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Dentition of moustached tamarins (Saguinus mystax mystax) from Padre Isla Peru part 1 Quantitative variation.

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 130:352–363 (2006)
Dentition of Moustached Tamarins (Saguinus
mystax mystax) from Padre Isla, Peru, Part 1:
Quantitative Variation
Matthew A. Tornow,1* Susan M. Ford,2 Paul A. Garber,3 and Edward de sa Sauerbrunn2
1
Department of Sociology and Anthropology, Saint Cloud State University, Saint Cloud, Minnesota 56301
Department of Anthropology and Center for Systematic Biology, Southern Illinois University,
Carbondale, Illinois 62901
3
Department of Anthropology, University of Illinois, Urbana-Champaign, Illinois 61801
2
KEY WORDS
callithrichid; coefficient of variation; tamarin; dental variation
ABSTRACT
Analyses of dental variation in geographically restricted, wild populations of primates are extremely rare; however, such data form the best source
for models of likely degrees of variation within and
between fossil species. Data from dental casts of a geographically restricted population of moustached tamarins (Saguinus mystax mystax) from Padre Isla, Peru,
document high levels of dental variability, as measured
by coefficients of variation, in a nonsexually dimorphic
species, despite its isolation and small population
size. Like other primates, moustached tamarins show
Variation in modern primates is often used as a model
or baseline for determining likely degrees of variation
within and between fossil species (e.g., Gingerich, 1974;
Gingerich and Schoeninger, 1979; Cope and Lacy, 1992,
1995; Cuozzo, 2000, 2002). Recently, Plavcan and Cope
(2001, p. 206) urged that such analogies should be based
on data from ‘‘restricted geographic localities and time
horizons as much as possible.’’ However, detailed analyses of dental variation in a single, wild population of
any primate are extremely rare (Cuozzo, 2000; Sauther
et al., 2001), and have never been carried out on anthropoid primates. This study seeks to investigate dental
variability within a single, wild population of moustached tamarins (Saguinus mystax mystax), thus providing information regarding dental variability in haplorhine primates with characteristically simple teeth.
Prior studies indicating variation in tamarin teeth
include that of Kinzey (1973) on Saguinus mystax and
S. oedipus nonmetric features, Hershkovitz (1977) on 17
species, with a single toothrow measure, Swindler (1976)
on Saguinus geoffroyi metric and nonmetric features,
and Natori (1988) on nonmetric features in 11 species,
including S. mystax. [Natori (1992) also examined metric
data on these 11 (now 12) species, raising Saguinus
midas niger to separate species status, but the raw data
for this multivariate study are not given.] These studies
provide good comparative information on dental measurements for a number of tamarin species, but the samples include animals drawn from across a fairly large
geographic range for each species, and often the origins
of the animals are unspecified. Recent work on Lemur
catta (Sauther et al., 2001, 2002) and Galagoides demidoff (Cuozzo, 2000) demonstrated varying degrees of
dental variability found in geographically restricted
C 2006
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WILEY-LISS, INC.
lower variability in the dimensions of the first molars
and increased variability in the dimensions of the final
molars in the toothrow. Moustached tamarins from Padre
Isla have a distinctive pattern of variability in the remaining teeth, including more stable tooth lengths
in the anterior and posterior portions of the toothrow,
and more stable tooth widths in the midregion of
the toothrow. High variability in incisor width may
be due to age effects of a distinctive diet and pattern of
dental wear. Am J Phys Anthropol 130:352–363, 2006.
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V
Wiley-Liss, Inc.
groups of strepsirhine primates. Knowledge of this variability is important in understanding the range of dental
variability present in a single breeding population
exploiting a common set of resources, but until now, such
intrapopulation data have been unavailable for anthropoid primates. In addition, as we collect more information on individual breeding populations of living primates, we can develop more robust criteria for defining
the nature of species boundaries and morphological distinctions that accompany genetic changes and ecologically adaptive shifts.
Traditionally, tamarins and marmosets are described
as primates with reduced dentitions, lacking third
molars and hypocones and (in common with all platyrrhines) lacking paraconids, hypoconulids, and any real
stylar or conule elaboration (Swindler, 1976; Rosenberger, 1981; Ford, 1980, 1986; Ankel-Simons, 1983;
Fleagle, 1999). However, Kinzey (1973) noted that some
tamarins, and in particular Saguinus mystax, expressed
a surprising degree of intraspecific variability in qualitative features of the molar dentition, particularly in the
Grant sponsor: National Science Foundation; Grant number: BNS
8310480; Grant sponsor: Research Board, University of Illinois.
*Correspondence to: Matthew Tornow, Department of Sociology
and Anthropology, Saint Cloud State University, Saint Cloud,
MN 56301. E-mail: matornow@stcloudstate.edu
Received 23 March 2005; accepted 24 August 2005.
DOI 10.1002/ajpa.20374
Published online 9 January 2006 in Wiley InterScience
(www.interscience.wiley.com).
353
SAGUINUS TEETH
development of cingular and stylar cuspules, for a small
primate with a supposedly simplified dental form. The
findings of Kinzey (1973), in conjunction with more
recent analyses of tamarin dental variability (e.g., Swindler, 1976; Natori, 1988, 1992), suggest that tamarin
teeth do exhibit varying degrees of occlusal complexity
in the number and orientation of cusps and crests. Since
many early primates resembled modern tamarins and
marmosets in having a small body size and simple, tritubercular upper molars, better knowledge of intrapopulation dental variability offers an important model for
interpreting taxonomic differentiation among fossil assemblages of the earliest primates.
The aim of this paper is to present detailed data on
tooth size and shape in a single population of moustached tamarins. These data are then summarized
within a context of species recognition in fossil samples
and models of evolutionary processes within primates.
MATERIALS AND METHODS
One of us (P.A.G.) carried out long-term research in the
1980s and 1990s on a free-ranging population of moustached tamarins inhabiting Padre Isla (South 38 440 ,
West 738 140 ), a protected biological reserve located in
the Amazon River in northeastern Peru (Fig. 1). Padre
Isla is a recent, small island (5.2 km2) formed approximately 80–90 years ago from sediments of the Rio Amazonas (Moya et al., 1980). Three major lagoons (chochas)
run across the island, dividing it into narrow strips of
forest. The island receives 2,500–3,000 mm of rainfall
per year, and is inundated from March–June.
Primates are not native to Padre Isla. Between 1977–
1980, the Proyecto Peruano de Primatologia wild-trapped
and released for study 87 moustached tamarins (Saguinus
mystax) on the island, all taken from localities in Northeastern Peru (Moya et al., 1990). The entire founding
population consisted of 18 natural groups and two artificial groups composed of wild individuals from separate
wild-caught traps. Individuals were assigned to age categories (infant, juvenile, subadult, or adult) on the basis
of genital development, tooth wear, and dental stain. Each
animal was sexed, marked with color-coded collars,
and tattooed. No S. mystax individuals have been introduced to Padre Isla since 1980, nor is it possible for primates to migrate between the mainland and the island
(Garber et al., 1984).
In 1981, Garber et al. (1984) conducted a field study of
positional behavior, feeding ecology, and demography of
groups on the island. In 1990, Garber et al. (1993a,b)
and Garber and Pruetz (1995) recensused and restudied
the population. This included 467 hr of behavioral observation, as well as trapping and marking 98 of 114 moustached tamarins residing in 16 social groups. Whereas
the mean size of the Padre Isla social groups ðx ¼ 7:0Þ
was larger than those from other regions of Peru
ðx ¼ 5:3Þ the mean group size at Padre Isla falls within
the size-range of other natural groups of mainland
Saguinus mystax (Garber et al., 1993a).
During the 1990 study period (June–November), tamarins were trapped using the Saguinus trapping method
(Encarnación et al., 1993). This involved habituating an
entire group to a baited trap site composed of a single
cage divided into 10 separate compartments, each with
its own manually operating doors (Fig. 2). The compartments were closed by a concealed researcher pulling a
string that ran directly from each door to a blind. The
Fig. 1. Map of Peru, showing location of Padre Isla.
Fig. 2. Saguinus trap.
trapped group was transported to the field laboratory.
Each individual was injected intramuscularly with 0.1–
0.15 cc of ketamine HCL, a tranquilizer, and 0.05 cc of
torbutrol, an analgesic. The tamarins were examined,
weighed, measured, marked with a permanent tattoo,
and fitted with a beaded identification collar. Dental molds
of the upper and lower right maxillary and mandibular
dentitions of 67 individuals (Fig. 3) (drawn from 14 of
the social groups) were made using Colténe President
Jet regular-body polyvinylsiloxane impression material,
administered to the dentition through a syringe. The impressions were sealed in labeled plastic vials and stored
in the field. All tamarins were released back into the
wild at the original trap site within 24 hr.
Dental molds were made over the course of several
months. Seven animals were recaptured and dental
molds were created twice, months apart, yielding a total
of 74 separate molds (plus some duplicates made at the
same time). These remained stored until 2002, when
casts were made. The 67 tamarin specimens include 38
males and 29 females. Most were identified in the field
as adult, although 3 were identified as young adult, 12
as subadult, and 3 as juveniles. All but the juveniles had
354
M.A. TORNOW ET AL.
Fig. 3. Anesthetized Saguinus mystax, showing teeth and
gums.
fully erupted permanent dentitions; some of the adults
showed advanced dental wear.
Tamarin teeth are small and very sharp (particularly
the canines), and the impressions were set in very shallow molds due to the fact that the impressions were
made on living animals with high gum lines. It took a
great deal of experimentation to develop a suitable protocol for achieving successful casts. We used Easyflo 60
liquid plastic by Polytek, because of its low viscosity,
negligible shrinkage, and fast-setting properties. The
molds were first set in plasticene bases and fitted tightly
in hollow plastic cylinders (film canisters lacking their
bases). After being filled with casting agent (original
casts were plain; a second set was dyed using TintsAll),
the molds were spun in a home-built centrifuge at moderate speed for 1 min. The casts were then allowed to set
for at least an additional 30 min before being removed.
(Attempts at using more viscous casting compounds,
slower-acting compounds, and autoclaves were all markedly unsuccessful.)
Given the long period (11–13 years) between the creation of the original molds and casting, we were concerned about degeneration of the molds. The molds had
been stored in plastic containers, and had been undisturbed during the intervening decade. They appeared
pristine, and casts matched extremely well with both
previously published measurements on Saguinus mystax
(Hershkovitz, 1977) and museum specimens that we
examined. As an additional test, a comparative study
was performed on sets of Araldyte epoxy casts of Victoriapithecus teeth made by Dr. Brenda Benefit (New Mexico State University) from molds made in 1983 with Xantopren Blue (a polyvinalsiloxane dental molding material
nearly identical to that used by Garber in 1990). To evaluate potential mold degradation, original casts (poured
shortly after the molds were made in 1983) were compared to a second set of Araldyte epoxy casts made in
2003, both visually and metrically. Visual assessment
demonstrated no identifiable warping or shrinkage. Independent metric analysis carried out by three individuals,
who measured each cast, demonstrated that interobserver error exceeded the size difference between original and recent casts from the same molds (B.R. Benefit,
personal communication). This experiment reinforced
our view that the S. mystax molds had not degenerated,
and that the casts are valid representations of the dentitions of these animals.
The dental casts were scored for 61 metric traits.
Measurements are illustrated in Figure 4, and included
the occlusal and cervical length and width of the upper
and lower incisors, the length, width, and crown height
of the upper and lower canines, the maximum lengths
and crown areas of P2/2, P3/3, P4/4, M1/1, and M2/2,
the maximum widths of P2, P3, P4, M1, and M2, the trigonid and talonid widths of P2, P3, P4, M1, and M2, the
lengths of the upper and lower anterior (I1/1–C) and posterior (P2/2–M2/2) toothrows, and the lengths of the upper
and lower diastemata between I2/2 and C. Linear measurements (taken using Mitutoyo digital calipers) were
scored by E.S. under binocular dissection, while area
measurements were taken by M.A.T. from digital images
on a Macintosh computer, using the public domain NIH
Image 1.62 program (developed at the US National Institutes of Health, and available on the Internet at http://
rsb.info.nih.gov/nih-image/). In order to evaluate potential error in dental measurements, roughly one-quarter
(20 of 74, or 27%) of the measurements were randomly
reevaluated by M.A.T. In no instance did interobserver
error exceed 0.05 mm for linear measurements, a commonly accepted degree of error for small primate teeth
(Swindler, 1976; Bown and Rose, 1987; Cuozzo, 2000).
Area measurements were repeated twice (i.e., three total
measurements) in NIH Image to ensure accuracy,
and the average measurement was used. In addition to
computing basic statistics, sex differences were analyzed
with Student’s t-tests, using a Bonferroni-corrected alpha
level for 0.05 (n tests ¼ 61; alpha ¼ 0.0008). Combinedsex variation was examined using the coefficient of variation (CV).
Comparisons to CVs reported for other primate populations were done in two ways. 1) We used pattern recognition to look for differing patterns in which regions of
the toothrow exhibited greater variance, by plotting the
CVs together. 2) In order to evaluate the potential significance of differences in CVs, since for most comparative
samples we had no access to the original data, we computed the 95% confidence intervals for our CVs in the
following manner. Standard error of the CV was computed using the formulae from Sokal and Rohlf (1987):
CV
SEcm ¼ pffiffiffiffiffiffi 2n
CV
SEcm ¼ pffiffiffi
2n
sffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffiffi
8
92ffi
CV
>
>
>
> for
1 þ 2:
;
100
for CV 15:
CV 15
ð1Þ
ð2Þ
The 95% interval was then computed as 61.96 SE of the
CV for the Saguinus mystax sample. CVs that fell outside this interval were considered significantly more
likely to be truly different (either more or less variable).
In order to examine contrasting patterns in covariance
within the toothrows of Saguinus mystax, principal components analysis (PCA) was performed, following the
exploration of human patterns of covariance by Harris
and Bailit (1988), Harris et al. (2001), and Harris and
Lease (2005). PCA was performed on the correlation
matrix of the 40 variables describing lengths and widths
of individual teeth and canine height. Data on M2 (upper
and lower), area measurements, and cross-toothrow lengths
were not included in the PCA, because many specimens
had missing data. Eigenvectors (loadings) were plotted
by measurement variable for the first four principal com-
SAGUINUS TEETH
355
Fig. 4. Dental measurements.
Occlusal views of right lower
(right) and upper (left) dentitions,
showing measurements. a, tooth
length; b, tooth width; c, trigonid
width; d, talonid width; e, incisal
length; f, cervical length for
uppers, and heel length for lowers;
g, incisal width; h, cervical width
for uppers, and maximum heel
width for lowers; i, diastema
length; j, anterior toothrow length;
k, posterior toothrow length. Canine crown heights are measured from cervical margin to incisal edge of crown. Area measurements follow occlusial outlines
of teeth (see text).
ponents. These were visually examined for contrasting
patterns in eigenvector direction (positive vs. negative)
and value. All statistical tests were done using JMP
4.0.4 (SAS Institute, Inc., 1989–2002).
RESULTS
Sexual dimorphism
There is no evidence for sexual dimorphism in any of
the quantitative traits examined, nor are there sex differences in patterns of variability as indicated by the
CVs, particularly using a Bonferroni-corrected alpha of
P < 0.0008. The greatest differences between the sexes
primarily lie in dimensions of incisors, where males are
consistently larger; however, none are significant even at
the 0.05 level. For all subsequent analyses, the sexes
were pooled.
Metric variability
The sample sizes, means, standard deviations, and
CVs for male, female, and pooled-sex samples are provided in Table 1, as are the standard errors of the CV
(SECV) and upper and lower 95% confidence intervals for
the pooled-sex sample. The greatest amount of metric
variation in Saguinus mystax (Fig. 5) is found in crown
areas of the cheek teeth (particularly the uppers), the
bucco-lingual (b-l) widths of the upper incisors, and the
length of the I2/2 -C diastemata (not shown). In contrast,
the mesio-distal (m-d) lengths of the central incisors and
the I1-C lengths are among the least variable, as are the
linear measurements (lengths and widths) of upper and
lower P4 and M1. For all dimensions except area and
trigonid width of the lower teeth, the last molars (M2)
are more variable than M1.
Figure 6 and Table 3 compare the Saguinus mystax
data with several samples from the literature, including
restricted geographic samples of Lemur catta (for C–M3,
Sauther et al., 2001) and Galagoides demidoff (for M1–
M3 only, Cuozzo, 2000), a nongeographically restricted,
separate-sex sample of Saguinus geoffroyi (Swindler,
1976), and a combined primate sample (n ¼ 48) from
Gingerich and Schoeninger (1979). The pattern exhibited
by the S. mystax population is only partly mirrored in
these other primates. In the nongeographically restricted
S. geoffroyi sample, all teeth except for the trigonid and
talonid widths of M2 show lower CV values than in the
Padre Isla sample. This effect is not due to the difference
between separate-sex (S. geoffroyi) vs. combined-sex
(S. mystax) samples. Tamarins show little to no sexual
dimorphism, and as seen in Table 1, CVs for separatesex samples of S. mystax are very similar to those of the
combined-sex sample, generally falling between the two
separate sex values.
356
M.A. TORNOW ET AL.
TABLE 1. Summary statistics for female, male, and combined-sex samples of Saguinus mystax1
Female
Cervical length, I1
Occlusal length, I1
Cervical width, I1
Occlusal width, I1
Cervical length, I2
Occlusal length, I2
Cervical width, I2
Occlusal width, I2
Length, C1
Width, C1
Height, C1
Length, P2
Width, P2
Length, P3
Width, P3
Length, P4
Width, P4
Length, M1
Width, M1
Length, M2
Width, M2
Length, I1–C1
Length, upper diastema
Length, P2–M2
Crown area, P2
Crown area, P3
Crown area, P4
Crown area, M1
Crown area, M2
Maximum heel length, I1
Occlusal length, I1
Maximum heel width, I1
Occlusal width, I1
Maximum heel length, I2
Occlusal length, I2
Maximum heel width, I2
Occlusal width, I2
Length, C1
Width, C1
Height, C1
Length, P2
Width, P2
Length, P3
Width, P3
Length, P4
Trigonid width, P4
Talonid width, P4
Length, M1
Trigonid width, M1
Talonid width, M1
Length, M2
Trigonid width, M2
Talonid width, M2
Length of anterior teeth, I1–C1
Length lower diastema
Length of toothrow, P2–M2
Crown area, P2
Crown area, P3
Crown area, P4
Crown area, M1
Crown area, M2
Male
Pooled
N
X
CV
N
X
CV
N
X
SD
CV
SECV
CV
1.96 SE
CVþ
1.96 SE
27
27
26
27
27
28
28
28
29
29
29
29
29
29
29
29
28
27
27
22
23
28
28
21
28
28
25
27
20
29
29
29
29
28
28
28
28
27
28
27
28
28
28
28
28
27
28
27
26
26
28
27
26
27
27
28
27
26
27
26
26
2.14
2.35
1.58
0.72
2.02
1.95
1.39
0.72
2.69
2.17
5.47
1.98
2.41
1.79
2.61
1.85
2.84
2.59
2.96
1.69
2.43
10.48
2.67
10.10
4.96
5.12
5.95
8.21
4.53
1.43
1.60
1.86
0.65
1.64
1.90
2.05
0.71
2.37
2.57
4.94
2.42
2.23
1.96
1.82
2.16
1.75
1.70
2.56
1.98
2.07
2.43
1.75
1.73
7.07
0.94
11.83
5.60
3.80
4.28
6.27
4.89
24.77
9.36
15.19
25.00
18.81
15.38
12.95
22.22
11.52
8.76
14.63
14.14
11.20
11.17
6.51
6.49
6.34
5.79
8.78
11.83
11.52
4.68
20.22
4.85
16.33
17.97
17.14
14.86
15.45
14.69
7.50
12.37
23.08
14.02
13.16
9.76
42.25
9.70
14.40
9.51
9.50
10.76
11.73
11.54
7.41
10.86
9.41
6.25
9.09
6.76
9.05
8.00
8.09
5.37
22.34
5.33
16.96
15.53
17.06
14.67
10.84
38
38
38
38
38
38
38
38
38
38
38
38
38
38
38
37
37
37
37
33
33
38
38
33
36
36
35
36
30
36
36
35
36
36
36
36
36
36
35
35
36
36
35
35
34
34
34
35
35
35
33
33
33
35
35
32
36
36
34
35
34
2.30
2.44
1.73
0.78
2.00
2.10
1.51
0.79
2.64
2.16
5.32
1.96
2.42
1.85
2.58
1.88
2.85
2.66
2.98
1.82
2.47
10.35
2.61
10.14
4.84
5.31
5.73
8.70
4.59
1.52
1.65
1.88
0.65
1.79
2.00
2.07
0.74
2.26
2.53
4.74
2.44
2.21
1.98
1.83
2.16
1.65
1.64
2.62
1.97
2.07
2.38
1.72
1.70
6.99
1.05
11.68
6.10
4.02
4.45
6.26
5.09
21.74
9.43
16.18
34.62
21.00
10.95
18.54
26.58
12.12
11.11
14.85
10.71
8.26
12.97
9.69
7.98
9.82
8.65
10.07
13.19
11.34
4.25
11.88
4.04
23.97
20.90
18.50
16.32
20.04
9.87
7.88
11.17
23.08
11.73
12.00
7.73
18.92
13.72
12.25
13.29
9.84
7.24
11.62
7.10
6.94
10.30
10.37
6.49
10.66
8.70
10.50
9.88
9.41
4.29
28.57
5.31
16.07
14.18
15.73
14.54
11.98
65
65
64
65
65
66
66
66
67
67
67
67
67
67
67
66
65
64
64
55
56
66
66
54
64
64
60
63
50
65
65
64
65
64
64
64
64
63
63
62
64
64
63
63
62
61
62
62
61
61
61
60
59
62
62
60
63
62
61
61
60
2.23
2.41
1.67
0.75
2.01
2.04
1.46
0.76
2.66
2.17
5.38
1.97
2.42
1.82
2.59
1.87
2.85
2.63
2.97
1.77
2.45
10.41
2.64
10.12
4.89
5.23
5.82
8.49
4.57
1.48
1.63
1.87
0.65
1.73
1.96
2.06
0.73
2.31
2.54
4.83
2.43
2.22
1.97
1.83
2.16
1.70
1.67
2.59
1.97
2.07
2.40
1.73
1.72
7.02
1.00
11.75
5.89
3.93
4.37
6.26
5.00
0.51
0.23
0.27
0.24
0.40
0.27
0.25
0.19
0.32
0.22
0.79
0.24
0.23
0.22
0.22
0.14
0.24
0.20
0.28
0.23
0.27
0.46
0.42
0.44
1.02
1.03
1.04
1.35
0.83
0.19
0.13
0.21
0.15
0.23
0.25
0.17
0.22
0.28
0.37
0.57
0.23
0.19
0.23
0.17
0.15
0.19
0.17
0.17
0.20
0.16
0.24
0.15
0.15
0.34
0.27
0.62
0.99
0.58
0.71
0.91
0.58
22.98
9.50
16.33
31.69
19.89
13.35
16.84
25.40
11.89
10.10
14.77
12.10
9.51
12.22
8.39
7.58
8.58
7.64
9.45
13.16
11.18
4.42
15.88
4.35
20.81
19.70
17.90
15.89
18.27
12.70
7.91
11.49
23.01
13.46
12.54
8.43
30.69
12.19
13.25
11.84
9.55
9.00
11.64
9.14
7.17
10.99
9.89
6.40
9.90
7.82
9.87
8.81
8.94
4.83
26.61
5.32
16.86
14.82
16.27
14.52
11.64
2.12
1.16
1.48
3.05
1.81
1.62
1.51
2.35
1.43
1.22
1.78
1.46
1.14
1.47
1.01
0.92
1.05
0.94
1.16
1.74
1.47
0.54
1.42
0.58
1.92
1.81
1.69
1.45
1.89
1.55
0.97
1.41
2.12
1.66
1.54
1.04
2.96
1.51
1.64
1.48
1.18
1.11
1.44
1.13
0.90
1.38
1.24
0.80
1.25
0.99
1.24
1.12
1.14
0.60
2.55
0.68
1.54
1.85
1.51
1.83
1.48
18.83
7.23
13.43
25.72
16.34
10.18
13.89
20.80
9.08
7.72
11.28
9.24
7.27
9.34
6.41
5.78
6.53
5.80
7.17
9.74
8.30
3.37
13.10
3.21
17.05
16.16
14.60
13.05
14.57
9.66
6.02
8.72
18.85
10.21
9.51
6.40
24.89
9.23
10.03
8.94
7.25
6.83
8.81
6.92
5.41
8.28
7.47
4.83
7.46
5.89
7.43
6.62
6.70
3.65
21.61
4.00
13.83
11.19
13.31
10.93
8.74
27.13
11.77
19.23
37.66
23.44
16.52
19.79
30.00
14.70
12.48
18.26
14.96
11.75
15.10
10.37
9.38
10.63
9.48
11.73
16.58
14.06
5.47
18.66
5.49
24.57
23.24
21.20
18.73
21.97
15.74
9.80
14.26
27.17
16.71
15.57
10.46
36.49
15.15
16.47
14.74
11.85
11.17
14.47
11.36
8.93
13.70
12.31
7.97
12.34
9.75
12.31
11.00
11.18
6.01
31.61
6.64
19.89
18.45
19.23
18.11
14.54
1
mean measurement; CV, coefficient of variation; SD, standard deviation of mean; SECV, standard error of coeffiN, sample size; X,
cient of variation; CV1.96SE and CVþ1.96SE define 95% confidence intervals of CV. Last four statistics are presented only for
pooled data, since Saguinus mystax is not sexually dimorphic dentally (see text).
SAGUINUS TEETH
357
Fig. 5. Plot showing CVs for dental mesio-distal lengths (L), bucco-lingual widths (W), and areas of Saguinus mystax combinedsex samples from Padre Isla, Peru. Up., upper; Lo., lower.
Fig. 6. Comparative CVs of upper and lower tooth lengths and widths for Saguinius mystax, Saguinus geoffroyi, Lemur catta,
Galagoides demidoff, and a pooled primate sample from Gingerich and Schoeninger (1979).
358
M.A. TORNOW ET AL.
The upper dentitions of the two tamarins show similar
patterns of variability, with the least variation in P4 and
M1 length, and an increase in the variability of M2.
Although absolutely less variable in terms of CV, Saguinus geoffroyi exhibits a similar pattern of variability in
lower tooth lengths to that seen in the Padre Isla sample
of Saguinus mystax, where the incisors are most variable, P3 shows slightly more variability than P2, P4 and
M1 are the least variable, and M2 demonstrates increased variability. However, evaluation of lower tooth
widths demonstrates different patterns of variability
both between the sexes of S. geoffroyi, and between
S. geoffroyi and S. mystax. Although in all three tamarin
samples, I1 width is more variable than that of I2, lower
canine width shows a different pattern of variability
between the S. geoffroyi sexes, with males showing
increased variability, but females decreased variability
in C width relative to that found in I2. The pattern of
canine variability found in the combined-sex sample of
S. mystax is like that of the S. geoffroyi males; evaluation of the separate-sex samples for S. mystax shows
that both males and females express this same pattern
(Table 1). S. geoffroyi and S. mystax also differ in the
pattern of variability in the widths of the cheek-teeth.
S. geoffroyi is least variable in P4, while S. mystax shows
less variability in M1 width. Variability in M2 width in
S. geoffroyi is extreme, showing significantly greater variability than that seen in S. mystax.
The other two geographically restricted primate samples also show lower variability than the Padre Isla tamarins, with the exception of the widths of the mid-dentition of Lemur catta (C1, P2/2, and P3/3), which are significantly more variable. Unfortunately, data are not
available on the anterior dentition of either L. catta or
Galagoides demidoff. For both L. catta and Galagoides
demidoff, M1 and to a degree P4 (data only for L. catta)
are among the least variable teeth, but M2 lengths and
widths, especially upper M2 for all measures in both and
M2 length in Galagoides, also have low CVs. However,
these are primates with three molars, and M3s show a
modest increase in variability in most dimensions.
Variability in Saguinus mystax equals or exceeds that
in the pooled primate sample of Gingerich and Schoeninger (1979) for almost all measurements except the
canines, lower P2–3 lengths, and I1 length, where the
pooled primate sample shows significantly greater variability. The pooled primate sample included a majority
of primates that are sexually dimorphic, which would
inflate the variability in canine and anterior premolar
dimensions, the most sexually dimorphic teeth in the
toothrow. The monomorphic tamarins are therefore unsurprising in showing lower variability for these traits,
in particular.
Principal components analysis
In addition to cross-species examinations, it can be
informative to explore patterns of covariance within tamarin jaws. Harris and Bailit (1988), Harris et al. (2001),
and Harris and Lease (2005) showed that interesting
patterns in covariance and contrast within toothrows
can be demonstrated using principal components analysis, at least for humans. In all cases they examined, for
both permanent and primary teeth, all dental variables
showed positive loadings on the first principal component (PC), reflecting size. For Solomon Islander permanent teeth, PC1 accounted for about 45% of the variance
(Harris and Bailit, 1988); for the primary teeth of various human groups, PC1 accounted for about 68% of the
variance (Harris and Lease, 2005). The authors argued
that components with eigenvalues greater than 1 are
most easily interpreted, and for humans, they found that
between two (primary teeth; Harris and Bailit, 1988)
and four (permanent teeth; Harris et al., 2001; Harris
and Lease, 2005) components reached that threshold of
contribution to the total variance. Looking at the remaining components, they found within-toothrow contrasts of various types, depending in part on the data
examined. These contrasts include enamel thickness to
dentine thickness (Harris et al., 2001) and dimensions of
anterior teeth to molars (Harris and Lease, 2005) on primary teeth. But most interesting for comparison here,
Harris and Bailit (1988) found three patterns of contrasts in human permanent teeth, in order of strength of
contrast: mesio-distal lengths vs. bucco-lingual widths
(PC2), anterior teeth vs. posterior teeth (PC3), and premolars vs. molars (PC4).
When a similar analysis is performed on tamarin teeth,
patterns are not as clearly defined as in human teeth. All
loadings on PC1 are indeed positive, but this component
only accounts for 14.6% of the variance. Twelve factors
have eigenvalues above 1, and together they account for
76.2% of the variance. The first five factors each have
eigenvalues above 2, and together account for 50.1% of
the total variance. We examined variable loadings on these
first five factors, with the first four shown in Figure 7
(these explain 14.6%, 13.4%, 9.1%, 7.5%, and 5.6% of
the variance, respectively). The contrasts seen are not as
clear as in the human populations, in part because the
canines often demonstrate patterns quite different from
those seen in the incisors, unlike the human sample.
PC1. All loadings are positive. However, the smallest
contributions (lowest values) are made by the canine and
M1 mesio-distal lengths and I1 widths (occlusal and cervical), while the strongest are P3 and P4/P4 mesio-distal
lengths.
PC2. There is a weak indication of a mesio-distal (negative) vs. bucco-lingual (positive) contrast, similar to that
seen much more strongly in the human population (Harris and Bailit, 1988). In tamarins, the negative mesiodistal loadings are strongest in the incisors, while the
postive bucco-lingual loadings are strongest in the canine,
premolar, and molar dimensions. The other dimensions
have eigenvector loadings closer to zero, with the exceptions of the contrary and highly positive loadings for
mesio-distal lengths of the upper canine and M1. Thus,
while a pattern similar to that seen in humans exists, it
is more weakly expressed and nonexistent in some parts
of the dental arcade.
PC3. While there are strong contrasts in the tamarin
loadings, a distinct pattern is difficult to discern, unlike
the very strong anterior vs. posterior tooth contrast seen
in humans for PC3 (Harris and Bailit, 1988; and in primary teeth on PC2, Harris and Lease, 2005). In tamarins, strong positive loadings appear for canine mesiodistal lengths and heights, and upper canine and P2, P3,
and P4 widths, contrasted to strong negative loadings for
incisor bucco-lingual occlusal widths and I1 occlusal
length. However, the negative loadings are not particularly strong, and loadings for incisor cervical dimensions
are close to 0 or positive. However, an anterior vs. posterior (including canine) tooth contrast is seen in bucco-
359
SAGUINUS TEETH
Fig. 7. Plots of weightings (eigenvectors) of 40 dental dimensions with each of first four retained principal components (PCs).
These include mesio-distal lengths and bucco-lingual widths within each arcade, plus canine heights (M2, area, and toothrow measurements were not included because of missing data). Within each arcade, sequence of points is I1, I2 (solid dots, cervical and then
occlusal measures), C (crosses), P2, P3, P4 (open squares), and M1 (asterisks). P4 and M1 include trigonid and talonid widths. Final
two points on each plot represent C heights (upper and lower, as crosses). Note that all loadings on PC1 are positive, but other
three show clear but complicated contrasts; see text.
lingual widths of the upper dentition. It may be that the
strong positive loadings of the canine dimensions in tamarins mask an anterior-posterior pattern in the other
quadrants of the jaw.
PC4. With a few exceptions, the tamarin pattern here
shows two sweeping upward arcs, contrasting negative
values for anterior upper dimensions to positive values
for posterior lower dimensions, with the rest near 0. The
exceptions are lower incisor occlusal bucco-lingual widths.
However, tamarin incisors show considerable wear with
age, which can dramatically affect this measure. This
pattern is not the same pattern seen in humans for PC4;
Harris and Bailit (1988) found a premolar/molar contrast. This latter contrast does appear with PC5 (not
shown), but it is weak, with low values and several
near 0.
Thus, PCA examination of covariance patterning in
tamarin teeth indicates that there are contrasting patterns, and that many of these patterns are similar to
those seen in humans, and in the same sequence of
importance. However, the tamarin patterns are all more
weakly expressed with more exceptions (particularly the
canine dimensions), and an additional pattern that
crosses the entire dentition (upper anterior to lower posterior in PC4) is seen that has not been reported for
humans.
DISCUSSION
Patterns of variability
The pattern of variability in Saguinus mystax is
marked by relatively more stable m-d lengths for anterior and posterior teeth, but more stable widths in the
mid-toothrow. Saguinus geoffroyi, on the other hand, has
more stable b-l widths throughout most of the toothrow
except M2, while Lemur catta shows the reverse pattern
to S. mystax (more stable lengths in the mid-toothrow,
and more stable widths in the mid and posterior teeth).
Galagoides demidoff shows a changing pattern in the
molar row, though all molar measurements show relatively low CVs. Thus, moustached tamarins are both
more variable than the other geographically restricted
primate populations examined to date, and exhibit a
unique pattern through the toothrow. Although molar area
was not computed as a simple product of length 3 width,
this measurement is still two-dimensional. Therefore,
the increased variability in this measure over linear
measures is expected.
The high variability in incisor b-l width (especially
occlusally) may relate to diet. Table 2 provides data on
the diet of moustached tamarins at three study sites in
Peru and Brazil. Their diet is composed principally of
fleshy fruits, insects, legumes, nectar, and exudates, and
they were also reported occasionally to eat vertebrates
360
M.A. TORNOW ET AL.
TABLE 2. Primate CVs compared with Saguinus mystax from Padre Isla1
Occlusal length, I1
Cervical width, I1
Occlusal length, I2
Cervical width, I2
Length, C1
Width, C1
Length, P2
Width, P2
Length, P3
Width, P3
Length, P4
Width, P4
Length, M1
Width, M1
Length, M2
Width, M2
Occlusal length, I1
Maximum heel width, I1
Occlusal length, I2
Maximum heel width, I2
Length, C1
Width, C1
Length, P2
Width, P2
Length, P3
Width, P3
Length, P4
Talonid width, P4
Length, M1
Trigonid width, M1
Talonid width, M1
Length, M2
Trigonid width, M2
Talonid width, M2
Saguinus
mystax CV
95% confidence
interval CV
9.50
16.33
13.35
16.84
11.89
10.10
12.10
9.51
12.22
8.39
7.58
8.58
7.64
9.45
13.16
11.18
7.91
11.49
12.54
8.43
12.19
13.25
9.55
9.00
11.64
9.14
7.17
9.89
6.40
9.90
7.82
9.87
8.81
8.94
7.23–11.77
13.43–19.23
10.18–16.52
13.89–19.79
9.08–14.70
7.72–12.48
9.24–14.96
7.27–11.75
9.34–15.10
6.41–10.37
5.78–9.38
6.53–10.63
5.80–9.48
7.17–11.73
9.74–16.58
8.30–14.06
6.02–9.80
8.72–14.26
9.51–15.57
6.40–10.46
9.23–15.15
10.03–16.47
7.25–11.85
6.83–11.17
8.81–14.47
6.92–11.36
5.41–8.93
7.47–12.31
4.83–7.97
7.46–12.34
5.89–9.75
7.43–12.31
6.62–11.00
6.70–11.18
Lemur
catta CV
8.28
15.80
7.70
13.30
7.10
13.50
7.50
5.40
6.00
5.00
5.00
4.40
6.80
11.90
6.40
12.30
4.80
8.80
4.90
5.20
6.00
6.90
Galagoides
demidoff CV
4.5
4.9
4.5
4.7
5.7
6.9
4.6
3.7
6.0
7.7
Saguinus
geoffroyi
male, CV
Saguinus
geoffroyi
female, CV
6.25
6.50
9.47
3.53
4.64
3.91
5.71
4.81
5.79
4.67
7.00
4.41
3.93
5.00
4.38
5.20
5.63
5.00
10.59
3.68
7.69
4.81
7.50
5.00
8.18
3.64
7.39
4.35
3.93
5.22
5.22
4.58
16.84
21.58
8.33
4.21
6.84
6.47
6.90
4.17
9.05
7.14
7.50
6.13
6.67
7.65
4.14
5.38
6.25
4.44
6.47
6.67
7.78
5.26
3.85
4.07
7.60
5.65
7.83
6.36
4.78
3.75
4.14
3.48
3.91
6.25
14.50
17.00
Pooled
primate CV2
9.4
9.7
10.2
10.0
15.8
14.4
9.9
8.7
8.6
8.6
7.6
7.9
6.1
7.1
6.3
7.0
10.4
9.5
10.0
9.3
16.6
17.4
11.8
10.5
14.9
11.0
7.7
8.7
6.0
7.1
5.8
7.1
CV, coefficient of variation; 95% confidence intervals of CV are defined by CV 6 1.96 SECV. CVs in bold fall outside of 95% confidence interval, and are considered significantly lower. CVs in italics fall outside of 95% confidence interval, and are considered significantly higher.
2
Pooled primate data (n ¼ 49) are from Gingerich and Schoeninger (1979).
1
TABLE 3. Diet of moustached tamarins
Fruits
Legumes
Exudates
Nectar
Insects
N
Location
Reference1
42.3
16.1
69.6
9.3
25.4
16.9
2.2
1.2
2.9
5.6
1.1
8.0
40.4
56.1
2.7
3,149
2,531
Quebrada Blanco
Padre Isla
NE Peru
1
2
3
1
1, Garber, 1993 (% time spent feeding and foraging); 2, Garber, unpublished (% time spent feeding and foraging); 3, Knogge and
Heymann, 2003 (% time spent feeding only).
(Heymann et al., 2000). Insects, principally large-bodied
orthopterans, account for a substantial portion of moustached tamarin feeding and foraging time in the study
groups of Garber (1993, and here), and foraging for
insects is considerably more time-consuming than foraging for plant parts. The data of Knogge and Heymann
(2003) show that for at least some moustached tamarins,
actual feeding time on insects is relatively low; however,
no measures of foraging time or the relative caloric content of these food items were presented in Knogge and
Heymann (2003). On Padre Isla, Norconk (1986) reported
that exudates, including those from legume pods, constitute a significant proportion of the diet during certain
months of the dry season. On Padre Isla and in other
parts of Peru and Brazil, the gooey exudates inside
legume pods appear to be an important food resource
(Peres, 1992; Garber, 1993b; Knogge and Heymann,
2003). In northeastern Peru, tamarins open Parkia pods,
eating the sticky interior but excreting the seeds (Knogge
and Heymann, 2003). One of us (P.A.G.) found that the
moustached tamarins on Padre Isla forage on pods of the
genus Inga. The pods of Inga are tough, leathery, and
sometimes woody, requiring considerable breaching with
the anterior dentition to open in order to access the soft
and sweet-tasting arilate seed coat, which is consumed.
The frequent use of the incisors in husking and breaching
may cause heavy wear with age, leading to the high variability in b-l occlusal width, in particular, in individuals
of varying adult age; this was explored further by Robinson (2004) and Robinson et al. (2004).
The second molars of Saguinus mystax are more variable than first molars in length, width, and crown area.
361
SAGUINUS TEETH
Comparisons with samples of Saguinus geoffroyi demonstrate that this increased variability in M2 is not unique
to S. mystax, but rather to tamarins as a whole when
compared with other primate species (e.g., Lemur catta
and Galagoides demidoff). This supports the view that
the second molar is less constrained in size and shape,
taking on the role of the hypervariable last molar normally filled by the third molar (Gingerich and Schoeninger, 1979), which is absent in tamarins.
Based on an analysis of dental metrics in 67 wildcaught and released Saguinus mystax, there is evidence
of high population variability in all measures. Such high
levels of dental variability were unexpected among individuals living in a geographically bounded population
that was founded by an initial population of only 87 individuals trapped in a restricted region of Peru. Dental
molds were made after this population had been isolated
for 13 years, and included the teeth of many individuals
born since the initial introduction of tamarins to Padre
Isla. One might predict that the combination of founder
effect and inbreeding would have resulted in reduced
variability. The finding of greater variability than present in the only other two reported geographically restricted primate populations where similar data were
collected can be interpreted in two ways.
First, moustached tamarins, at least in northeastern
Peru, may be naturally more variable in dental measures than other primates so far studied, and this variability characterized the founder group. While the original population introduced to Padre Isla consisted of individuals from different localities, all were from the same
general region of Peru. This region is smaller than the
geographically restricted Galagoides demidoff sample
from Ghana, Togo, and Benin (Cuozzo, 2000).
Alternatively, isolation on Padre Isla may have somehow released selective pressures and/or resulted, due to
stochastic processes, in markedly increased variability
over that characterizing other breeding populations of
primates. Although predatory selective pressures are
exhibited by the presence of constrictors and birds of
prey on Padre Isla, there are no known animals that
might compete with moustached tamarins for food resources; thus, dental metrics may be free to vary to a
greater extent than may be expected where competition
for resources is greater.
Comparable data on additional, geographically restricted primate populations, including other moustached
tamarins, will allow sorting between these two options.
However, if option 2 is correct, this suggests that not all
small founding populations (whether natural or humanengineered) are destined to ever-reducing degrees of variability (for discussions of founding population size and
variability, see Hartl, 2000; Ridley, 2004), a phenomenon
not entirely unexpected due to the limited time since initial introduction to the island. The population sampled
in 1990 included original founders and descendents.
These could have included up to 5–6 generations, given
sexual maturation around 2 years of age in tamarins,
but more likely 2–3 generations, since the oldest females
in a social group are generally the only breeding animals
(Garber et al., 1993a).
Case study: the
Absarokius abbotti–A. noctivagus complex
Coefficients of variation from geographically restricted
populations are particularly useful for assessing the dis-
tinctness of fossil populations. As an example, the specific status of the early Eocene omomyoid Absarokius
noctivagus relative to Absarokius abbotti remains disputed. Matthew (1915) initially diagnosed the species
Absarokius noctivagus relative to A. abbotti on the basis
of its more advanced dentition. Szalay (1976) retained
this specific distinction, noting the larger, more buccally
distended P4 of A. noctivagus. However, metric analysis
of Absarokius specimens from the Bighorn Basin, Wyoming, led Bown and Rose (1987) to the conclusion that
A. noctivagus was a junior synonym of A. abbotti. They
found that despite a wider P3 and P4 in the type specimen of A. noctivagus than in other Absarokius specimens from similar stratigraphic levels, the size distribution of these teeth among the entire sample suggested
intraspecific variability. Williams (1994) resurrected Absarokius noctivagus on the basis of statistically significant size differences (P3 length and width, P4 width, M1
width, and M2 length) between specimens from the
Washakie Basin, Wyoming, and those specimens from
the Bighorn Basin that Bown and Rose (1987) had
attributed to A. abbotti. Most recently, Tornow (2005)
chose to subsume both species within A. abbotti in his
analysis of omomyoid relationships, noting only modest
degrees of variability in a combined sample of Absarokius abbotti and A. noctivagus.
In order to evaluate the specific status of the Absarokius abbotti–A. noctivagus complex, we evaluated a combined sample of Washakie Basin and Bighorn Basin
Absarokius relative to the geographically restricted Saguinus mystax data. Coefficients of variation were calculated for P3 length (n ¼ 17, CV ¼ 10.37), P3 width (n ¼
17, CV ¼ 6.86), P4 width (n ¼ 22, CV ¼ 6.31), M1 talonid
width (n ¼ 33, CV ¼ 4.98), and M2 length (n ¼ 30, CV ¼
4.80). In no instance did the level of variability in the
Absarokius sample exceed the upper 95% confidence
limit for the S. mystax sample. This supports the contention that the combined A. abbotti–A. noctivagus complex
represents a single species: Absarokius abbotti. With the
exception of P3 length, which falls within the range
of variability found for S. mystax, all measurements prove
to be significantly less variable than those measurements
among S. mystax from Padre Isla.
When the standard error of the coefficient of variation
(SEcv) of the Absarokius sample is computed for those
measurements that fell below the 95% confidence intervals for the Saguinus sample (P3 width SEcv ¼ 9.95; P4
width SEcv ¼ 8.83; M1 width SEcv ¼ 6.63; M2 length
SEcv ¼ 6.47) and compared with the CVs for S. mystax,
all but the width of P3 are significantly less variable in
the Absarokius sample. This suggests that, while the
width of P3 in the Absarokius sample appears to be less
variable than it is in S. mystax from Padre Isla, a larger
sample size of Absarokius is necessary to conclude that
this difference is statistically significant.
CONCLUSIONS
Examination of casts of teeth from a geographically
restricted population of moustached tamarins, Saguinus
mystax, increases our knowledge of primate dental variability, and demonstrates that patterns of variability differ between primates. Saguinus mystax shows no sexual
dimorphism in either metric dimensions or degrees of
variability, as measured by coefficients of variation. This
population of S. mystax is far more variable in the
lengths of the upper and lower incisors, canines, P2/2,
362
3
M.A. TORNOW ET AL.
1
2
P /3, M /1, and M /2, and the widths of the upper and
lower incisors, C1, P4, M1, and M2, than other reported
geographically restricted primate populations and one
other reported tamarin species. This raises questions
about the effects of isolation and small population size
on variability. All reported geographically restricted populations share a pattern of low variability in the dimensions of the first molars, and increased variability in the
dimensions of the final molar in the toothrow. However,
the remaining pattern seen in S. mystax is distinctive,
including more stable tooth lengths in the anterior and
posterior portions of the toothrow, and more stable tooth
widths in the midregion of the toothrow. High variability
in incisor width may be due to the age effects of a distinctive diet and wear (Robinson, 2004; Robinson et al., 2004).
Attempts at identifying the number of species in the
fossil record are generally predicated based on variability seen in living primate species. This study indicates
that primate species vary in patterns within the toothrow. Moreover, at least one anthropoid (Saguinus mystax
mystax) is more variable than strepsirhines and available cross-primate models for certain dental dimensions.
More studies on other geographically restricted samples
of anthropoids, including anthropoids of larger body size,
will help discern if this greater variability is a tamarinspecific pattern or one shared with other anthropoids.
Tamarin variability is particularly significant for interpretations of variability and species boundaries in smallbodied omomyoids and early anthropoids.
ACKNOWLEDGMENTS
We thank Frank Cuozzo, Michelle Sauther, and Alexandra Robinson for discussions, Brenda Benefit for confirmation of the consistency of the molds over time, and
Robert Corruccini for advice on statistical matters. The
final version was immeasurably improved thanks to the
comments of Clark Larsen and two anonymous reviewers.
We are grateful for their input; remaining errors are our
fault alone. P.A.G. thanks Sara and Jenni for their love,
and for allowing me to spend time with the wonderful
moustached tamarins of Padre Isla.
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