Dentition of moustached tamarins (Saguinus mystax mystax) from Padre Isla Peru part 1 Quantitative variation.код для вставкиСкачать
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 V 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. C 2006 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: email@example.com 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. 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