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