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Brief communication Enamel thickness and durophagy in mangabeys revisited.

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 147:326–333 (2012)
Brief Communication: Enamel Thickness and Durophagy
in Mangabeys Revisited
W. Scott McGraw,1* James D. Pampush,2 and David J. Daegling2
1
2
Department of Anthropology, Ohio State University, Columbus, OH
Department of Anthropology, University of Florida, Gainesville, FL
KEY WORDS
Cercocebus; Lophocebus; dentition; diet
ABSTRACT
The documentation of enamel thickness
variation across primates is important because enamel
thickness has both taxonomic and functional relevance. The
Old World monkeys commonly referred to as mangabeys
have figured prominently in investigations of feeding ecology and enamel thickness. In this article, we report enamel
thickness values for four mangabey taxa (Cercocebus atys,
Cercocebus torquatus, Lophocebus aterrimus, and Lophocebus albigena), offer revised interpretation of the significance
of thick enamel in papionin evolution, and place our new
data in a broader comparative framework. Our data indicate
that all mangabeys have thick enamel and that the values
obtained for Cercocebus and Lophocebus equal or exceed
those published for most extant non-human primates. In
addition, new field data combined with a current reading of
the dietary literature indicate that hard foods make up a
portion of the diet of every mangabey species sampled to
date. Clarification on the relationship between diet and
enamel thickness among mangabeys is important not only
because of recognition that mangabeys are not a natural
group but also because of recent arguments that explain
thick enamel as an evolved response to the seasonal consumption of hard foods. Am J Phys Anthropol 147:326–333,
2012. V 2011 Wiley Periodicals, Inc.
Enamel thickness varies significantly across the primate order (Molnar and Gantt, 1977; Kay, 1981;
Dumont, 1995; Shellis et al., 1998; Smith et al., 2005;
Olejniczak et al., 2008). Understanding its sources of
variation is important because enamel thickness provides both a taxonomic (Martin, 1985; Grine and Martin,
1988; Conroy, 1991; Brunet et al., 1995; Leakey et al.,
2001; Schwartz, 2000; Kono, 2004) and a functional (e.g.,
Molnar and Gantt, 1977; Teaford and Ungar, 2000; Shimizu, 2002; Grine, 2005; Vogel et al., 2008; Constantino
et al., 2009) signal. With regard to the latter, several
authors have argued that the amount of enamel on tooth
crowns is related to the hardness of ingested items. Primates that consume soft foods are probably at low risk
of breaking their teeth during mastication; however,
hard foods likely pose greater dangers to tooth integrity.
One hypothesized mechanism for protecting and prolonging the lifespan of a tooth, either by increasing its
capacity to resist abrasion or by decreasing the likelihood of a fracture, is to increase enamel thickness on the
occlusal surface (Teaford, 2007; Lucas et al., 2008), and
comparative analyses suggest that hard-object feeders
tend to have greater enamel thickness values than do
soft-object feeders (Kay, 1981; Dumont, 1995).
The Old World monkeys commonly referred to as mangabeys have figured prominently in investigations of
feeding ecology and enamel thickness. Kay (1981) calculated relative enamel thickness values from worn teeth
to test whether thick enamel was associated with terrestrial foraging (Jolly, 1970). His sample included the
arboreal Cercocebus (Lophocebus) albigena and predominantly terrestrial Cercocebus torquatus, and in determining that there was no significant difference in M2 enamel
thickness between these mangabeys, Kay argued that
enamel thickness variation was related more to the consumption of hard foods (Molnar and Gantt, 1977) than to
the substrate on which foraging occurred. Dumont
(1995) provided an explicit test of the hard-object feeding
hypothesis by examining enamel thickness and diet in
pairs of primate and chiropteran species that ingested
foods of differing hardness. Dumont (1995) calculated M1
thickness values for a variety of taxa including graycheeked Cercocebus (Lophocebus) albigena and redcapped Cercocebus torquatus mangabeys. She concluded
that the difference in enamel thickness between mangabey species (Table 1) was attributable to the fact that
the former was a hard-object feeder while the latter consumed soft fruit. When these data are compared with M1
thickness values of other taxa (Shellis et al., 1998; Martin et al., 2003; Olejniczak et al., 2008), the relative
thickness of the gray-cheeked mangabey (mean 5 16.85)
is among the highest of all non-human primates (second
only to Cebus apella), whereas the relative thickness
value of the red-capped mangabey (12.89) appears unremarkable by comparison (Table 1). The exceptionally
thick molar enamel of gray-cheeked mangabeys was also
noted by Lambert et al. (2004), who hypothesized that
this dental attribute in Lophocebus albigena was related
to the demands of processing hard foods during fallback
episodes. According to these authors, thick enamel would
be found in any taxon that relies on hard foods during at
C 2011
V
WILEY PERIODICALS, INC.
C
Grant sponsor: National Science Foundation BCS; Grant numbers: 0840110, 0921770, 0922429.
*Correspondence to: W. Scott McGraw, Department of Anthropology, 4064 Smith Laboratory, Ohio State University, 174 West 18th
Ave., Columbus, OH 43210-1106. E-mail: mcgraw.43@osu.edu
Received 23 June 2011; accepted 28 September 2011
DOI 10.1002/ajpa.21634
Published online 19 November 2011 in Wiley Online Library
(wileyonlinelibrary.com).
327
ENAMEL THICKNESS IN MANGABEYS
TABLE 1. Summary of M1 average and relative enamel thickness values
Taxon
Homo sapiens
Cebus apella
Cebus apella
Lophocebus albigena
Cebus capucinus
Papio cynocephalus
Pan troglodytes
Theropithecus gelada
Macaca nemestrina
Pongo pygmaeus
Aotus trivirgatus
Cercocebus torquatus
Pithecia monachus
Trachypithecus cristatus
Alouatta villosa
Nycticebus coucang
Gorilla gorilla
Otolemur gamettii
Lemur catta
Saimiri sciureus
Callithrix jacchus
Hylobates muelleri
Ateles sp.
Pongo pygmaeus
Pan troglodytes
Cercocebus sp.
Ateles geoffroyi
Symphalangus syndactylus
Gorilla gorilla
Alouatta seniculus
Ateles paniscus
Eulemur sp.
a
Tooth
M1
M1
M1
M1
M1
M1
M1
M1
M1
M1
M1
M1
M1
M1
M1
M1
M1
M1
M1
M1
M1
M1
M1
M1
M1
M1
M1
M1
M1
M1
M1
M1
N
7
1
2
2
3
1
3
1
1
1
1
3
1
1
1
1
1
1
1
4
2
4
1
3
5
1
7
5
4
6
1
1
Average enamel
thickness
1.271
0.99
.500 (.001)a
1.17 (0.013)
0.75 (0.074)
0.867
0.808
0.888
0.539
0.85
.208a
1.24 (0.118)
.276a
0.383
0.424
0.221
0.836
0.214
0.217
0.15
0.116
Relative thickness
value or mean (SD)
3D enamel
thickness (SD)
Source
13.62 (1.7)a
12.7
12.6 (0.83)a
11.2 (1.4)a
18.53
10.9 (1.4)a
10.1 (2.05)a
8.9 (1.3)a
8.9 (1.5)a
7.45
7.32
Shellis et al., 1998
Dumont, 1995
Martin et al., 2003
Dumont, 1995
Dumont, 1995
Shellis et al., 1998
Shellis et al., 1998
Shellis et al., 1998
Shellis et al., 1998
Shellis et al., 1998
Martin et al., 2003
Dumont, 1995
Martin et al., 2003
Shellis et al., 1998
Shellis et al., 1998
Shellis et al., 1998
Shellis et al., 1998
Shellis et al., 1998
Shellis et al., 1998
Shellis et al., 1998
Shellis et al., 1998
Olejniczak et al., 2008
Olejniczak et al., 2008
Olejniczak et al., 2008
Olejniczak et al., 2008
Olejniczak et al., 2008
Olejniczak et al., 2008
Olejniczak et al., 2008
Olejniczak et al., 2008
Olejniczak et al., 2008
Olejniczak et al., 2008
Olejniczak et al., 2008
a
19.84
21.36
18.845 (.671)a
16.85 (.530)
15.13 (1.587)
15.104a
14.587a
13.897a
13.462a
12.248a
12.05a
12.89 (1.659)
11.81a
11.939a
11.988a
10.315a
9.39a
9.243a
8.115a
8.492a
8.769a
Calculated from published data.
least some portion of the year, assuming no ecological
mismatch (e.g., Cuozzo and Sauther, 2006; Millette et
al., 2009).
Hard-object feeding has been described in mangabeys
since the first field studies on these monkeys (Haddow,
1952; Chalmers, 1968; Jones and Sabater Pi, 1968; Kingdon, 1971; Quiris, 1975; Waser, 1975, 1984; Homewood,
1978), and several authorities have linked mangabey
dental features, including large incisors and thick molar
enamel, with durophagous tendencies (Kingdon, 1971;
Hylander, 1975; Kay, 1981, 1984). However, since the
publication of these early studies, our understanding of
mangabey taxonomy, ecology, and behavior has changed
significantly. The term ‘‘mangabey’’ now refers to monkeys from two clades: arboreal mangabeys are placed in
the genus Lophocebus and are most closely related to
Papio and Theropithecus while the more terrestrial mangabeys comprise Cercocebus, which is the sister taxon of
Mandrillus (Groves, 1978; Disotell et al., 1992; Harris
and Disotell, 1998; Fleagle and McGraw, 1999, 2002;
Gilbert, 2007).
The recognition of mangabey diphyly combined with
new information on the foods and feeding habits of several Cercocebus taxa (Shah, 2003; Wieczkowski, 2009;
Cooke and McGraw, 2010; Devreese, 2011; McGraw et
al., 2011) prompted us to revisit what is known about
enamel thickness in several mangabey taxa from different clades. The purpose of this brief report is to provide
new enamel thickness values for four mangabey taxa, to
clarify points raised in the original article by Dumont
(1995) concerning diets and enamel thickness of mangabeys generally, and to place these data in a comparative
framework. In addition to establishing new benchmarks
for enamel thickness in anthropoids, we also clarify the
relationship between feeding behavior and enamel thickness in Cercocebus and Lophocebus generally. We justify
our investigation as these new data bear on recent arguments concerning the evolution of thick enamel in
response to the consumption of mechanically protected
fallback foods (Lambert et al., 2004; Constantino et al.,
2009).
METHODS
We obtained average and relative enamel thickness
values for unworn or lightly worn M2s from one graycheeked mangabey Lophocebus albigena, one red-capped
mangabey Cercocebus torquatus, and one black mangabey Lophocebus aterrimus. Although some authors (e.g.,
Dumont, 1995) have sampled teeth and/or tooth sections
with exposed dentine by reconstructing the enamel cap
from the outline of the enamel dentine junction (EDJ),
we excluded tooth sections with exposed dentine from
our sample. Research on EDJ topography and enamel
surface contours in humans and extinct hominins has
shown the EDJ to be an unreliable guide to reconstructing enamel cap topography (Schwartz et al., 1998).
Each tooth was cleaned and fixed using cyanoacrylate
(to prevent chipping) and coronally sectioned with a diamond-wafering blade on a Buehler-Isomet low-speed
American Journal of Physical Anthropology
328
W.S. MCGRAW ET AL.
Fig. 1. Occlusal surface of Cercocebus torquatus right M2. 1
5 exposed dentine on protoconid; 2 5 sampling plane of section.
[Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]
saw. The Lophocebus albigena and Lophocebus aterrimus
teeth were sectioned through both the mesial (protoconid-metaconid) and distal (hypoconid-entoconid) cusp
pairs. Because the Cercocebus torquatus tooth had
exposed dentine on the protoconid (Fig. 1), only the distal cusp pair was sampled in this specimen.
Exposed sections were gently scoured with 0.5% phosphoric acid to enhance the boundary between the enamel
and dentine. Each cut generated two exposed faces, and
digital photographs were taken of each face and processed in ImageJ (Abramoff et al., 2004) to obtain the
measures of combined dentine/pulp area (b), enamel cap
area (c), and length of EDJ (e) (Fig. 2). Following Martin
(1985), we averaged the measures over each tooth and
used these measures to calculate two values of enamel
thickness: 1) average enamel thickness [AET
5 c/e] and
p
2) relative thickness [RET 5 (c/e 3 100)/ b]. The values
we report are averages of measurements gathered by
David Daegling and James Pampush (DJD and JDP),
which regression analysis shows high interobserver consistency (T 5 44.212, P \ 0.001, R2 5 0.981). These
data, as well as those collected from three Cercocebus
atys specimens measured earlier (Daegling et al., 2011),
are compared with values of various primates compiled
from the literature (Shellis et al., 1998; Martin et al.,
2003; Olejniczak et al., 2008).
RESULTS
M2 relative enamel thickness values for Lophocebus
aterrimus (n 5 1), Lophocebus albigena (n 5 1), Cercocebus torquatus (n 5 1), and Cercocebus atys (n 5 3) are
presented in Table 2 along with comparative M2 data
from the literature (Shellis et al., 1998; Martin et al.,
2003; Olejniczak et al., 2008). For discussion purposes,
the taxa are arranged in the order of increasing magnitude of relative enamel thickness. Our study is obviously
sample-limited; however, the single or mean values we
obtained for the four mangabey taxa equal or exceed
those of all extant primates measured except for Cebus
apella, Homo sapiens, and Daubentonia madagascarienAmerican Journal of Physical Anthropology
Fig. 2. Mesial face of coronal section through the hypoconidentoconid cusp pair of a right M2 of Cercocebus torquatus. c 5
enamel cap; e 5 enamel dentine junction (outlined with dashed
line); b 5 dentine/pulp area (hemmed by dashed and solid line).
[Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.]
sis. To state in another way, of the six extant primate
taxa with thickest M2 enamel, four are mangabey species. In addition, the M2 thickness value obtained for
Cercocebus torquatus was greater than that obtained for
Lophocebus albigena, a finding opposite of that reported
for first molars in these taxa (Table 1; Dumont, 1995).
These data indicate that all mangabeys have thick
enamel and that the values obtained for mangabeys in
both clades rank among the highest published values for
extant primates (Table 2).
DISCUSSION
Primates that consume hard foods tend to have thick
enamel (Ungar, 2008). Thus, two species differing in the
hardness of their diets are expected to differ in their relative enamel thickness with thicker enamel predicted in
the taxon that consumes more obdurate items. This
hypothesis was tested by Dumont (1995) in her comparative study of paired chiropteran and primate taxa including two mangabey species. Dumont (1995) obtained an
M1 relative thickness mean of 16.85 for Cercocebus
(Lophocebus) albigena and 12.89 for Cercocebus torquatus. Although not statistically significant, Dumont concluded that the difference in enamel thickness was
attributable to the fact that Lophocebus albigena was a
hard-object feeder, whereas Cercocebus torquatus was a
soft-object feeder. We suggest that this dietary dichotomy
does not accurately describe the feeding habits of these
monkeys, nor do our data support the interpretation
that Lophocebus albigena and Cercocebus torquatus differ in relative enamel thickness. Our reading of the literature, combined with new data on mangabey feeding
behavior and M2 enamel thickness, leads us to conclude
329
ENAMEL THICKNESS IN MANGABEYS
TABLE 2. Summary of M2 average and relative enamel thickness values
Taxon
Cebus apella
Homo sapiens
Lophocebus aterrimus
Cercocebus torquatus
Daubentonia madagascariensis
Homo sapiens
Lophocebus albigena
Cercocebus atys
Cebus apella
Macaca nemestrina
Pongo pygmaeus
Hylobates muelleri
Papio sp.
Theropithecus gelada
Macaca mulatta
Ateles geoffroyi
Papio cynocephalus
Callicebus moloch
Erythrocebus patas
Pan troglodytes
Alouatta pigra
Trachypithecus cristatus
Cercopithecus mona
Pan troglodytes
Symphalangus syndactylus
Chiropotes satanas
Propithecus diadema
Alouatta sp.
Gorilla gorilla
Cacajao calvus
Saimiri sciureus
Perodicticus potto
Alouatta seniculus
Eulemur sp.
Gorilla gorilla
Callithrix jacchus
Galago
a
b
Tooth
N
Average thickness
value or mean (SD)
Relative thickness
value or mean (SD)
Source
M2
M2
M2
M2
M2
M2
M2
M2
M2
M2
M2
M2
M2
M2
M2
M2
M2
M2
M2
M2
M2
M2
M2
M2
M2
M2
M2
M2
M2
M2
M2
M2
M2
M2
M2
M2
M2
1
9
1
1
1
9
1
3
1
1
3
4
2
3
3
9
1
1
2
10
1
1
1
1
9
2
1
1
4
1
1
1
7
1
1
1
1
0.65
1.46 (0.49)
0.787
1.026
0.408
1.236
0.785
0.826 (0.049)
0.486
0.732
1.156 (0.228)
0.5 (0.1)
0.995 (0.289)
1.107
0.546
0.411 (0.063)
0.598
0.259
0.479
0.756 (0.056)
0.54
0.428
0.379
0.725
0.553 (0.09)
0.223 (0.004)
0.342
0.4
1.05 (0.18)
0.279
0.159
0.179
0.397 (0.065)
0.24
0.827
0.11
0.12
23.6
23.4 (8.4)
22.849
22.667
21.685b
20.756b
19.799
19.664 (2.416)
19.211b
17.177b
16.3 (2.3)
14.3 (2.1)
14.9 (2.6)
14.67b
13.149b
12.6 (1.7)
12.44b
12.32
12.298b
11.7 (1.1)
11.64
11.443b
11.294b
11.219b
11.02 (1.9)
10.35 (0.784)
10.251b
10.09
9.9 (1.6)
9.84
9.659b
9.356b
9.2 (1.1)
9.2
8.791b
8.109b
6.33
Olejniczak et al., 2008a
Olejniczak et al., 2008a
This study
This study
Shellis et al., 1998
Shellis et al., 1998
This study
Daegling et al. (2011)
Shellis et al., 1998
Shellis et al., 1998
Olejniczak et al., 2008a
Olejniczak et al., 2008a
Olejniczak et al., 2008a
Shellis et al., 1998
Shellis et al., 1998
Olejniczak et al., 2008a
Shellis et al., 1998
Martin et al., 2003
Shellis et al., 1998
Olejniczak et al., 2008a
Olejniczak et al., 2008a
Shellis et al., 1998
Shellis et al., 1998
Shellis et al., 1998
Olejniczak et al., 2008a
Martin et al., 2003
Shellis et al., 1998
Olejniczak et al., 2008a
Olejniczak et al., 2008a
Martin et al., 2003
Shellis et al., 1998
Shellis et al., 1998
Olejniczak et al., 2008a
Olejniczak et al., 2008a
Shellis et al., 1998
Shellis et al., 1998
Olejniczak et al., 2008a
Olejniczak et al. (2008) reported raw 3D AET and RET values, which were used here to generate the reported M2 data.
Relative thickness values derived from data in Shellis et al., 1998.
that all mangabey taxa process hard objects to varying
degrees and that all mangabeys have thick enamel
(Table 2; Fig. 3).
In contrasting the diets of Cercocebus (Lophocebus)
albigena and Cercocebus torquatus, Dumont (1995) cited
three sources: Chalmers (1968), Waser (1977), and Kingdon (1974). Both Chalmers (1968) and Waser (1977) discussed the diets of Lophocebus albigena and both
referred to hard-object feeding in this taxon. Neither article makes reference to Cercocebus torquatus. The third
cited source (Kingdon, 1974) is a large volume that discusses the feeding habits of many African monkeys
including Lophocebus albigena; however, we find no
mention of soft-object feeding by Cercocebus torquatus in
this book. On the basis of the information obtained in
these sources, we find no justification for characterizing
Cercocebus torquatus as a soft-object frugivore other
than Dumont’s (1995) pronouncement to this effect.
A significant body of information on mangabey feeding
has accumulated since Dumont’s (1995) article, including
important information on the diet and foraging behavior
of Cercocebus torquatus. Recent fieldwork in Sette Cama,
Gabon indicates that red-capped mangabeys consume significant quantities of obdurate foods, including a large
percentage of Sacoglottis gabonensis seeds (Cooke et al.,
2009; Cooke and McGraw, 2010). These seeds, which can
remain on the ground for months without rotting, are
also a major contributor to the diet of Cercocebus atys in
the Ivory Coast’s Taı̈ Forest (McGraw et al., 2011). Material properties tests have shown that this seed, in addition to being very tough, has a fragmentation index value
that exceeds those of popcorn kernels and prune pits
(Fig. 4) and can therefore be described as stress-limited
because fragmentation index values correlate positively
with hardness (McGraw et al., 2011). The diet of the agile
mangabey Cercocebus agilis includes mechanically resistant seeds and nuts (Shah, 2003; Devreese, 2011), and
Kenya’s Tana River mangabey Cercocebus galeritus feeds
on many foods with puncture resistance scores that fall
within the hardness range of other primates described as
hard-object feeders (Homewood, 1978; Wahungu, 1998;
Wieczkowski, 2009). We do not yet have detailed accounts
of the diet or food material properties of the sanje mangabey, Cercocebus sanjei; preliminary information suggests
that this taxon also feeds in part on hard seeds and nuts,
some of which are collected from the forest floor (Ehardt
et al., 2005; Mwamende, 2009; C. Ehardt, unpublished
data cited in Wieczkowski, 2009). Given the recurrent
theme of hard-object feeding throughout these studies
and accepting the premise that selection should favor
American Journal of Physical Anthropology
330
W.S. MCGRAW ET AL.
Fig. 3. Means and 95% confidence limits for M2 relative
enamel thickness. Species means reported in Table 2 are used
in the confidence interval calculation. Datum for Homo uses the
mean reported by Shellis et al. (1998); those for Pan troglodytes
and Gorilla gorilla use means reported by Olejniczak et al.
(2008) owing to larger sample sizes for these taxa in the respective studies. The Cebus apella datum averages the values
reported in Shellis et al. (1998) and Olejniczak et al. (2008). The
approach of the upper confidence limit in hominoids and prosimians to the lower confidence limit of the mangabeys is driven
by high outlying values in Homo and Daubentonia, respectively.
Other cercopithecoids 5 Macaca nemestrina, Papio sp., Theropithecus gelada, Macaca mulatta, Papio cynocephalus, Erythrocebus patas, Trachypithecus cristatus, Cercopithecus mona. Hominoids 5 Homo sapiens, Pongo pygmaeus, Hylobates muelleri,
Pan troglodytes, Symphalangus syndactylus, Gorilla gorilla.
Ceboids 5 Cebus apella, Ateles geoffroyi, Callicebus moloch,
Alouatta pigra, Chiropotes satanas, Alouatta sp., Cacajao calvus, Saimiri sciureus, Alouatta seniculus, Callithrix jacchus.
Prosimians 5 Daubentonia madagascariensis, Propithecus diadema, Perodicticus potto, Eulemur sp., Galago.
thick enamel even if hard objects are consumed only during fallback episodes, all Cercocebus taxa are expected to
have thick molar enamel.
The feeding habits of Lophocebus albigena have been
well studied at several sites and consumption of seeds
and nuts, including hard ones, is associated with graycheeked mangabey feeding at all localities (e.g., Chalmers, 1968; Waser, 1977; Olupot, 1988; Tutin et al., 1997;
Poulsen et al., 2001; Lambert et al., 2004). The feeding
behavior of the black mangabey, Lophocebus aterrimus,
is much less well known; however, the single long-term
study indicates that this species—like its congener—consumes a significant portion of seeds and nuts (Horn,
1987). Hardness data on black mangabey foods have not
yet been collected; however, given their ecological similarity to gray-cheeked mangabeys (Kingdon, 1997; GautierHion et al., 1999), as well as the similar geometry of
their mandibles and teeth (Groves, 1978; Daegling and
McGraw, 2007), we predict that the black mangabey diet
contains mechanically resistant foods. It is very likely
that both members of Lophocebus are hard-object feeders,
and if this is accurate, both should have thick enamel.
Based on a current reading of the literature, hard
foods make up a portion of the diet of every mangabey
species from both clades. We recognize that there is significant variation in the amount and frequency with
which hard objects are consumed by different mangabey
species; however, we feel it is unwise to characterize any
mangabey as a ‘‘soft-object feeder,’’ least of all members
American Journal of Physical Anthropology
Fig. 4. Fragmentation index Sacoglottis gabonesis compared
with other hard foods. This seed, which can be described as
stress limited, is frequently consumed by at least two mangabey
species: Cercocebus torquatus and Cercocebus atys. Comparative
data from Williams et al. 2005.
of Cercocebus (cf. Dumont, 1995). Indeed, for taxa such
as Cercocebus atys and Cercocebus torquatus, the
percentage of hard objects in the annual diet is considerable. For example, in the Ivory Coast’s Taı̈ Forest,
Sacoglottis gabonesis seeds are the most stress-limited
items consumed by sooty mangabeys and are also the
most frequently consumed food annually and during
every month of the year (McGraw et al., 2011). Given
that all mangabeys appear to be durophagous and possess
relatively thick molar enamel (Fig. 3), we question both
the premise and conclusions of Dumont’s (1995) argument.
Clarification on the relationship between diet and
enamel thickness among mangabeys is important not
only because of recognition that mangabeys are not a
natural group but also because of the role mangabeys
have played in understanding those factors responsible
for the extent that enamel thickness varies across all
primates. This is especially true with respect to recent
arguments relating the evolution of thick enamel to the
seasonal consumption of hard foods. Lambert et al.
(2004) produced an influential article that compared the
diets and food hardness values of two Ugandan monkeys
that differed in molar enamel thickness. These authors
demonstrated that while there was significant diet overlap, the thick-enameled gray-cheeked mangabey (Lophocebus albigena) consumed several foods—hard seeds and
bark—that the thin-enameled redtail monkey (Cercopithecus ascanius) did not. Because hard foods were not
consumed frequently by Lophocebus albigena, the
authors concluded that the thick enamel found in graycheeked mangabeys was selected for not as a response to
‘‘habitual’’ hard-object processing, but in order to withstand stress resulting from processing hard foods during
less frequent, but critical, fallback episodes when preferred resources were not available. In the author’s
words, ‘‘it is not so much what is consumed most commonly (i.e., soft, fleshy fruit) that selects for enamel
thickness, but the hardness of foods that are consumed
infrequently’’ (Lambert et al., 2004; p 367).
Lambert et al. (2004; p 363) citing data from Kay
(1981) stated that ‘‘Lophocebus albigena has among the
thickest molar enamel of any extant primate.’’ We agree,
but note that gray-cheeked mangabey molar enamel is
not exceptionally thick when compared with all other
ENAMEL THICKNESS IN MANGABEYS
331
fessor Bassirou Bonfoh. For permission to work in the
Taı̈ Forest, the authors thank the Ministere de
l’Enseignement Superieur et de la Recherche Scientifique et de l’Innovation Technologie and the Ministere de
l’Environment, des Eaux et Forets, Office Ivorien de
Parcs et Reserves. They also thank the members of the
Taı̈ Monkey Project, especially Mr. Richard Paacho and
the TMP field coordinator, Dr. Anderson Bitty. All
research activities were carried out under approved
IACUC protocols from the Ohio State University and the
University of Florida.
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Fig. 5. Relative enamel thickness values of mangabey species compared with other papionins. Points represent group
means or single values and error bars are 95% confidence intervals. All taxa represented by single specimens except Cercocebus atys (n53).
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al., 2011). We also recognize that we have not discussed
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Lophocebus and Cercocebus awaits examination of ancestral papionins such as Procercocebus (Gilbert, 2007) and
Parapapio (Freedman, 1957). Such an exercise would
help to elucidate the evolutionary plasticity of this important feature (e.g., Hlusko et al., 2004; Kelley and
Swanson, 2008).
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