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Dental microwear and diet in Venezuelan primates.

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AMERICAN JOURNAL. OF PHYSICAL ANTHROPOLOGY 88:347-364 (1992)
Dental Microwear and Diet in Venezuelan Primates
MARK F. TEAFORD AND JACQUELINE A. RUNESTAD
Department of Cell Biology and Anatomy, The Johns Hopkins University
School of Medicine, Baltimore, Maryland, 21205
KEY WORDS
Scanning electron microscopy, Tooth abrasion,
Ceboidea, Alouatta, Ateles, Aotus, Chiropotes, Pithecia, Cebus,
Saimiri
Recent microwear analyses have demonstrated that wear
ABSTRACT
patterns can be correlated with dietary differences. However, much of this
work has been based on analyses of museum material where dates and locations of collection are not well known. In view of these difficulties, it would be
desirable to compare microwear patterns for different genera collected from
the same area at the same time.
The opportunity to do this was provided by the collections of the Smithsonian Venezuelan Project (Handley, 19761, in which multiple primate genera
were collected from the same humid tropical forest sites within the same
month. The monkeys represent a wide range of dietary preferences, and
include Saimiri, Cebus, Chiropotes, Ateles, Aotus, Pithecia, and Alouatta.
As in previous microwear analyses, epoxy replicas were prepared from
dental impressions, as described by Rose (1983) and Teaford and Oyen (1989).
Two micrographs were taken of facet 9 on an upper second molar of each
specimen. Computations and analyses were the same as described by Teaford
and Robinson (1989).
Results reaffirm previously documented differences in dental microwear
between primates that feed on hard objects versus those that do not-with
Pithecia and Alouatta at the extremes of a range of microwear patterns including more subtle differences between species with intermediate diets. The
subtle microwear differences are by no means easy to document in museum
samples. However, additional results suggest that 1) the width of microscopic
scratches may be a poor indicator of dietary differences, 2) large and small pits
may be formed differently, and 3) there are very few seasonal differences in
dental microwear in the primates at these humid tropical forest sites.
0 1992 Wiley-Liss, Inc.
Dental microwear analysis is a relatively
new source of information about dental
function in prehistoric mammals (Grine,
1986; Grine and Kay, 1988; Harmon and
Rose, 1988; Kelley, 1986; Puech et al., 1980,
1983; Rensberger, 1978, 1986; Robson and
Young, 1990; Rose et al., 1981; Ryan and
Johanson, 1989; Solounias et al., 1988;
Teaford, 1991, in press; Teaford and Walker,
1984;Van Valkenburgh et al., 1990; Walker,
1981; Walker et al., 1978). As such, it holds
much promise, but some difficulties still remain. One problem is that while analyses of
0 1992 WILEY-LISS, INC.
fossil material are ultimately dependent
upon comparisons with modern teeth, most
work on modern teeth (e.g., Ryan, 1981;
Teaford, 1985,1988; Teaford and Robinson,
1989; Ungar 1990; Van Valkenburgh et al.,
1990) has utilized museum collections
where dates and locations of collection are
not always well-known. This information
can be of critical importance for interpretations of dental microwear-especially in
Received October 30,1990; accepted December 31,1991.
348
M.F. TEAFORD AND J.A. RUNESTAD
analyses of closely-related species or species
with similar diets (Gordon, 1984b; Kelley,
1990; Teaford, 1991; Teaford and Glander,
1991). Teaford and Robinson (1989) have
even suggested that seasonal differences in
diet within species may lead to recognizable
differences in molar microwear, although
only in samples from ecological life zones
with significant seasonal variation in resource availability. This should come as no
surprise, because seasonal variations in resource availability have already been shown
to lead to seasonal variations in the proportion of different dietary components in certain species (Davies, 1984; Glander, 1981;
Robinson, 1986). Moreover, recent research
indicates that the physical properties of
many food items are extremely complicated
- physical properties may differ within single food items, and those of certain foods
may even change between seasons (Kinzey,
1990; Kinzey and Norconk, 1990; Lucas,
1989; Lucas and Corlett, 1991; van Roosmalen, 1984; van Roosmalen et al., 1988).
All the above complexities pinpoint another
weakness of dental microwear analyses: the
limited range of species examined to date.
For New World primates, small numbers of
Ateles, Cebus, and Chiropotes have been examined (Kay, 1987; Teaford, 1985, 1988;
Teaford and Walker, 19841, but only Cebus
nigrivittatus and Alouatta palliata have received anything close to a thorough examination (Teaford and Glander, 1991; Teaford
and Robinson, 1989).
If dental microwear analyses are to live up
to their potential, then we must have a better grasp of variations in diet and dental
microwear in modern mammals. Without
such knowledge, we will surely lose information through oversimplification of diet, microwear, or both. As a n example, recent
work with laboratory primates (Teaford and
Oyen, 1989b,c) suggests that not all microscopic pits on teeth are formed in the same
manner. Small pits may be formed by strict
tooth-on-tooth wear, whereas large pits may
be caused by the compression of hard objects
between enamel surfaces. This hypothesis
may be supported by Robson and Young’s
(1990) discovery that trailing edges of facets
show more pits than leading edges on marsupial carnassial teeth. Citing Gordon’s
(1982, 1984b) model of scratch and pit formation, together with Osborn and Lumsden’s (1978) model of carnassial biting, Robson and Young suggest that changes in
carnassial orientation during the chewing
stroke should lead to relatively more shear
at the leading edge and relatively more compression a t the trailing edge. However, another factor to consider is that, for any given
facet, tooth-tooth contact (and thus toothon-tooth wear) is probably more likely to occur at the trailing edge-after the tooth has
sliced through a piece of food. One of us
(M.T.) has occasionally observed similar differential pitting on human molar wear facets. Since human molars are unlikely to undergo the degree of tilting hypothesized for
carnassials, tooth-on-tooth wear might be
an additional explanation for the formation
of small pits.
The purpose of this study is to use a welldocumented museum collection to expand
our database of dental microwear patterns
in modern New World monkeys. In the process, we hope to shed new light on the relationship between dental microwear and
diet.
MATERIALS AND METHODS
Materials
The material collected by the Smithsonian
Venezuelan Project (SVP) (Handley, 1976)
seemed ideally suited for this study for a
number of reasons. First, multiple primate
genera were collected during the same time
period from the same site, allowing a n unusually high degree of control over habitational, seasonal, and taxonomic variables.
Second, the SVP collection allowed expansion of our comparative database a s the
monkeys sampled include sizable numbers
of Saimiri sciureus, C . nigriuittatus, Chiropotes satanas, Ateles belzebuth, Aotus trivirgatus, Pithecia pithecia, and Alouatta seniculus. Third, previous studies (Kay, 1987;
Teaford, 1985; Teaford and Robinson, 1989)
had already shown that the teeth in this
collection were generally suitable for microwear analyses.
Specimens utilized had been collected
within two-month time spans during 19661967 from four humid tropical forest sites
DENTAL MICROWEAR IN VENEZUELAN PRIMATES
349
(Holdridge, 1971) in Venezuela. Cebus, Aotus, Saimiri, Ateles, Alouatta and Chiropotes
were sampled during June and July of 1967
from the site known as Rio Manapiare (near
San Juan; latitude 5”, 18‘ north; longitude
66“) 13’ west); Cebus and Pithecia during
June and July of 1966 from the site known
as El Manaco (6“,17’ north; 61”, 19‘ west);
Saimiri, Ateles, and Chiropotes during
March and April of 1967 from the site known
as Rio Mavaca (near Esmeralda; 2”, 15’
north; 65”,17‘ west); and Cebus and Chiropotes during January and February of 1967
from the site known as Rio Cunucunuma
(near Belen; 3”, 39’ north; 65”, 46’ west).
Thus, at each site there was one species
(either Chiropotes or Pithecia) known to be
both a seed-predator and a consumer of
large amounts of fruit (Ayres, 1989; Buchanan et al., 1981; Happel, 1982; Kinzey,
1989, 1990; Kinzey and Norconk, 1990;
Kinzey et al., 1990; Mittermeier and van
Roosmalen, 1981; Norconk and Kinzey,
1990; Setz, 1987; van Roosmalen et al.,
1981, 1988). Each site also had at least one
species with a more variable diet. From the
sites known as El Manaco and Rio Cunucunuma, the other species was C. nigrivittatus, a species known to eat mainly ripe fruit
and invertebrates, as well as hard objects on
occasion (Robinson, 1986). Along with Chiropotes, species from Rio Mavaca includedA.
belzebuth and S. sciureus. Ateles is known to
feed mainly on ripe fruits and occasionally
on leaves (Klein and Klein, 1977; Robinson
and Janson, 1986>, while Saimiri feeds
mainly on insects (Mittermeier and van
Roosmalen, 1981; Terborgh, 1983). From
Rio Manapiare, a diverse assortment of primates included A. trivirgatus and A. seniculus, in addition to Chiropotes satanas, A. belzebuth, C. nigriuittatus, and S. sciureus. A.
trivirgatus has a varied diet including large
amounts of fruit supplemented by insects,
flowers, and leaves (Robinson et al., 1986;
Wright, 1985, 1989); whereas A. seniculus
feeds mainly on fruit and leaves (Crockett
and Eisenberg, 1986; Gaulin and Gaulin,
1982).
Rose (1983) and Teaford and Oyen (1989a).
Thus, in each case, an addition-curing dental impression material was used to take the
impression (either “Express, Light Body,
Regular Set,” 3M, or “President Jet Regular,” Coltene), and each impression was then
poured with epoxy (either (‘Araldite,”CibaGeigy, or “Epoxydent,” Oxy Dental Products) to make a positive cast.’
The epoxy casts were sputter-coated with
approximately 200 A of gold and examined
in an AMRAY 1810 scanning electron microscope in secondary emissions mode. Methods of SEM data collection were essentially
the same as those described by Teaford and
Walker (1984). However, in this study micrographs were only taken of crushing facets
on M2 of each specimen. As cusp tip facets
may obliterate crushingrgrinding facets during the course of tooth wear (Gordon, 1988;
Teaford, 1988) and cusp tip facets may exhibit dental microwear patterns intermediate between those on shearing and crushing/
grinding facets (Gordon, 1982, 1984b), most
micrographs for this study were taken on
facet 9, near the base of the protocone. The
only exceptions involved 2 specimens of
Pithecia, where there was a curious absence
of facets in the central basin. In such cases,
the cusp tip facet of the protocone was used.
These procedures were also meant to minimize the effects of possible intrafacet differences in dental microwear (Robson and
Young, 1990; Teaford, 1988). For each individual, two micrographs that appeared to be
representative were taken of different areas
on the facet a t magnification of 500 x . Each
micrograph covered an area of approximately .03 mm2. All of the microwear features within each micrograph were measured in microns, by using a digitizer
controlled by a minicomputer system. Thus,
for each micrograph, the total number of features was recorded and the maximum
length and width of each feature were digitized.
Data collection
‘All “Express” impressions were taken with the hydrophobic
form of this impression material. 3M has since stopped making
it. The newer, hydrophilic version of “Express”has given us problems with “pitting“ artifacts (Gordon, 1984a) and poor resolution
of detail when poured with industrial epoxies such a s “Araldite.”
Each specimen was cleaned and replicated using the techniques described by
M.F. TEAFORD AND J.A. RUNESTAD
350
Data analysis
As in previous studies (Gordon, 1982;
Grine, 1986; Teaford, 1985, 1986;Teaford
and Robinson, 1989; Teaford and Walker,
19841,the ratio of the maximum length to
the maximum width of each microwear feature was used to categorize that feature a s
either a pit or a scratch. To avoid the problem of short scratches being categorized as
pits (Teaford, 1985, 19881, a 4:l length:width ratio was used to distinguish between pits and scratches.
Since individual microwear features probably cannot be treated as independent
events (Teaford, 1988; Teaford and Oyen,
1989c),statistical analyses centered around
the use of mean values (for various microwear measurements) computed for each
individual. In other words, for each individual, data from each pair of micrographs
were pooled to yield the following measurements for each specimen: 1) average number
of features per micrograph, 2) percentages of
pits (and scratches), 3)average width of pits,
and 4)average width of scratches. As large
pits may be formed differently than small
pits, we also recorded the proportion of total
features that were small pits and large pits.
Since prism boundaries might serve a s
points of weakness in the enamel (Maas,
1988,1991),wear caused by tooth-tooth contacts might yield pits roughly the same size
as prisms. While we currently know far too
little about variations in the enamel microstructure of primates (Boyde and Martin,
1982, 1984), a pit width of 4 microns was
used as the cut-off between large and small
pits in this study because we felt this was a
reasonable approximation of prism size in
New World monkeys, based on published
micrographs (Martin et al., 1988).A variance stabilizing transformation (the arcsine
transformation) was performed on all proportions before the computation of any statistics. Since the length of features was frequently truncated by the small size of field
of view (Teaford and Walker, 1984),feature
lengths were only used in the categorization
of pits and scratches.
To compare microwear measurements between genera at Rio Mavaca and Rio Manapiare, we used a combination of single-factor
analysis of variance and a multiple comparison test (the Student-Newman-Keuls test)
(Zar, 1974:151-155).These techniques were
also used in comparisons between genera for
the entire sample (ignoring collection sites).
A nested analysis of variance was not used
due to drastic differences in sample size
within and between sites (Sokal and Rohlf,
1981:293-308).For samples from El Manaco
and Rio Cunucunuma (where only two genera were available per site) we used the
Mann-Whitney test (Zar, 1974:109-1 13).
This technique was also used in intergeneric
comparisons of species collected in different
seasons, a s samples from two of the sites
(Rio Mavaca and Rio Cunucunuma) were
collected during the dry season, while the
remaining samples were collected during
the wet season (Ewe1et al., 1976).Finally, to
begin to understand the interaction of
causal factors in the development of dental
microwear patterns, two-way analyses of
variance were run for three comparisons: (1)
microwear patterns exhibited by Ateles,
Saimiri, and Chiropotes at the sites of Rio
Mavaca and Rio Manapiare; ( 2 ) microwear
patterns exhibited by Chiropotes and Cebus
atRio Cunucunuma and Rio Manapiare; and
(3)microwear patterns exhibited by Ateles,
Cebus, Chiropotes, and Saimiri from wet
and dry sites. Through these ANOVAs we
hoped to gain a different perspective on the
effects of site, genus, and/or season on dental microwear patterns. We also hoped to see
if there were any significant interactions between site and genus or between genus and
season. For example, the effects of genus
might vary between sites. In all statistical
analyses, only P-values less than 0.05were
considered significant.
Our overall expectation was that it would
be easiest to demonstrate microwear differences between genera from specific sites and
dates of collection a s these comparisons
would minimize geographical and seasonal
variations in diet and dental microwear. In
these cases, we expected that hard object
feeders, such as Chiropotes and Pithecia
(Apes, 1989;Buchanan et al., 1981;Happel,
1982;Kinzey, 1989, 1990;Kinzey and Norconk, 1990;Kmzey et al., 1990;Mittermeier
and van Roosmalen, 1981; Norconk and
Kinzey, 1990; Setz, 1987; van Roosmalen
DENTAL. MICROWEAR IN VENEZUELAN PRIMATES
et al. 1981, 1988), would have a higher incidence of pitting on their molars than soft
object feeders, such as Alouatta (Crockett
and Eisenberg, 1986; Gaulin and Gaulin,
1982). However, if small pits are formed
differently than large pits, then we might
also expect soft fruit eaters like Alouattu
(Crockett and Eisenberg, 1986; Gaulin and
Gaulin, 1982) and Ateles (Klein and Klein,
1977; Robinson and Janson, 1986) to
show relatively high frequencies of small
pits. We did not know what microwear patterns t o expect for Saimiri as no previous
microwear work had been done with insect
eaters (Mittermeier and van Roosmalen,
1981; Terborgh, 1983). Likewise, it was unclear what microwear patterns might be
found on the teeth of Aotus. Given the
high proportion of fruit in its diet (Robinson
et al., 1986; Wright, 1985, 19891, one might
expect a varied assortment of pits on its
teeth, but only if other food items (or abrasives on food items) did not have a disproportionate effect on microwear patterns
(Solounias et al., 1988; Van Valkenburgh
et al., 1990).
We expected interpretations to be more
difficult if we ignored the sites of collection
and merely compared microwear patterns
between all available genera, since seasonal
or geographical differences in diet and dental microwear might introduce just enough
variation to complicate matters. Still, as the
humid tropical forest has relatively little
seasonal variation in resource availability
(Foster, 1980; Leigh et al., 19821, we expected to find very few seasonal differences
in dental microwear (Teaford and Robinson,
1989).
RESULTS OF MOLAR MICROWEAR
COMPARISONS
El Manaco (Pithecia pithecia and
Cebus nigriviffatus)
Pithecia had significantly greater proportions of pits, small pits, and large pits, but
average pit width was significantly larger in
C‘ebus (Table 1, Figs. 1,2).
351
I
352
M.F. TEAFORD AND J.A. RUNESTAD
l2
11
10
c
-
9 8 7 -
6 5 -
,
Cebus
nigrivitrarus
-FT
4 -
312"
0.2
'
I
'
0.5
0.6
0.7
Arcsine Transformation of % Pits
(mean and s. d.1
0.3
0.4
"
0
H
Fig. 1. El Manaco molar microwear comparison.
11
-
10
;
h
2
0.0
0.8
-I
small pits
large pits
Pithecia
pith.
Cebus
nigriv.
Fig. 2. Comparison of small versus large pits between genera of El Manaco.
"
O
.-$ 2 9 E G
v
5
8 .
5 %7 :
9E
c-
g
5.
6:
4 -
3 2"
0.2
"
I
'
' '
'
'
1
0.3
0.4
0.5
0.6
0.7
0.8
Arcsine Transformation of % Plts
(mean and s. d.)
Fig. 3. Rio Cunucunuma molar microwear com.
parison.
.-
Chtropoier
small pits
rn
r<
bus
n,j,I>
large PlIS
Fig. 4. Companson of small versus large pits between genera of Rio Cunucunuma.
Rio Cunucunuma (Chiropotes satanas
and Cebus nigrivittatus)
Chiropotes had significantly greater proportions of pits and small pits, but pit width ouatta and Ateles (Table 4). Chiropotes and
was significantly greater in Cebus (Table 2, Aotus also had significantlyhigher numbers
of features per micrograph than did AlFigs. 3,4).
ouatta. The proportion of pits was signifiRio Mavaca (Chiropotes satanas, Ateles
cantly greater in Chiropotes, Aotus, Ateles,
belzebuth, and Sairniri sciureus)
and Saimiri, as compared with Cebus and
Chiropotes showed a significantly higher Alouatta (Fig. 7). The proportion of small
proportion of large pits than did either Ate- pits in Chiropotes was significantly greater,
les or Saimiri (Table 3, Fig. 5). Pit width for as compared with Cebus, Alouatta, and
Chiropotes was also significantly greater Saimiri (Fig. 8). Aotus, Ateles, Saimiri, and
Alouatta all had significantly greater prothan that for Ateles and Saimiri (Fig. 6 ) .
portions of small pits than did Cebus. For
Rio Manapiare (Chiropotes satanas,
large pits Saimiri had significantly higher
Cebus nigrivittatus, Ateles belzebuth,
percentages than Alouatta and Cebus while
Saimiri sciureus, Aotus trivirgatus, and
Chiropotes and Aotus had significantly
Alouatta seniculus)
higher values than Alouatta. Cebus showed
Cebus had a significantly greater number significantly wider pits than did Aotus, Chiof features per micrograph than did Al- ropotes, and Alouatta (Fig. 7). Scratch width
DENTAL MICROWEAR IN VENEZUELAN PRIMATES
353
was the only microwear measurement in
this comparison to show differences in variance between samples (as evidenced by Bartlett’s test). As a result, the fact that Ateles
and Aotus showed wider scratches than did
Cebus should be viewed as suggestive at
best.
Merged sites (Chiropotes satanas,
Pithecia pithecia, Cebus nigriviftatus,
Ateles belzebuth, Saimiri sciureus, Aotus
trivirgatus, and Alouatta seniculus)
Virtually all of these microwear comparisons showed significant differences in variance between genera (again, as evidenced by
the Bartlett’s test). The only “exception,”the
number of features per micrograph, showed
barely insignificant differences between
genera (P < .06). While some of these difference in variance might prove interesting in
future analyses (e.g., less variation in the
incidence of large pits on the teeth of Chiropotes and Pithecia), the more important implication for this study is that an underlying
assumption of ANOVA and the multiple
comparisons test (homoscedasticity)was not
met for the merged samples. As a result,
only the data for these samples are presented in Table 5.
“Wet” versus “dry” sites (Chiropotes
satanas, Cebus nigrivitfatus, Ateles
belzebuth, and Saimiri sciureus)
Cebus from the “wet”sites of Rio Manapiare and El Manaco had significantly more
features per micrograph than did Cebus
from the “dry” site of Rio Cunucunuma (Table 6). For Saimiri, two differences appeared. The proportion of small pits was significantly smaller, while average pit width
was significantly greater in specimens collected from the “wet” site of Rio Manapiare
than in those collected from the “dry” site of
Rio Mavaca. There were no other significant
differences detected between specimens collected in different seasons.
Two-way analyses of variance
Rio Mavaca vs. Rio Manapiare (Ateles,
Chiropotes, Sa im iri1
Dental microwear patterns showed no significant effects due to site, although pit
354
M.F. TEAFORD AND J.A. RUNESTAD
width showed nearly significant effects (see
Table 7). The only significant effects due to
genus were for the percentage of large pits,
although the number of features per micrograph also showed nearly significant effects
(see Table 7). Significant effects for the interaction of site and genus were shown for
pit width, and the percentages of small and
large pits (see Table 7).
Rio Cunucunuma vs. Rio Manapiare
(Cebus, Chiropotes)
The only significant effects due to site
were for the number of features per micrograph and for scratch width (see Table 8). By
contrast, every microwear measurement except the number of features per micrograph
showed significant effects due to genus (see
Table 8). There were no significant interactive effects for any of the microwear measurements (see Table 8).
Dry sites vs. wet sites (Ateles, Cebus,
Chiropotes, Saimiri)
The only significant effect due to season
was for the percentage of small pits (Table
9). All microwear measurements except the
number of features per micrograph and
scratch width showed significant effects due
to genus (see Table 9). However, genus-related differences in pit width and the percentage of small pits must be tempered by
the fact that significant interactive effects
were also documented for these comparisons
(Table 9).
DISCUSSION
Average number of features
per micrograph
The only sample for which there were any
significant differences in number of features
per micrograph was Rio Manapiare. At this
site, Alouatta had fewer features than did
Cebus, Chiropotes, and Aotus; and Ateles
had fewer features than did Cebus. As in
previous work with Alouatta palliatta
(Teaford, 1988; Teaford and Glander, 19911,
this relatively low number of features may
be due to the obliteration of features by
other wear processes, such as acid erosion.
The overall lack of significant differences in
number of features may be due to the consid-
DENTAL MICROWEAR IN VENEZUELAN PRIMATES
355
erable amount of variation present in the
samples, especially the variation between
certain sites (e.g., Rio Cunucunuma vs. Rio
Manapiare), as documented in the two-way
analyses of variance (Table 8).
Significance of pitting
Chiropores
sat.
A re 1 e s
belz.
Suimirr
sciur.
small pits
large pits
Fig. 5. Comparison of small versus large pits between genera of Rio Mavaca.
Saimiri sciureus
belzebuth
3
2
0.2
.
L
.
l
*
0.4
0.3
”
l
0.5
.
l
.
0.7
0.6
0.8
Arcsine Transformation of % Pits
(mean and s. d.l
Fig. 6. Rio Mavaca molar microwear comparison.
12
11
0.2
.
I
.
I
.
Cebus nigrivittatus
I
’
I
Ateles
.
I
.
belzeburh
0.3
0.4
0.5
0.6
0.7
Arcsine Transformation of % Pits
(mean and s. d.)
0.8
Fig. 7. Rio Manapiare molar microwear comparison.
Cebus and Alouatta consistently had the
lowest incidence of pitting, as both were significantly lower than all other genera wherever comparisons were possible. As Alouatta
is primarily a soft fruit eater (Crockett and
Eisenberg, 1986; Gaulin and Gaulin, 1982)
and Cebus has been observed to eat invertebrates and occasionally hard objects, as well
as soft fruit (Robinson, 19861, one might not
expect these two genera t o fall out together.
This again raises the question of whether or
not the classification of “pit” is specific
enough (i.e., perhaps not all pits are formed
alike). When the pits were separated into
small and large pits, differences between Cebus and Alouatta emerged. In the Rio Manapiare sample, Alouatta had a greater proportion of small pits than did Cebus. In fact, all
the remaining genera in all samples had
proportionally more small pits than did Cebus. When average pit width was examined,
however, Cebus had larger pits than did all
the other genera. Thus, while Cebus had a
low incidence of pitting, those pits that were
present were relatively large. This suggests
that hard objects may have a disproportionate effect on dental microwear patterns, and
it is further evidence that small and large
pits may be formed differently.
Focusing on the remaining genera, Pithecia and Chiropotes generally showed high
incidences of large and small pits, but so did
Aotus and Saimiri. In contrast, Ateles frequently had a high incidence of pitting, but
most of those pits were small. Some of these
results (e.g., the high incidence of large pits
on the teeth of Pithecia and Chiropotes) support the idea that large pits are formed during the mastication of hard objects. Likewise, the high incidence of small pits on the
molars of Ateles. Chiropotes, and Pithecia
might be taken as evidence that small pits
can indeed be formed in the mastication of
soft fruit. However, the results forAotus and
Saimiri are a bit surprising.
M.F. TEAFORD AND J.A. RUNESTAD
While Aotus certainly has a variable diet
(Robinson et al., 1986; Wright, 1985, 19891,
it is generally not considered a hard-object
feeder. Two interpretations might explain
the high incidence of large pits on its teeth:
1)Aotus might occasionally feed on hard objects or insects (see below) which might have
a disproportionate effect on microwear patterns, or 2) small pits might create minute
points of weakness in the enamel, causing
large pits to form by the amalgamation of
small pits. The results for Ateles and Cebus
argue against the latter alternative, for if
small pits could eventually grow into large
pits, one would not expect to find teeth with
predominantly large or small pits. Perhaps
the most reasonable explanation at this
stage is that Aotus is occasionally feeding on
hard objects or insects.
The presence of a high proportion of large
pits on the teeth of Saimiri is harder to interpret, as not enough is known about the
physical properties of invertebrate preywhile some insects might be "fluid-filled
rigid hollow tubes" (Lucas, 1979:504), others
might not be. Hence, it is still unclear
whether or not insect mastication should be
considered a cause of abrasive wear, toothon-tooth wear, and the like. One would expect abrasive wear to result if invertebrates
gradually break down into coarse, resistant
fragments when chewed. However, if the
fluid-filled tube model is accurate, tooth-ontooth wear could result from the high-impact tooth-tooth contact that might result
from sudden drops in resistance to occlusion
as tooth cusps pierce exoskeletons and hit
fluid. In view of the general lack of information on the physical properties of invertebrates a s food items, interpretation of the
high incidence of large pits in Saimiri (and
perhapsdotus) is best deferred until more is
known.
Scratch widths
Comparisons of scratch widths yielded
few consistent differences. Ateles might be
characterized by relatively wide scratches,
as compared with Cebus. Overall, however,
scratch widths showed few significant differences. Given the range of genera examined here, it is quite possible that the lack of
significant differences reflects the underly-
DENTAL MICROWEAR IN VENEZUELAN PRIMATES
T
.z cd
M
0
2
Chiropotes
sat.
Aotus
triv.
Saimiri
sciur.
357
T,
Cebus
nigriv.
Ateles
belz.
Alouatta
senic.
small pits
large pits
Fig. 8. Comparison of small versus large pits between genera of Rio Manapiare.
of consistent microwear patterns were evident from the results of this study. First, the
clearest differences in microwear were genSeasonal differences
erally between species with contrasting diComparison of genera collected in differ- ets collected from the same sites during the
ent seasons also revealed few significant dif- same months. For example, the greater pitferences. Cebus from “wet” season sites (Rio ting incidences seen in Pithecia or ChiropManapiare and El Manaco) had a greater otes, when compared with Cebus at El Mannumber of features than from a “dry”season aco and Rio Cunucunuma, were clear-cut.
site (Rio Cunucunuma) (see Table 6). Second, species with similar diets showed
Saimiri showed two related differences be- few significant differences in microwear.
tween sites-average pit width was greater, The hard-objecufruit consumers Pithecia
while the incidence of small pits was less in and Chiropotes had high proportions of both
the “wet” site sample (Rio Manapiare) than small and large pits. As a result, average pit
in the “dry” site sample (Rio Mavaca). As width in these genera was not very great.
discussed earlier, most of the paucity of sea- These microwear patterns probably relate to
sonal differences is probably due to rela- the preponderance of soft fruit and hard
tively minor resource fluctuations in the hu- fruit in the diets of Pithecia and Chiropotes.
mid tropical forest, even with seasonal By contrast, moderate to high levels of small
changes in rainfall (Foster, 1980; Leigh pits, but low levels of large pits, characteret al., 1982). Nonetheless, some taxa (e.g., ized the wear seen in soft-fruit eating AlSaimiri) may undergo enough change in the ouatta and Ateles.
availability of their preferred foods to alter
Further relationships between diet and
dental microwear patterns, especially if microwear were less obvious. Saimiri, a n inthese taxa have variable diets including sect eater, had high proportions of both
small and large pits. As not much is known
items of differing physical properties.
about the physical properties of insects, inSUMMARY
terpretation of this result awaits future reAs might be expected with good control search. Animals with more variable diets
over dates and sites of collection, a number had wear patterns which suggested that ocing complicating effects of enamel microstructure (Maas, 1988,1991).
358
M.F. TEAFORD AND J.A. RUNESTAD
casional food items might cause disproportionate effects on dental microwear. For example, Aotus had high small and large pit
proportions like Saimiri; and, even more intriguing, Cebus had low pitting incidences
accompanied by the largest pit sizes of any
of the genera. Not surprisingly, there were
few significant differences that could be related to season of collection.
CONCLUSIONS
Taken together, these results show that
we are probably a t the limits of resolution of
museum analyses of dental microwear and
published dietary information for these species. At best, the available dietary information represents a summary of observations
collected over one or more years of behavioral observation from one or more sites.
None of that dietary information has been
collected for the individual animals or the
sites used in this study. Since the animals
themselves were generally collected over a
one- to two-month period at each site, the
microwear data gathered here represent a
series of one- to two-month snapshots of behavior, and we simply cannot distinguish
between certain interpretations. For instance, some of the similarities in microwear
patterns (e.g., between Saimiri and Aotus)
may be due to significant dietary overlap
between species or to the fact that certain
dietary differences are simply indecipherable through dental microwear analyses.
Only further microwear work with live,
wild-trapped animals (e.g., Teaford and
Glander, 1991) will be able to sort through
these alternatives.
In addition to diet-microwear correlates,
we can also begin to draw conclusions on the
usefulness of some microwear measurements. As in previous microwear analyses
(e.g., Solounias et al., 1988; Teaford, 1985,
1988, in press; Teaford and Walker, 19841,
scratch width showed few significant differences between genera. In fact, the only cases
in which scratch width has proven useful
have been intraspecific comparisons (e.g.,
human hunter-gatherers versus agriculturalists) (Teaford, 1991). As differences in
enamel microstructure might be least likely
in such cases and most likely in intergeneric
comparisons (like those presented here),
100.22
(f24.1)
110
(3115.0)
111.33
(k11.8)
90.61
(124.8)
**114.05
(k22.0)
91.4
(f34.0)
82.33
(f37.4)
80.25
(f29.7)
**6.55
(fl.1)
4.02
(fl.2)
5.05
(11.2)
5.73
(51.6)
7.91
(f1.6)
8.95
(f2.4)
6.38
(572.0)
3.77
(f1.2)
Pit width
(microns)
0.96
(f0.l)
( f O . 1)
1.07
(f0.2)
0.99
(f0.2)
1.15
0.96
(f0.2)
1.05
(f0.2)
1.25
(f0.4)
1.17
(f0.3)
Scratch
width
(microns)
0.57
(f0.1)
0.65
(f0.05)
0.66
(fO.l)
0.67
(fO.l)
0.39
(rt0.l)
0.41
(*0.1)
0.58
(k0.2)
0.59
(fO.1)
Arcsine
transformation
of % pits
'Wet season sites included Ria Manapiare and El Manaco. Dry season sites included Rio Mavaca and Ria Cunucunuma.
**Significantly different (P< 0.05).
Drv
Saimiri sciureus
Wet
Dry
Chiropotes satanas
Wet
Dry
Cebus nigriuittatus
Wet
Dry
Ateles belzebuth
Wet
Taxon
Mean no. of
features per
micrograph
TABLE 6. Comparison of molar microwear in Venezuelan primates'
**0.34
(fO.1)
0.52
(f0.04)
0.48
(fO.l)
0.48
(50.1)
0.19
(f0.05)
0.19
(rt0.04)
0.48
(10.2)
(fO.1)
0.43
Arcsine
transformation
of % small pits
(< 4 microns)
0.43
(fO.l)
0.34
(f0.l)
0.41
(h0.04)
0.42
(f0.05)
0.33
(50.1)
0.35
(fO.l)
0.37
(f0.1)
0.3
(fO.l)
Arcsine
transformation
of % large pits
(> 4 microns)
360
M.F. TEAFORD AND J.A. RUNESTAD
TABLE 7. Results of Two-way Analyses of Variance of Microwear Data for Rio Mauaca us. Rio Manapiare
(Ateles, Chiropotes, Saimiri)
No. of features
Arcsine (prop. of pits)
Arcsine (prop. of
small pits)
Arcsine (prop. of
large pits)
Pit width
Scratch width
,001
,595
2.166
3.299
1.344
,088
,385
,593
3.459*
2.000
5.193**
3.469*
3.976
,224
1.985
2.595
11.270*'*
,671
*P< .05; **P < .02; ***P< .001.
TABLE 8. Results of Two-way Analyses of Variance of Microwear Data for Rio Cunucunuma us. Rio Manapiare
(Cebus, Chiropotes)
Variables
No. of features
Arcsine (prop. of pits)
Arcsine (prop. of
small pits)
Arcsine (prop. of
large pits)
Pit width
Scratch width
Site effects
(1 df)
F-values for comparisons
Genus effects
(1 df)
Site*genus
(2 d o
13.118***
1.506
1.278
1.859
75.652***
170.054***
,332
,142
.352
7.598*
1.915
38.442***
6.899*
,202
1.050
1.135
.054
11.050**
* P < .02;**P < .01; ***P< .001.
TABLE 9. Results of Two-Way Analyses of Variance of Microwear Data for Dry Sites us. Wet Sites (Ateles,
Cebus, Chiropotes, Saimiri)
Variables
No. of features
Arcsine (prop. of pits)
Arcsine (prop. of
small pits)
Arcsine (prop. of
large pits)
Pit width
Scratch width
Wetldry effects
(1df)
F-values for comparisons
Genus effects
(3 df)
Wet/dry*genus
(3 df)
1.19
1.03
5.865**
1.762
32.108***
43.995***
1.081
,461
3.519*
3.173*
1.960
3.251
3.239
0.000
16.214***
1.992
5.649**
1.341
*P< .05; **P< .02; ***I' < ,001
this might be further evidence that intergeneric comparisons of scratch widths might
be hampered by intergeneric differences in
enamel microstructure (Maas, 1988,1991).
Pitting incidence was found to be more
informative when divided into large and
small pits. This distinction made it possible
to distinguish between the low pitting incidences of Cebus and Alouatta, animals with
dissimilar diets. Cebus was found to have a
high proportion of large pits, while Alouatta
had a higher proportion of small pits, Given
the presence of occasional hard objects in
the diet of Cebus, and the dominance of soft
fruit in the diet of Alouatta, this might support the idea that large pits are formed differently than small pits. Large pits might
well be fractures in the enamel caused by
the compression of hard objects between
enamel surfaces. If, however, small pits are
formed by tooth-on-tooth wear, as was suggested earlier, then what wear process is in-
DENTAL MICROWEAR IN VENEZUELAN PRIMATES
36 1
Apparent c o n t a c t area
0= True contact
Fig. 9. Apparent and true contact areas.
volved? To put it another way, what really
happens during tooth-to-tooth contact? As
Roulet (1987) has noted for the wear of dental restorative materials, “if two surfaces
are in contact with each other, they will only
touch each other [over] a very small
area. . . Therefore, the apparent contact
area [will be] much larger than the true contact area” (1987:60) (see Fig. 9). In fact, the
sum of the true contact areas may be as
small as 1/10,000 of the apparent contact
area (Roulet, 1987). As a result, what might
seem like small loads applied to the teeth
may ultimately be transformed into extremely high pressures at microscopic contact points on the enamel. This, in turn,
might lead to two possibilities. If the pressure was great enough, the repulsive forces
between atoms might be overcome (Roulet,
1987), and minute welds could occur between prisms, or between hydroxyapatite
crystallites, on the opposing teeth. This
could result in adhesive wear through the
transfer of material from one surface to the
other. If, on the other hand, prism bound-
aries are points of weakness in the enamel
(Maas, 1988, 19911, the high pressures at
microscopic contact points might easily lead
to microscopic fracturing of prisms at prism
boundaries. In either case, the net result
would be a series of prism-sized pits caused
by strict tooth-on-tooth wear-perhaps
Walker’s (1980, 1984) enamel prism “plucking.” Either of these processes might explain
why acid erosion can help increase other
rates of wear (i.e., acid erosion might accentuate enamel prism relief, which might, in
turn, lead to more microscopic prism-toprism contacts, and thus more wear).
Single-factor analyses of variance and
two-way analyses of variance showed
roughly similar results. Granted, the results
of the two-way ANOVA’s must be viewed
with caution, due t o differences in sample
sizes and to the fact that comparisons could
only be made between certain sites and genera. Still, the results are fairly encouraging.
As might be expected (Maas 1988, 1991),
certain intergeneric differences had to be
tempered by significant interactive effects.
362
M.F. TEAF’ORD AND J.A. RUNESTAD
For instance, the incidence of large pits on
the teeth of Saimiri varied between Rio Mavaca and Rio Manapiare (compare Tables 3
and 4). Other comparisons! however, yielded
no significant interactive effects (e.g., between Cebus and Chiropotes at Rio Cunucunuma and Rio Manapiare). Interestingly,
the two-way ANOVA’s also showed that certain genera (e.g., Saimiri) might show seasonal differences in dental microwear (e.g.,
the proportion of small pits), while other
genera (e.g., Chiropotes) might not. Thus, at
these humid tropical forest sites, there were
no microwear patterns that could be attributed solely to season of collection irrespective of genus. Surprisingly, all of the significant interactive effects in the two-way
ANOVAs involved measurements of the
size of pits or the incidence of small or large
pits on the teeth. At the present time, we
cannot explain this finding, but to help sort
through variations in dental microwear patterns, future dental microwear analyses
should probably include two-way analyses of
variance in conjunction with other modes of
analysis whenever possible.
In closing, this project has demonstrated
that, even at relatively homogeneous humid
tropical forest sites, molar microwear patterns can be tied to dietary information in a
number of New World primate genera.
However, as dietary distinctions become
more subtle, microwear differences become
harder to document. In effect, we may be
reaching the limits of resolution of microwear analyses of museum material. Still,
we have found evidence that not all microscopic pits on teeth are formed alike. More
importantly, this study has demonstrated
significant differences in molar microwear
between primates that have traditionally
been viewed as “frugivores” in most morphological analyses. This raises the hope that
similar differences might be recognizable in
analyses of fossil material, bringing u s one
step closer to a n understanding of the evolution of diet and morphology.
ACKNOWLEDGMENTS
We thank Richard Thorington and
Charles Handley (Smithsonian Institution)
for allowing access to specimens in their
care. We also wish to thank Mary Maas and
3 anonymous reviewers for their comments
on the manuscript. This work was supported
by grants from the L.S.B. Leakey Foundation and NSF grants 8803570,8904327, and
8605172.
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