ranges of SQ values are similar. It appears as if
the extant hominoid range is upshifted relative to the Early Miocene ape range
but reflects a comparable array of diets (Kay and Ungar 1997; Ungar et al. 2004).
This can be confirmed by ‘‘anchoring’’ the range using independent data such as
dental microwear patterning.
8.5.6 Dental microwear analyses
Fifty years ago, investigators realized they could gain insights into jaw movement
and tooth use through light microscope analyses of wear patterns on teeth (Butler
1952; Dahlberg 1960; Dahlberg and Kinzey 1962). Subsequent work rekindled
interest in the topic (Grine 1977; Rensberger 1978; Walker et al. 1978; Puech and
Prone 1979; Ryan 1979) as many workers shifted to using the scanning electron
microscope. Since then, analyses of modern and fossil material have yielded
insights into dietary variations within and between species and also new perspectives on the evolution of tooth use and diet in animals ranging from dinosaurs to
human ancestors (see Teaford 1994; Rose and Ungar 1998; Ungar 2002 for recent
reviews).
The advantage of dental microwear analysis is that it provides evidence of
what an animal was actually doing during its lifetime, not merely what it was
capable of doing. Thus far, analyses of modern hominoids have generally been
based on small samples (Gordon 1982, 1984; Teaford and Walker 1984; Teaford
1988; King et al. 1999), a factor which must be kept in mind when considering
microwear data for animals, like chimpanzees and orangutans, with variable
diets. Also, standard SEM analyses are proving to have a subjective component
that may complicate comparisons of results between different investigators
(Grine et al. 2002). Still, results to date suggest diets dominated by soft fruit for
the chimpanzee; fruit with perhaps some hard objects for the orangutan; and
tough, leafy vegetation for the mountain gorilla (Teaford and Walker 1984;
Teaford 1988) (> Figure 8.5). Interestingly, comparisons of results for lowland
and mountain gorillas yield microwear differences suggestive of the dietary
differences documented in the literature (Tutin and Fernandez 1993; Remis
1997), with lowland gorillas showing a higher incidence of pitting on their molars
as compared with mountain gorillas (King et al. 1999) (> Figure 8.6). Dental
microwear analyses of Pan paniscus are just beginning.
Dental adaptations of african apes
8
. Figure 8.5
Scanning electron micrographs of modern and fossil molars. a ¼ Cebus apella, b ¼ Homo
sapiens (Arikara), c ¼ Homo habilis, d ¼ Homo erectus, e ¼ Pan troglodytes, f ¼ Gorilla gorilla
beringei
As might be expected, dental microwear analyses of human ancestors have
focused on whichever fossils are available. For the anterior teeth, qualitative
studies have suggested similarities between early hominid incisor wear and that
observed on modern primates that routinely employ a great deal of incisal
preparation (Puech and Albertini 1984). Quantitative analyses of Australopithecus
afarensis suggested similarities with lowland gorillas or perhaps savanna baboons
(Ryan and Johanson 1989), while more detailed analyses of Paranthropus robustus
and A. africanus (Ungar and Grine 1991) showed great variabilitiy within each
species, but a greater density of features on the incisors of A. africanus, suggesting
that A. africanus had a heavier emphasis on incisal preparation than in P. robustus.
In the molar region, qualitative analyses have raised many possibilities
that have been often repeated in the literature. For instance, the robust australopithecines have been characterized as indistinguishable from modern chimpanzees or orangs (Walker 1981), perhaps with more abrasive molar wear than in the
gracile australopithecines (Puech et al. 1985, 1986; Puech 1986b). Quantitative
analyses have begun to refine these interpretations from a number of different
15
16
8
Dental adaptations of african apes
. Figure 8.6
Scanning electron micrographs of Gorilla gorilla beringei (top) and Gorilla gorilla gorilla
(bottom)
perspectives. Studies of nonocclusal microwear have focused primarily on more
recent European taxa, with initial analyses portraying the Neanderthals as more
carnivorous than their immediate predecessors, or subsequent Homo sapiens
(Lalueza Fox and Pérez‐Pérez 1993; Lalueza et al. 1996). However, subsequent
work has raised the possibility of sexual differences in diet in Homo heidelbergensis (Pérez‐Pérez et al. 1999), and a more heterogeneous diet for the Neanderthals,
with a shift in food processing in the Upper Paleolithic (Pérez‐Pérez et al. 2003).
Quantitative analyses of fossil molar occlusal microwear began with Grine’s
pioneering work on the South African australopithecines, where Paranthropus
robustus was shown to exhibit more microwear and more pitting on its molars
than did A. africanus (Grine 1981, 1986, 1987; Grine and Kay 1988). This leant
Dental adaptations of african apes
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8
huge support to Robinson’s ideas of dietary differences among the australopithecines, with the so‐called robust forms consuming harder foods that required more
variable grinding movements in chewing. Recent work has taken analyses a step
further by incorporating samples of australopithecines and early Homo from East
and South Africa. Initial results give further credence to Ryan and Johanson’s
(1989) idea of similarities between Australopithecus afarensis and lowland gorillas
(Teaford et al. 2002a; Grine et al. in preparation). Meanwhile, analyses of early
Homo have begun to help sort through the variable assemblage that now encompasses that taxon, with Homo erectus/ergaster showing a higher incidence of
pitting on its molars than that found in Homo habilis (Ungar et al. in press),
suggesting the consumption of tougher or harder food items by the former group.
As most studies of dental functional morphology ultimately hinge upon
assumptions of the usefulness and selective advantage of the structures being
measured, dental microwear analysis can certainly provide corroborative evidence for other hypotheses, for instance (as noted earlier) by ‘‘anchoring’’ analyses of dental morphological variation. Thus, dental microwear and molar
shearing crest analyses for Eurasian fossil hominoids suggest that Oreopithecus
was a folivore, Ouranopithecus was a hard‐object feeder, and remaining forms
such as Dryopithecus were soft‐fruit eaters (Ungar et al. 2004). By contrast, molar
shearing crest analyses of African Miocene hominoids suggest at first glance that
all were either soft‐fruit eaters or hard‐object feeders. However, the microwear
evidence suggests that molar shearing quotients for the African Miocene taxa are
‘‘downshifted’’ by about 50%, with Rangwapithecus as a folivore and the remaining taxa as soft‐fruit eaters.
Obviously, knowing what we now do about primate diets, dietary categorizations such as these are gross oversimplifications. Either fallback foods or
preferred foods may be of crucial importance for the survival and reproduction
of individuals. Thus, either may be a selective force to be reckoned with in the
evolution of morphological differences. So how can we tease them apart? The key
lies in the collaborative use of as many lines of evidence as possible, on samples
that are as large as possible (Teaford et al. 1996). For the fossil record, we have
what we have, and we have to make do with it until more fossils are discovered.
However, even now, the combination of dental microwear analyses and other
morphological data has allowed researchers to document a gradual broadening of
dietary capabilities in the earliest hominids (Teaford and Ungar 2000). This has
then provided a backdrop against which to interpret the origin and early evolution of our genus (Teaford et al. 2002b), including, once again, insights into the
distinction between dental capabilities and dental use, as the ability to process
certain foods may well have been of critical importance in certain situations (e.g.,
meat‐eating in Homo erectus) (Ungar et al. in press).
17
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Dental adaptations of african apes
The bottom line is that researchers have only begun to tap into the wealth of
data, some from old sources and some from new. As noted above, new landmark‐
free analyses of morphology allow comparisons of tooth shape at any degree of
wear, without the subjective identification of specific landmarks. Similarly, new
objective methods of dental microwear analysis (Scott et al. 2005) allow the rapid
characterization of microscopic wear surfaces for entire teeth in a matter of
minutes. Through techniques such as these, we cannot help but gain a better
grasp of variations in modern animals. With that will come a better understanding of the intricacies of dental function, and with that will come a clearer picture
of our past.
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