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Dental wear wear rate and dental disease in the African apes.

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American Journal of Primatology 72:481–491 (2010)
RESEARCH ARTICLE
Dental Wear, Wear Rate, and Dental Disease in the African Apes
ALISON A. ELGART
Department of Biological Sciences, Florida Gulf Coast University, Fort Myers, Florida
The African apes possess thinner enamel than do other hominoids, and a certain amount of dentin
exposure may be advantageous in the processing of tough diets eaten by Gorilla. Dental wear (attrition
plus abrasion) that erodes the enamel exposes the underlying dentin and creates additional cutting
edges at the dentin-enamel junction. Hypothetically, efficiency of food processing increases with
junction formation until an optimal amount is reached, but excessive wear hinders efficient food
processing and may lead to sickness, reduced fecundity, and death. Occlusal surfaces of molars and
incisors in three populations each of Gorilla and Pan were videotaped and digitized. The quantity of
incisal and molar occlusal dental wear and the lengths of dentin–enamel junctions were measured in
220 adult and 31 juvenile gorilla and chimpanzee skulls. Rates of dental wear were calculated in
juveniles by scoring the degree of wear between adjacent molars M1 and M2. Differences were
compared by principal (major) axis analysis. ANOVAs compared means of wear amounts. Pearson
correlation coefficients were calculated to compare the relationship between molar wear and incidence
of dental disease.
Results indicate that quantities of wear are significantly greater in permanent incisors and molars
and juvenile molars of gorillas compared to chimpanzees. The lengths of dentin–enamel junctions were
predominantly suboptimal. Western lowland gorillas have the highest quantities of wear and the most
molars with suboptimal wear. The highest rates of wear are seen in Pan paniscus and Pan t. troglodytes,
and the lowest rates are found in P.t. schweinfurthii and G. g. graueri. Among gorillas, G. b. beringei
have the highest rates but low amounts of wear. Coefficients between wear and dental disease were low,
but significant when all teeth were combined. Gorilla teeth are durable, and wear does not lead to
mechanical senescence in this sample. Am. J. Primatol. 72:481–491, 2010.
r 2010 Wiley-Liss, Inc.
Key words: dental wear; African apes; wear rate
INTRODUCTION
Gorillas (Gorilla gorilla and Gorilla beringei
beringei) are presumed to possess numerous adaptations to deal with the communition of an herbivorous, tough diet [e.g., Blower, 1956; Carroll, 1988;
Cousins, 1988; Groves, 1966, 1971; Remis, 1994;
Sarmiento et al., 1996; Schaller, 1963]. In the
absence of any gorilla fossil evidence, it is not
possible to trace the historical genesis of these
adaptations, but the three gorilla populations are
assumed to have similar dietary ‘‘selective regimes’’
in comparison to other taxa that would determine
the fitness of certain traits [Baum & Larson, 1991].
Adaptations will be defined here as traits that
enhance performance in an individual. This will be
tested by their ‘‘current utility’’ [Baum & Larson,
1991; Gould & Vrba, 1982; Greene, 1986; Losos &
Miles, 1994]. Performance, defined as how an
individual carries out a task, determines what
resources can be used, and in turn will have an
impact upon reproduction and survival (fitness)
[Wainwright, 1994]. Traits that affect the processing
of food and test durability, such as dental wear rate,
r 2010 Wiley-Liss, Inc.
quantity of dental wear, and presence or absence of
dental pathology related to dental failure, were
chosen to test performance. This study was part of
a wider study examining masticatory functional
morphology using the phylogenetic method in which
Gorilla is compared to its sister taxon, Pan.
Like any tool, teeth are subject to surface wear
from use. To date, no studies have correlated the
true toughness of food to the quantity of dental wear
in animals, although such wear and friction studies
are carried out in materials science. Previous studies
have demonstrated that excessive dental attrition
can have dire effects in organisms, from reduced
Contract grant sponsor: Mario Einaudi Center of Cornell
University, Kosciusko Foundation.
Correspondence to: Alison A. Elgart, Department of Biological
Sciences, Florida Gulf Coast University, 10501 FGCU Blvd.
South, Fort Myers, FL 33965. E-mail: aelgart@fgcu.edu
Received 19 May 2009; revised 8 December 2009; revision
accepted 12 December 2009
DOI 10.1002/ajp.20797
Published online 13 January 2010 in Wiley InterScience (www.
interscience.wiley.com).
482 / Elgart
fecundity to early mechanical senescence [Lanyon &
Sanson, 1986; Raupp, 1985]. Once the enamel is
worn away, the processing of food on the underlying
dentin is very inefficient in comparison to enamel,
and an animal has to either consume more food or
chew more in order to survive [Lanyon & Sanson,
1986; Pérez-Barberı́a & Gordon, 1998].
The mountain gorilla (Gorilla beringei beringei)
diet is highly herbivorous and is presumed to be
tough relative to other gorilla populations [see
Elgart-Berry, 2004]. Gorillas in general possess
molars with higher cusps and ‘‘greater shearing’’
capabilities than other African apes [Kay, 1975,
1981; M’Kirera & Ungar, 2003; Shea, 1983; Uchida,
1996], as is expected with a tough diet. They have the
thinnest enamel of any ape [Kay, 1981; Kono, 2004;
Olejiniczak et al., 2008; Vogel et al., 2008], which
may be advantageous because it wears quickly
creating additional cutting edges between the enamel and dentin [Aiello et al., 1991; Kay, 1985; Kono,
2004; Mills, 1978; Vogel et al., 2008]. Whether this
constitutes an adaptation in Gorilla or G. b. beringei,
in particular, will be tested by examining if teeth are
worn to a theoretical optimal level.
It has previously been reported that Gorilla has
greater quantities of dental wear than Pan and
Pongo, mainly due to an earlier weaning age [Aiello
et al., 1991], but studies are not conclusive as to
which gorilla species demonstrates the greatest
amount [Cousins, 1988; Welsch, 1967]. This study
will examine whether mountain gorillas have greater
dental wear than other African apes and whether
this is correlated with dental disease. High degrees of
wear may either be directly fatal, affecting food
processing, or indirectly fatal by causing disease,
which in turn affects food consumption. The overall
quantity and position (anterior vs. posterior) of
dental wear between two species each of gorillas
and chimpanzees were calculated by measuring the
mean percent area of dentin exposure on the occlusal
surface of the teeth for each molar tooth and for the
incisors using digital imaging. Quantity of wear is, of
course, correlated with age; therefore, rates of dental
wear were also calculated in juvenile Pan and Gorilla
by scoring the quantity of wear between adjacent
molars M1 and M2.
eating brittle food. At the very least, this would cause
the teeth to come into contact more often with the
abrasives found either outside the food plants (dust)
or inside the food plants (phytoliths), causing greater
dental wear [Fortelius, 1985; Janis, 1995; Lucas
et al., 1986]. Raupp [1985] demonstrated that beetles
wore their mandibles faster when they fed on
‘‘tougher’’ leaves, and consequently, worn mandibles
slowed ingestion rates and lowered fecundity. According to Fortelius [1985], Laws observed that
hippopotami graze on grass and water plants, but
have evolved from mammals that were not grazers.
Their diet is tougher and more abrasive than that of
their ancestors, and they incur such high degrees of
wear on their teeth that they often die of mechanical
senescence at ages older than 30 years. Hypothetically, a similar situation may be present in some
gorillas.
Gorilla Morphology at the Species Level
Like hippopotami, gorillas have evolved from
primates that were not strict herbivores. Miocene
hominoids were probably frugivorous [Andrews,
1981; Kay, 1977; Nelson, 2003] and most extant apes
have a diet consisting predominantly of ripe fruit.
Gorillas have larger molars with higher cusps,
greater shearing, crushing, and grinding capabilities
than other African apes [Kay, 1975, 1978, 1981; Kay
& Hylander, 1978; Shea, 1983; Uchida, 1996], and
about 6% have fourth molars [Schultz, 1950].
Gorillas also have higher, narrower dentin horns,
extensions of dentin that present as pointed cusps
due to the thin enamel, in comparison to orangutans
and chimpanzees [Shellis et al., 1998]. Relative to the
molars, gorillas have smaller, narrower incisors than
do other apes [Kay & Hylander, 1978; McCollum,
2007].
Morphological distinctions exist at the gorilla
species level as well. Mountain gorillas (G. b.
beringei) may exhibit adaptations to a herbivorous
diet such as larger teeth, more developed jaw
musculature, higher crowned molars, extra cusps
five and six on the upper teeth and an extra cusp six
on the lower teeth, and a longer tooth row in
comparison to western lowland gorillas (G. g. gorilla)
[Booth, 1971; Cousins, 1988; Groves, 1970; Uchida,
1996].
Wear and Physical Properties of Food
In certain dental wear studies, physical properties are inferred, albeit not directly tested. Smith
[1972], investigating dental wear in several human
populations, found a high correlation between the
rate of wear and the ‘‘properties of the diet,’’
although these are not detailed. Welsch [1967]
concluded that folivorous primates had more wear
on their posterior teeth than did frugivorous primates. Animals that masticate tougher foods would
have to chew these foods more thoroughly than those
Am. J. Primatol.
Gorilla Dental Wear and Pathological
Conditions
Previous studies have reported moderate
amounts of periodontal disease in gorillas. Mountain
gorillas suffer from heavy calculus deposits, which
result in 100% of adult museum specimens exhibiting alveolar destruction [Cousins, 1988; Lovell,
1990]. Lovell [1990] reported that out of 22 individuals in Fossey’s mountain gorilla collection, 18%
suffered from periapical abscesses and 45% had
Dental Wear in African Apes / 483
interdontal abscesses, and each individual had lost
approximately one tooth ante-mortem. Schultz
[1950], whose study collection did not include
mountain gorillas, concluded that abscesses were
found in similar frequency in gorillas and in other
apes. Lowland gorillas have smaller teeth and
mandibles than the highland species, and their
premolars and molars are crowded. They also suffer
from alveolar abscesses [Elgart-Berry, 2000]. Cousins
[1988] reported less dental wear in mountain gorilla
teeth compared to lowland gorilla teeth, due to the
extra cusps, but conversely Welsch [1967, p 989]
reported ‘‘especially heavily worn teeth’’ in mountain gorillas in comparison to other apes.
A certain amount of wear on molars is advantageous to gorillas. Attrition will wear the enamel
covering the molar cusps and the dentin below will
be exposed, thereby creating additional cutting edges
at the dentin–enamel junction [Aiello et al., 1991;
Kay, 1985; Kono, 2004; Mills, 1978; Vogel et al.,
2008]. Tools are often made with a hard, wearresistant material next to a softer one, so that
differential wear has the effect of sharpening the
structure [Rabinowitz, 1995], which is akin to the
positioning of enamel (hard and wear resistant) next
to dentin (soft) in worn teeth. An animal example of
this is found in rodent central incisors, which lack
enamel on the lingual aspect thereby maintaining a
sharp edge. As teeth wear, additional enamel–dentin
cutting edges increase until a certain time, when the
‘‘dentin lakes’’ begin to merge. Further wear blunts
and obliterates the enamel edges until finally the
whole occlusal surface is exposed dentin, all the
cutting edges are gone, and wear is very rapid
through the soft dentin. The molars are worn down
to stubs and they are virtually useless in processing
food, as demonstrated in koalas and red deer
[Lanyon & Sanson, 1986; Pérez-Barberı́a & Gordon,
1998]. Animals with excessive dental wear exhibit a
higher number of chews per amount of food ingested,
lower food intake, spend longer periods of time
chewing, and have larger fecal particles. Lanyon and
Sanson [1986, p 171] conclude ‘‘tooth wear is (thus)
ultimately responsible in determining the physiological well-being and hence longevity of an animal.’’
In this study, gorillas are expected to have a
greater degree of wear than chimpanzees, but it is
hypothesized that the position of this wear will
differ. Generally, frugivores exhibit greater wear of
anterior teeth than of posterior teeth, as demonstrated in colobus [Janis, 1984] and chimpanzees
[Dean et al., 1992]; therefore, it is expected that
gorillas will have more posterior wear in comparison
to chimpanzees. However, confounding variables
include the ingestive positioning of food and ambient
dust. For example, Bwindi gorillas (G. b. beringei)
were observed to pull stems and bark through their
incisors as well as postcanine teeth [Elgart-Berry,
2000], and therefore, not all incisal wear can be
attributed to fruit ingestion. If the attrition of the
thin enamel of the gorilla is an adaptation, gorillas
should have a higher wear rate than chimpanzees
and should have more teeth at optimal wear states,
although optimality is not a necessity for identifying
adaptations [Greene, 1986]. If performance is not
affected, gorilla teeth should be durable; pathological
conditions related to dental failure should not be
correlated with the amount of dental wear in
individuals.
METHODS
Skeletal collections were accessed from the
National Museum of Natural History, Washington,
DC, The Cleveland Museum of Natural History,
Cleveland, and the Musée Royal de L’Afrique
Centrale, Tervuren, Belgium. This study did not
involve any living primates; therefore, the research
protocols and ethical standards for working with
such primates do not apply. The research did adhere
to all legal requirements.
Dental wear (attrition plus abrasion) was quantified on the incisors and molars of 39 Gorilla
beringei beringei, 32 Gorilla gorilla graueri, 69
Gorilla gorilla gorilla, 19 Pan paniscus, 53 Pan t.
troglodytes, and 8 Pan t. scheweinfurthii adult crania
(Table I). Wear of deciduous dentition (aged 3–6
years) was measured in 5 G. b. beringei, 5 G. g.
graueri, 13 G. g. gorilla, and 8 P. t. troglodytes. Using
a method similar to Uchida [1996], the occlusal
surface of the dentition was videotaped using a Sony
Hi-8 video camera fitted with a macro-lens positioned
on a tripod perpendicular to the cervical line of the
teeth. A horizontal plane was achieved by placing a
line level on the occlusal surface of the teeth. A scale
was placed either on the teeth or next to them at the
level of the occlusal surface and the scaled image of
two teeth was digitized using the program NIH
Image (developed by W. Rasband). Each dentin lake
TABLE I. Dental Wear Measurements Taken
Areas of dentin quantified (in mm)
Adults
1. Right I1 and I2 (or left where right is missing)
2. Lingual half of M1, M2, M3
3. Buccal half of M1, M2, M3
4. Right I1 and I2
5. Lingual half of M1, M2, M3
6. Buccal half of M1, M2, M3
7. Occlusal surface area
8. Dentin area percentage: ((lingual1buccal dentin)/occlusal
surface area)
9. Perimeter of dentin exposures
Juveniles: all the above measurements except
(a) Right i1, i2, i1, and i2 where present
(b) Right m1, m2, m1, m2
(c) Right M1 and M1 only
Am. J. Primatol.
484 / Elgart
TABLE II. Index of Dental Pathology
Dental disease categorization
1. No dental pathology observed
2. Minor dental pathology present, e.g., calculus or roots
partially exposed
3. Moderate dental pathology present, e.g., one abscess, or
two minor conditions or two or more teeth lost
premortem
4. Three or more pathological conditions present in
dentition including at least one abscess
5. Severe dental pathology, e.g., multiple abscesses
Fig. 1. Digitized image of two mandibular molars with dentin
lakes traced.
was traced (Fig. 1). Image calculated the area and
perimeter of the whole tooth and the area of dentin
exposure. Quantity of wear is measured in two
dimensions only, so total wear will be underestimated. This type of study ignores the wear of the
enamel before dentine is exposed, as Mayhall and
Kageyama [1997] point out, but gorillas and chimpanzees have thin enamel.
Other measurements include the lengths of
dentin–enamel junctions (the ‘‘blades’’) on all molars
to test how many individuals exhibit the ‘‘optimum’’
in length [Alexander, 1996; Lanyon & Sanson, 1986].
These lengths were measured and calculated as the
perimeter of enamel on M1–M3, and the optimal
length was defined as the maximum amount that the
perimeter measures before the junctions are obliterated by further wear and the lengths decrease. Dental
wear that has not reached the optimum in length
is referred to as ‘‘suboptimal,’’ while wear that is
past the optimum is ‘‘supra-optimal.’’ A polynomial
regression of the second order was run to examine
the relationship between the perimeter and the mean
amount of wear across the three molars, the latter of
which loosely estimates age. A regression plot depicts
the optimum at maximum y where x 5 xmax and the
slope of the line is zero [Alexander, 1996].
The mean percent area of dentin was calculated
for each molar and incisor. Mean and standard
deviations of percent wear were calculated for each
tooth per species, and ANOVAs contrasted the means
of dentin exposure of the Pan species, the three
populations of adult gorillas, and the juveniles. Incisal
to molar wear ratios comparing wear on the maxillary
first incisor (I1) to the maxillary first molar (M1) were
tested for significant differences by a paired t-test.
Ante-mortem tooth loss and dental disease
(abscesses, caries, and excess calculus) were recorded
in all specimens. Severity of pathology was categorized according to an index (Table II), with 1 scored if
there is no pathology related to the dentition and 5
scored if severe dental disease is present. Pearson
correlation coefficients were calculated first between
Am. J. Primatol.
the quantity of wear on maxillary M1 and the
pathology index and second between the quantity
of wear on the maxillary I1 and the index to test
whether a linear relationship exists between each
pair. A Fisher’s r to z transformation was carried out
on the correlations and 95% confidence intervals
were calculated to test for significance.
Wear Rate
Compromising this wear study is the lack of known
ages for most museum specimens; therefore, an ageindependent measurement, dental wear rate, was
calculated [Molnar et al., 1983; Rose & Ungar, 1998;
Scott, 1979; Smith, 1972]. Rate of wear was compared
in juvenile Pan and Gorilla by the principal axis
technique [Benfer & Edwards, 1991; Scott, 1979],
which is based on measuring the amount of wear on
M1 when M2 comes into occlusion, and represents
approximately 2.7 years of wear in apes [Aiello & Dean,
1990]. It employs Model II regression, which does not
assume that the X variable is measured without error
[Sokal & Rohlf, 1995]. Furthermore, there is no causal
relationship between each x and y (wear on M1 and M2
in this case) warranting least-squares regression
analysis. Model II regression defines an ellipse of points
and fits a line through the principal axis of it. The slope
of this line indicates the wear rate and may be
compared to other slopes, with a high slope indicative
of a high rate of wear [Scott, 1979].
To test for precision of measurement, the
dentition of ten specimens was measured twice.
Forty-six different measurements were compared in
a paired sample t-test. The correlation coefficient was
0.99 and P-values were nonsignificant (P40.05).
RESULTS
The results of an intergeneric comparison of the
quantity of dental wear are presented in Table III
and are depicted in Figure 2. Unpaired t-tests
(df 5 160–198) compared permanent and deciduous
dentition of all Gorilla and Pan samples. Adult
gorillas have significantly (Po0.05) greater attrition
on their M1, M3, and on their first incisors compared
to adult chimpanzees. In juveniles, gorillas have
Dental Wear in African Apes / 485
significantly greater amounts of wear on m1 and m2,
but significantly less wear than chimpanzees on i1.
The mean amount of wear (percent of exposed
dentin) and the standard deviation for each tooth by
species is presented in Table IV. The highest
percentiles are found in the upper first incisor: Pan
paniscus exhibits the greatest mean quantity of wear
on this tooth (67.2%), followed by Gorilla g. gorilla
(66.7%), and G. g. graueri (61.7%). The wear on the
mandibular incisors is greatest in western lowland
gorillas (G. g. gorilla) while eastern lowland gorillas
(G. g. graueri) have the greatest wear on the first
molars. Dental wear of mountain gorillas (G. b. beringei)
is very low, even lower than any Pan measurement
(Fig. 3). All standard deviations in this table are very
high, as there is much variation in mean quantity of
wear. It is age-dependent and not very informative.
The mean percent perimeter, which is the length
of the dentin–enamel junctions divided by the
perimeter of the whole tooth, is given for each
species as well. This number is an average across the
maxillary molars M1 to M3. Eastern lowland gorillas
have the maximum perimeter length for M1–M3
followed by Pan t. schweinfurthii.
The polynomial regression revealed a significant
(Po0.0001) relationship between the perimeter and
the mean percent wear across the molars
(R2 5 0.799). In the regression plot (Fig. 4), the
optimum is positioned at 50% wear. Only 4%
(N 5 23) of G. b. beringei, 15% (N 5 47) of G. g.
gorilla, 21% (N 5 31) of G. g. graueri, and 13%
(N 5 50) of Pan have supra-optimal perimeters,
meaning that the vast majority of individuals have
less than an optimal quantity of dentin–enamel
junctions (Fig. 4).
TABLE III. Results of a Gorilla-Pan Comparison by
Student’s t-Tests of the Quantity of Wear on the
Mandibular Permanent Molars (M) and Incisors (I)
and the Deciduous Molars (m) and Incisors (i)
Tooth
I1
I2
M1
M2
M3
i1
i2
M1
M2
Gorilla X7SD
Pan X7SD
P-value of t-test
49.7730.5
35.1728.4
33.3724.9
20.5720.1
13.7720.6
15.573.1
21.474.5
61.5719.8
81.6720.8
37.2726.1
33.1724.4
25.8723.9
15.7720.3
8.2712.9
19.974.1
22.774.1
29.473.7
45.577.8
o0.01
0.64
o0.05
0.11
o0.05
o0.05
0.51
o0.001
o0.0001
P-values are two-tailed. Values are percent wear on a tooth relative to the
occlusal surface.
Fig. 2. Comparison of the percent dentin exposure on the occlusal
surface of mandibular permanent incisors (I) and molars (M) and
deciduous incisors (i) and molars (m) in Pan and Gorilla.
TABLE IV. Means and Standard Deviations of Degree of Wear, by Tooth and by Species
Tooth
Species
N
M3 X7SD
M3 X7 SD
M2 X7 SD
M2 X7 SD
M1 X7 SD
M1 X7 SD
G. b. beringei
G. g. gorilla
G. g. graueri
Pan paniscus
P. t. schweinfurthii
P. t. troglodytes
29
68
35
15
9
52
1.373.0
11.8717.9
12.4718.6
7.279.1
14.3712.9
6.1713.4
11.7725.6
16.8721.9
17.6723.8
5.675.8
15.6717.5
7.3712.4
7.3711.2
25.6725.8
27.7726.4
11.5715.0
28.1728.4
13.6720.4
8.0714.7
24.2721.4
24.9722.4
12.3714.1
31.7728.6
14.6720.2
22.1724.5
38.2726.4
48.1732.1
28.7724.2
36.7727.8
25.1723.5
14.3718.9
37.6725.8
37.9725.6
21.9718.9
31.1728.3
25.1724.9
Tooth
Species
G. b. beringei
G. g. gorilla
G. g. graueri
Pan paniscus
P. t. schweinfurthii
P. t. troglodytes
I X7SD
I2 X7SD
I X7SD
I1 X7SD
Mean % perimeter,
M1 M37SD
21.6721.8
46.9732.3
37.6735.1
58.2734.6
46.7737.4
40.7731.0
17.2721.2
40.5730.9
34.0729.8
35.4722.0
32.7726.5
31.7724.3
30.2728.8
66.7732.8
61.7730.6
67.2727.5
53.3737.5
51.6728.5
32.5732.7
52.9730.7
46.8729.2
47.8724.6
35.3728.5
32.6724.8
11.4713.5
25.6722.9
29.0723.8
17.0716.1
26.6721.4
14.8718.2
2
1
Values are percents. Mean percent of perimeter is the average perimeter of the dentin lakes from M1–M3. Bold indicates highest value for each tooth.
Am. J. Primatol.
486 / Elgart
Fig. 3. Means of percent attrition on occlusal surface of
mandibular molars (M) and incisors (I) for all species measured.
Fig. 4. Plot of the polynomial regression of the second order for
all individuals. The x-axis is the mean percent wear on the
maxillary molars M1–M3, and the y-axis is the length of the
dentin-enamel junctions (perimeter). The regression equation
and R2 is given below the graph.
An ANOVA: F 5 6.1, df 5 91, P 5 0.003 examined the differences in the quantity of wear within
the Gorilla genus (Table V). Significant differences
(Po0.05) were found between G. b. beringei and
G. g. gorilla, and often between G. b. beringei and
G. g. graueri. In each of these cases, G. b. beringei
has the least amount of wear, G. g. gorilla has
the greatest amount of wear on the incisors, and
G. g. graueri the greatest amount on the molars.
Another ANOVA: F 5 4.7, df 5 2, P 5 0.02 demonstrates that this pattern is already present in the
juveniles in the second deciduous molar. In both
ANOVAs, the variation within a group is larger than
the variation between groups.
The mean percent and standard deviation of
wear on the maxillary first incisor and molar, incisor
to molar ratios, and results of the paired two-tailed ttests (df 5 22–103) are shown in Table VI. All ratios
are greater than one because incisal wear is greater
than molar wear in each species. Mountain gorillas
have the lowest mean ratio (1.4), followed by Gorilla
g. graueri (1.6), while all other species have means
above 3.0, which means these latter species have
approximately twice as much wear on their incisors
as on their molars. An ANOVA: F 5 3.03, df 5 5,
P 5 0.01 deemed the differences between the eastern
gorillas on one hand and the western gorillas and
Pan species on the other significant.
To examine wear rate, major axis equations
from Model II regression of the wear on the
maxillary first and second molar were calculated
and plotted for each species (Fig. 5). Slopes of each
line (Table VII), indicating the wear rate, are similar,
and range from 1.1 to 1.49. Ninety-five percent
confidence limits were calculated and the only slopes
TABLE V. Results of ANOVAs and Student’s t-Tests of Mean Degree of Wear by Gorilla Subspecies and by Upper
Tooth
Species ANOVA
I1
t-tests
I2
t-tests
M1
t-tests
M2
t-tests
M3
t-tests
m2
Perimeter M1–M3
t-tests
G. b. beringei X7SD
G. g. gorilla X7SD
G. g. graueri X7SD
30.2728.8
G. b. beringei–G. g. gorilla
G. b. beringei–G. g. graueri
21.6721.7
G. b. beringei–G. g. gorilla
21.5724.5
G. b. beringei–G. g. gorilla
G. b. beringei–G. g. graueri
7.3711.2
G. b. beringei–G. g. gorilla
G. b. beringei–G. g. graueri
1.373.0
G. b. beringei–G. g. gorilla
G. b. beringei–G. g. graueri
5.5
11.4713.5
G. b. beringei–G. g. gorilla
G. b. beringei–G. g. graueri
66.7732.8
61.7730.6
46.9732.3
37.6735.1
38.2726.4
48.1732.1
25.6725.8
27.7726.4
11.8717.9
12.4718.6
12.1
25.6722.9
9.4
29.0723.8
Bold numbers show highest values per tooth.
Am. J. Primatol.
P value
0.0002
o0.0001
0.002
0.008
0.001
0.002
0.004
0.0009
0.002
0.0006
0.0002
0.020
0.020
0.020
0.060
0.003
0.002
0.0008
Dental Wear in African Apes / 487
TABLE VI. Means and Results of Paired t-Tests on Incisor vs. Molar Wear for Each Species
Subspecies
N
% wear I17SD
Gorilla b. beringei
Gorilla g. graueri
Gorilla g. gorilla
Pan paniscus
Pan t. troglodytes
P. t. schweinfurthii
21
21
66
13
44
5
30.2733.1
62.2728.9
77.1729.5
68.1726.7
52.6730.0
53.2737.4
P value
G. b. beringei
G. b. beringei
G. g. graueri
G. g. gorilla
Pan paniscus
Pan t. troglodytes
P.t. schweinfurthii
–
0.67
o0.01
0.001
0.04
0.04
% wear M17SD
G. g. graueri
0.67
–
o0.01
o0.01
o0.001
0.03
26.7726.3
46.3730.1
38.2727.1
28.8724.2
25.3724.4
29.3725.7
G. g. gorilla
o0.01
o0.01
–
0.10
0.18
0.62
I1/M1 X
1.4
1.6
3.1
4.4
3.8
3.6
Pan
paniscus
0.001
o0.01
0.10
–
0.42
0.62
Pan t.
troglodytes
0.04
o0.001
0.18
0.42
–
0.88
Pan t.
schwein-furthii
0.04
0.03
0.62
0.62
0.88
–
Means, standard deviations, and the mean ratio of maxillary incisal to molar (I1/M1) wear is presented in the upper table. In the lower table, the significance
of the test is given as a P-value. Significant P-values are in bold.
TABLE VIII. Amount of Tooth Loss and Dental
Disease, by Percentage, for Each Species
Fig. 5. Comparison of major axis lines for each species. Wear on the
second maxillary molar (M2) is contrasted with wear on the first
maxillary molar (M1). The equations of the lines are in Table VII.
TABLE VII. Equations of the Principal or Major
Axis, from Model II Regression
Group
N
Equation of
principal axis
95% confidence
interval of slope
Gorilla b. beringei
Gorilla g. graueri
Gorilla g. gorilla
Pan paniscus
Pan t. troglodytes
P.t. schweinfurthii
16
28
68
16
52
7
y 5 3.911.29x
y 5 9.011.14x
y 5 7.711.24x
y 5 4.611.49x
y 5 6.611.30x
y 5 3.911.10x
1.2–1.5
1.0–1.5
1.1–1.4
1.0–2.0
1.2–1.5
0.8–1.1
Sample size, N, and 95% confidence intervals for the slopes are given.
that have separate intervals with reasonable certainty are G. g. gorilla and Pan t. schweinfurthii.
Pan paniscus has the highest wear rate, while P. t.
troglodytes and G. b .beringei have moderately high
rates. The lowest wear rates are found in P. t.
schweinfurthii and G. g. graueri. These rates are
opposite what one would expect from the quantity of
Species
N
Tooth loss (%)
Dental disease (%)
G. b. beringei
G. g. gorilla
G. g. graueri
Pan paniscus
Pan t. troglodytes
29
68
35
15
52
21
26
5
27
24
45
28
8
33
6
wear; however, the regression’s intercept indicates
that the amount of wear is highest in eastern
lowland gorillas when M2 comes into occlusion and
lowest in mountain gorillas. Only two of the rates,
that of G. g. gorilla and Pan t. schweinfurthii, are
significantly different. Among gorillas, mountain
gorillas have the highest rate of wear, followed
by western lowland gorillas and eastern lowland
gorillas.
Table VIII displays the percentage of antemortem tooth loss and dental disease, including
abscesses, caries, excess calculus, and root resorption, for each species. Mountain gorillas display the
greatest amount of dental disease (45%) due to a high
frequency of abscesses and problems associated with
excessive calculus deposits, and bonobos the greatest
amount of tooth loss (27%). Common chimpanzees
have the second highest percent of individuals with
tooth loss at 24% and a high incidence of caries. For a
similar reason, Western lowland gorillas also have a
high incidence of dental disease (28%). Eastern lowland gorillas have lower incidence of missing teeth
(5.3%) and dental disease (8%).
Pearson correlation coefficients expressing the
relationship of wear on individual teeth (M1, M2, etc.)
and dental disease for all teeth measured were
Am. J. Primatol.
488 / Elgart
TABLE IX. Pearson Correlation Coefficients for the Relationship between the Wear on (A) the Maxillary First
Molar and Pathological Conditions, and (B) the Maxillary First Incisor and Pathological Conditions in All
Individuals and Broken Down by Species
Maxillary M1-pathology
Group
Overall
Gorilla b. beringei
Gorilla g. graueri
Gorilla g. gorilla
Pan paniscus
Pan t. troglodytes
P. t. schweinfurthii
N
202
25
35
71
15
50
6
Correlation coefficient
0.19
0.20
0.05
0.34
0.39
0.43
0.81
Maxillary I1-pathology
P-value
N
o0.01
0.370
0.760
0.030
0.157
o0.01
0.051
171
21
25
57
12
50
6
Correlation coefficient
0.133
0.36
0.15
0.33
0.23
0.37
0.64
P-value
0.080
0.111
0.491
0.010
0.487
o0.01
0.192
Sample size and P-values are given. Bold P-values indicate significance at the Po0.05 level.
approximately 0.20. All were significant at Po0.05
according to a Fisher’s r to z transformation and a
confidence interval calculation except for the correlation between I1 wear and pathology. When the
correlation coefficients are examined by species, all
are low (under 0.5) with the exception of Pan t.
schweinfurthii and many are not significant, with
P-values above 0.05 (Table IX). The only significant
relationships in which the confidence interval does
not include zero are found between the correlations
of M1 and I1 wear to the disease indices of Gorilla g.
gorilla and Pan t. troglodytes.
DISCUSSION
Some hypotheses were supported while others
were not. As was predicted, adult gorillas have
significantly greater amounts of wear on their molars
and on their first incisors than adult chimpanzees,
and greater wear is found on the posterior teeth.
Correlations between dental disease and the amount
of dental wear were low, and no significant correlation was found in mountain gorillas, although one
was found in western lowland gorillas and common
chimpanzees. Contrary to what was predicted,
gorillas do not have a higher wear rate nor do they
have more teeth with an optimal dento–enamel
junction length than chimpanzees, nor do mountain
gorillas display the greatest amount of wear among
gorillas as was expected with a tougher diet.
The greater amount of wear in adult gorillas
compared to chimpanzees confirms the results of
other studies [Aiello et al., 1991; M’Kirera & Ungar,
2003; Welsch, 1967]. Juvenile gorillas have greater
wear than juvenile chimpanzees on their deciduous
molars but not on their incisors. Aiello et al. [1991]
also found greater attrition in deciduous Gorilla
dentition compared to Pan and Pongo, but they did
not test this statistically. They attributed this finding
to an earlier weaning age: gorillas are reported to eat
solid food at one to two months of age [Fossey &
Harcourt, 1977], and dentin exposure begins at
Am. J. Primatol.
about six months [Aiello et al., 1991] while chimpanzees do not eat solid food until about four to six
months [Goodall, 1986].
The difference in the amount of wear in adults is
presumably due to dietary differences: if gorillas are
processing tougher foods, then more power strokes of
the mandible are necessary, which translates into more
cutting by the ‘‘blades’’ of the dentition. More data are
required on the physical properties of gorilla and
chimpanzee foods to conclude this definitively. Increasing occlusal dental wear usually has the effect of
increasing the occlusal area of a tooth [Pérez-Barberı́a
& Gordon, 1998], which would be advantageous to
gorillas. Confounding this simple relationship is the fact
that due to thin enamel and high cusps, Gorilla has
very steep intercuspal angles while Pan has shallow
angles [M’Kirera & Ungar, 2003; Spears & Crompton,
1996]. With age, these differences in relief are maintained even with increasing dental attrition [M’Kirera
& Ungar, 2003; Ungar & M’Kirera, 2003], indicating
that functional morphology is maintained with wear.
Mountain gorillas exhibited the least amount of
wear among gorillas, which is probably not attributable to their diet because eastern lowland gorillas
consume many of the same items [Elgart, 2010], yet
exhibit the greatest amount of wear. The reason for
low amounts of wear in mountain gorillas remains
unclear. It may be due to the ages of the sample, and
the fact at least some of them were the victims of
poachers, to less ambient dust in their environment,
or to an unknown variable. Cousins [1988] concluded
that mountain gorilla teeth have less wear than
western lowland gorilla teeth because their teeth
have accessory cusps, but conversely, Janis and
Fortelius [1988] demonstrated that larger teeth will
have more rapid wear. No difference was found
between the amount of wear in males and females in
this study, even though males would have larger
teeth. Welsch [1967] reported the opposite of Cousins
[1988] and of this study, concluding that G. b.
beringei have especially worn teeth, but his sample
is unknown, and may now be named G. g. graueri.
Dental Wear in African Apes / 489
Bonobos and western gorillas have the highest
degree of wear on I1, which is significantly greater
than mountain gorillas. This may be due, in part, to
the processing of fruit, stems, and bark, which
requires utilization of the spatulate first incisor.
Kinzey [1984] also found greater incisal wear in
P. paniscus compared to P. t. troglodytes, which he
attributed it to the eating of fibrous plant matter.
The incisal to molar wear comparison confirms the
distinction in wear between those species that process
more food at the anterior of the mouth compared to the
posterior. Pan paniscus, P. t. troglodytes, and G. g.
gorilla have about twice as much wear on their incisors
as they do on their molars. The western lowland gorilla
(G. g. gorilla) eats more fruits than do the eastern
gorilla species. Other studies also reported greater
anterior wear than posterior wear in African apes
[Dean et al., 1992; Kinzey, 1984; Nichols & Zihlman,
2002]. It was expected that Pan as a frugivore would
have greater wear on the incisors compared to the more
folivorous Gorilla because there is evidence that
folivorous primates have more wear on their posterior
teeth compared to frugivores [Welsch, 1967], but the
results here were inconclusive. Mountain gorillas and
eastern lowland gorillas had the lowest ratios, which is
expected from the amount of tough vegetation in their
diet [Elgart-Berry, 2004].
All species had predominantly suboptimal wear,
not supra-optimal, meaning that for most individuals, dentin–enamel junctions were still increasing
and had not reached their peak. The lowland gorilla
species displayed the greatest average wear across
the molars, yet there was only a maximum of 21%
individuals with supra-optimal wear.
A significant (Po0.05) relationship was found
between dental disease and wear overall on each of
the incisors and molars except for the first incisor;
however, the coefficients are all very low. A significant relationship was found for wear and dental
disease in western lowland gorillas and common
chimpanzees. Both species had high amounts of
tooth loss and incidence of caries. In general, wear
is not a good predictor of incidence of dental disease.
The wear rates were opposite what one would
expect from the comparison of the amount of wear,
but can partially be explained by the y-intercept,
which indicates the amount of wear on M1 when M2
comes into occlusion [Benfer & Edwards, 1991].
There is approximately 2.7 years between eruptions
of M1 and M2 and no difference has been found in
eruption times between gorillas and chimpanzees
[Aiello & Dean, 1990; Aiello et al., 1991; Shea, 1983]
even though gorillas grow faster [Shea, 1983]. Eastern lowland gorillas have the highest wear on M1 at
time zero (9.0), while western lowland gorillas are
second highest, at 7.7, which explains why the
amount of wear is greater in these species. Mountain
gorillas have the second lowest amount of wear at
time zero and have low amounts overall.
The wear rates of all African apes are similar,
ranging from 1.1 to 1.49, with bonobos at the high
end of the range followed by central chimpanzees
and mountain gorillas. The lowest wear rates are
found in western chimpanzees and eastern lowland
gorillas. For comparison, the wear rate in three
human populations ranged from 1.06 to 1.43 (mandible and maxilla, respectively) for Indian Knoll, 0.63
to 0.87 for the Campbell Site, and 1.14 to 1.19 for the
Hardin Site [Scott, 1979]. One might attribute a
lower rate in the eastern lowland gorillas to the
enlarged teeth of this species [Benfer & Edwards,
1991; Elgart-Berry, 2000]; however, because eastern
lowland gorillas have a more confined gape than
mountain gorillas [Elgart-Berry, 2000; Taylor, 2003],
they may process less food per chew, which would
lead to a lower wear rate than mountain gorillas.
The presumed tougher diet of Pan paniscus
compared to the other Pan species may be the cause
for the high wear rate in this species, but the rate of
P. paniscus has the largest confidence interval as well.
McCollum [2007] noted that the bonobo sample at the
Royal Museum in Tervuren, which was measured here,
suffered extreme periodontis and premature tooth loss.
The fact that Pan t. troglodytes and P. t. schweinfurthii,
whose diets are similar, do not have more similar wear
is additional evidence that something other than diet is
a factor. Factors that were not measured here and may
be important are the levels of ambient dust and the age
at weaning. Abrasives in a diet are an important factor
in dental wear [Aiello et al., 1991; Ungar et al., 1995]:
the communition of dust and grit accumulations on
plants can be equal to the impact of masticating silica
in grass. Both have caused the evolution of wearresistant teeth [Janis, 1995]. Mountain gorillas start
eating solid food earlier than chimpanzees at Gombe,
but weaning ages of each species are not known [Aiello
et al., 1991 and references therein]. It is also important
to keep in mind that in each individual, wear will be
affected by tooth loss, and that the wear rates are
calculated from juvenile dentition. It is possible that
wear rates of adults would be different.
High wear rates were found where there was a
high incidence of tooth loss. This sample of Pan
paniscus has the greatest amount of tooth loss (27%)
along with a high frequency of dental disease (33%),
and the highest wear rate. Pan t. troglodytes, with a
wear rate second to P. paniscus, has the second
highest percent of individuals with tooth loss (24%).
Mountain gorillas (G. b. beringei) have a high rate
and the highest frequency of dental disease (45%).
Western lowland gorillas (G. g. gorilla) have moderate-to-high rates of wear, and display excessive
quantities of wear: 29% of M1s had no cutting
surfaces remaining. Similar to G .b. beringei and
P. paniscus, they have poor dental health (26% tooth
loss and 28% dental disease).
Eastern lowland gorillas, G. g. graueri, have a
low wear rate, and also have fewer incidence of
Am. J. Primatol.
490 / Elgart
missing teeth (5%) and dental disease (8%) than do
the other species, even though they demonstrate the
greatest quantity of wear of all species on their first
molars. Thirty percent of G. g. graueri molars were
worn down to dentin.
This study neglects to take into account the
wear on the enamel that occurs before dentin is
reached, which would be slightly greater in Pan than
in Gorilla [Kay, 1981; Kono, 2004; Olejiniczak et al.,
2008; Vogel et al., 2008]. It also fails to quantify
additional wear once all the dentin has been exposed:
the maximum amount of wear is 100% of the dentin
in this study. However, quantifying dentin exposure
on a digital image is a more objective method than
utilizing wear stages. Results of this study agree with
McCollum [2007] who also used digital imaging, but
not with earlier studies [e.g., Welsch, 1967], who
fitted wear into stages.
Do gorilla teeth demonstrate current utility and
high performance that suggest adaptation to their
diet? Evidence in this study that gorilla teeth are
durable despite a mechanically demanding diet
includes: teeth are not at an optimum in wear, but
they have yet to reach the optimum and are not past
it. In addition, dental disease cannot be predicted by
dental wear in any species, which indicates that
excessive wear is not causing mechanical senescence
in this sample. On the other hand, gorillas are not
characterized by a high wear rate in comparison to
chimpanzees, and it was postulated that a certain
amount of wear in gorilla teeth would be advantageous to the processing of their diet. Despite their
thinner enamel and more mechanically demanding
diet, gorilla teeth are as durable as chimpanzee teeth
according to the results of this study.
ACKNOWLEDGMENTS
I thank Richard Thorington of the National
Museum of Natural History, Wim Van Neer at the
Musée Royal de L’Afrique Centrale, Tervuren,
Belgium, and Bruce Latimer of the Cleveland
Museum of Natural History for allowing me to access
their material. Finally, I thank two anonymous
reviewers who provided me with much-needed
constructive criticism and good comments.
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