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. 2025 Nov 19;188(3):e70167. doi: 10.1002/ajpa.70167

Enamel Prism Angle Variation and Hard‐Object Feeding in Cercopithecoids With Known Diets

Jacob Scheinblum 1, W Scott McGraw 1, Kaita Gurian 1, Debbie Guatelli‐Steinberg 1,✉
PMCID: PMC12628355  PMID: 41257393

ABSTRACT

Objectives

To examine relationships between enamel prism angles relative to wear surfaces and dietary hardness in three cercopithecoid genera. We hypothesized that the hard‐object feeding (durophagous) Cercocebus atys and Lophocebus albigena would have higher prism angles, making their enamel in this region stiffer and stronger in this region, than the soft‐object feeding Cercopithecus. We further investigated whether the habitually durophagous Cercocebus atys and the fallback hard‐object feeding Lophocebus albigena had similarly high prism angles.

Materials and Methods

Molars were sectioned using standard protocols and imaged with a Motic BA 310 Microscope with a Moticam camera. ImageJ FIJI was used to measure prism and wear angles. Measurements were made on 13 Cercocebus atys, 13 Lophocebus albigena, and 11 Cercopithecus molars, though sample sizes varied for different comparisons.

Results

Repeated measures regressions of upper functional and non‐functional cusps were used to test for the effects of tooth, genus, tooth‐genus interaction, and wear angle on prism angle. Genus and wear angle were found to be statistically significant predictors. Pairwise comparisons revealed significantly higher prism angles in Cercocebus atys vs. both Lophocebus albigena and Cercopithecus. There was no significant difference between Lophocebus albigena and Cercopithecus in prism angles.

Discussion

Our finding that the prism angles of a fallback hard‐object feeder ( Lophocebus albigena ) are more similar to those of a soft‐object feeder (Cercopithecus) than to a habitual hard‐object feeder ( Cercocebus atys ) suggests that the correspondence between durophagy and enamel microstructure is not straightforward, complicating our ability to infer durophagy in the fossil record.

Keywords: enamel, enamel prisms, hard‐object feeding, mastication, teeth

Left: Cercocebus atys specimen 16–9 third molar showing Phase II enamel prism angle (angle between prism path and wear facet) and wear angle (angle between wear facet and enamel dentin junction (EDJ)). Scatterplot of prism vs. wear angles for the Phase II wear facet. Note the higher angles for Cercocebus.

graphic file with name AJPA-188-e70167-g002.jpg

1. Introduction

Reconstructing diet in fossil hominins remains a central aim of biological anthropology (Ungar 2012); however, identifying reliable dietary signals from teeth is often challenging. For example, the nature of the feeding ecology of the robust east African hominin Paranthropus boisei is a vexing problem due to the mismatch between diet inferred from tooth morphology versus that indicated by dental microwear and the chemical composition of enamel (Daegling et al. 2013; Strait et al. 2013). Some of the difficulty in interpreting signals of dietary adaptation from tooth morphology in fossils comes from gaps in our understanding of how diet, feeding behavior, and dental structure relate in living primates. The present study examines relationships between one such aspect of dental structure—the angles that enamel prisms make to worn enamel surfaces—in primates that eat hard foods, either seasonally or year‐round, and in primates that do not eat them.

Hard‐object foods are considered “fallback” dietary items by some authors because primates access them only when preferred softer foods are not available. This is the case for the mangabey Lophocebus albigena , a species known to consume hard seeds during periods of food scarcity when preferred softer food items are less abundant (Lambert et al. 2004). Observing that Lophocebus albigena has thick enamel that would resist fracture from the large forces required to break hard seed casings, Lambert et al. (2004) proposed that hard foods, even if eaten infrequently, provide a selection pressure favoring thick enamel because such hard foods may have been critical to survival during periods when softer foods were not available. McGraw et al. (2012, 2014) challenged the idea that hard foods are always dietary fallbacks, showing that another mangabey, Cercocebus atys , ate obdurate foods year‐round and also had thick enamel, presumably as an adaptation to its reliance on mechanically challenging foods as a dietary staple.

These findings spurred further investigation of Lophocebus albigena and Cercocebus atys to determine whether the feeding habits of these fallback vs. habitual hard‐object consumers were associated with differences in dental form (Guatelli‐Steinberg et al. 2022, 2023). These authors argued that if differences in the molars of these two thickly enameled taxa could be associated with fallback vs. habitual hard‐object feeding, such information might be used to infer the nature of durophagy in the fossil record. For example, the fact that the thickly enameled Paranthropus boisei lacks indications of hard‐object feeding such as those gleaned from microwear (Ungar et al. 2008) or suggested by interpretations of stable isotopes (Cerling et al. 2011; Ungar and Sponheimer 2011) has been reconciled by some who posit that P. boisei may have been a fallback hard‐object feeder (Strait et al. 2013; Ungar et al. 2008). Such arguments might be tested (vs. merely offered) if it could be determined that among extant taxa, there are features of dental architecture associated with diets differing in the contribution of hard‐object foods, that is, fallback versus habitual consumption.

Guatelli‐Steinberg et al. (2022, 2023) identified differences in crown strength, occlusal basin enamel thickness, molar sidewall flare, estimated critical fracture loads, elastic modulus, hardness, and elasticity index between Cercocebus and Lophocebus and the non‐durophagous Cercopithecus. These authors concluded that Cercocebus atys, the habitual hard‐object feeder, exhibited greater fracture resistance than both Lophocebus albigena and Cercopithecus (Buzzard 2006; Gautier‐Hion et al. 1981; McGraw et al. 2007), the latter comprising species that consume primarily fruit and other soft objects (Buzzard 2006; Gautier‐Hion et al. 1981; McGraw et al. 2007). Differences in fracture resistance among these taxa were most pronounced in the “functional” cusp, which is the primary cusp involved in crushing and grinding foods (Kono 2004; Schwartz 2000).

Functional cusps have been defined in terms of their role in the chewing cycle (Schwartz 2000). There are three distinct strokes within the chewing cycle (Figure 1): the Closing Stroke, the Power Stroke, and the Opening Stroke (Hillson 1996). During the Closing Stroke, the tips of the buccal and lingual cusps on the upper and lower molars are brought into contact with each other. The next stroke, the Power Stroke, is divided into two phases: Phase I (which itself has two distinct stages) and Phase II. During the first stage of Phase I, molar cusps slide against each other as the teeth move towards centric occlusion, producing a shearing force. At the end of the second stage of Phase I, the “functional” cusps come into full centric occlusion and food particles are crushed in the occlusal basin of the opposing tooth crown. During Phase II, the functional cusps are involved in a grinding action, as the lingual surfaces of the buccal cusps of the lower molar grind against the buccal surfaces of the lingual cusps of the upper molar (see Figure 1). During the final stroke, the Opening Stroke, teeth end contact as the jaw moves to its maximum gape (Hillson 1996).

FIGURE 1.

FIGURE 1

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Diagram of Power Stroke Phases. This figure shows the distinct phases of the Power Stroke of the chewing cycle; shearing and crushing occur in Phase I while grinding occurs in Phase II. Source: Fiorenza et al. (2015). Permission to use image granted by Luca Fiorenza.

We note that the designation “functional” and “non‐functional” is somewhat of a misnomer, as the entire crown, of course, is functional in some capacity. Non‐functional cusps (the upper molar's buccal cusps and lower molar's lingual cusps) are indeed functional in that they are involved in both shearing and crushing action during Phase I (Macho and Shimizu 2009). We use the terms “functional” and “non‐functional” cusps here as a convenience so that we can more easily relate the present study to previous work on these samples (Guatelli‐Steinberg et al. 2022, 2023).

Understanding the stages and phases of the Power Stroke is an integral part of the present study's theoretical considerations, as this work focuses on the angle between enamel prisms (Figure 2) and wear facets that are produced during chewing. Enamel prisms are the basic structural unit of enamel, forming along the path traveled by ameloblasts (enamel‐forming cells) during tooth development and extending from the enamel‐dentin junction (EDJ) to the surface of the tooth (Nanci 2008). Prisms approach wear facets at the enamel surface at various angles in mammals, including primates, as explored by both Macho and Shimizu (2009) and the present study. As did Macho and Shimizu (2009), we examine both Phase I and Phase II wear facets. Phase I wear facets are present on the non‐functional cusps and appear to form in response to shearing as well as crushing (Macho and Shimizu 2009) during Phase I of the chewing cycle. Phase II wear facets form on the functional cusps (Figure 1). Labelling these “Phase II” wear facets implies that wear develops on them during grinding only, but wear on these facets is also produced during crushing, which occurs at the end of Phase I. Indeed, Hylander and Crompton (1980) and Wall et al. (2006) found that in macaques and baboons, respectively, food breakdown occurred mostly during Phase I of the chewing cycle suggesting that Phase II wear facets form predominantly during crushing at the end of Phase I.

FIGURE 2.

FIGURE 2

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Diagram of Enamel Prism Formation. Enamel prisms form in pathways left by ameloblasts during tooth development. Source: O'Meara et al. (2018). This article, which appeared in the Royal Society Open Science was published under a Creative Commons license (CC‐BY 4.0).

Guatelli‐Steinberg et al.'s (2022, 2023) conclusion that differences in fracture resistance were most pronounced in the functional cusp may suggest that selection pressures for fracture resistance are created during crushing and grinding of hard foods, and that these selection pressures are greater for primates that engage in habitual durophagy than those experienced by fallback hard‐object feeders. It is also worth noting that these authors found estimated critical fracture loads to be greater in both Cercocebus atys and Lophocebus albigena than in Cercopithecus, indicating that both fallback and routine hard‐object feeding may act as selection pressures for fracture resistance.

The present study continues this line of inquiry by examining enamel prism angles relative to wear surfaces in primates that consume hard objects routinely ( Cercocebus atys ), as dietary fallback ( Lophocebus albigena ), and rarely (Cercopithecus). Macho and Shimizu (2009) proposed that the orientation of enamel prisms relative to tooth wear surfaces may be adaptations for load resistance. The authors suggested that when the long axes of prisms are arranged parallel to the direction of the load, enamel is stiffer than when prisms are arranged perpendicularly. Possibly as important, they stated “Furthermore, forces applied along the prism axes are less likely to result in tensile stresses forcing prisms apart whereas loading perpendicular to the long axes of prisms will push prisms apart” (2009, 242) potentially initiating fractures that would then travel along prism boundaries. Consistent with their explanation, Carvalho et al. (2000) found that the tensile strength of enamel is greater when loads are parallel to the long axes of enamel prisms. These authors (Carvalho et al. 2000, 254) explain that the fracture resistance of the enamel prism “…when stressed parallel to its long axis can be attributed to the fact that each enamel rod functions as an integral unit and the hydroxyapatite crystals themselves do not cleave during tension, forcing the fracture to preferentially occur within the organic interprismatic substance.”

We recognize that the mechanics of fracture in enamel, a complex material with a hierarchical organization structure (Wilmers and Barmann 2020), are not simply a matter of prism orientation to wear surfaces. We also recognize that enamel decussation is the primary toughening mechanism that impedes the propagation of cracks within tooth enamel (Bajaj and Arola 2009). That said, wear surfaces traverse the outer enamel region of radial enamel through the transition to the decussated enamel closer to the enamel‐dentin junction (Figure 3). It is in the radial and transitional enamel where prism angles are expected to be oriented at higher angles to the wear surface, parallel to the direction of crushing based on Macho and Shimizu's arguments. (Figure 3). We note that radial enamel “… is essential for proper dental function because prisms have high compressive strength that minimizes the risk of failure when transferring bite forces to food particles. High compressive strength means that prisms will resist deformation better when they bear loads in the same direction as their long axis” (Foster 2022, 15).

FIGURE 3.

FIGURE 3

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Diagram of expected prism angulation to molar wear facets. Diagram showing expected prism angles in relation to wear facets based on theoretical considerations of Macho and Shimizu (2009). The dotted blue lines demarcate the angle between the flat surface of each wear facet and the orientation of enamel prisms to that surface. Macho and Shimizu (2009) predicted that this angle would not be as wide for the Phase I wear facet of a non‐durophagous monkey (shown in the molar at left) as it would be in a durophagous monkey (shown in the molar on the right). In the durophagous monkey, the angle is wider because enamel prisms are expected to meet both Phase I and Phase II wear facets at high angles. Source: Guatelli‐Steinberg et al. (2019) (illustration by Mackie O'Hara).

It is also possible that the greater stiffness of enamel where prisms are oriented parallel to the loading axis would more efficiently transfer bite forces into hard food objects. That is, less energy would be dissipated because the enamel would resist deformation when using high bite forces to bite into hard foods. A similar argument related to bite force (though not hard foods in particular) was advanced by Foster (2022) who found that enamel in the cusps of primate molars is “stiffer and harder” than enamel at the crown base. He argues that the greater stiffness and hardness of enamel in the cusps allow for “the transmission of bite forces into food particles, while resisting failure due to wear and fracture.” (Foster 2022, 89).

The angles that prisms meet wear surfaces may also affect abrasion resistance. In a paper using an FEA approach, Shimizu et al. (2005) found that enamel with the greatest resistance to abrasion had prisms oriented at low angles (less than 45°) to wear surfaces. This finding seems inconsistent, however, with previous work (by Boyde and Fortelius 1986; Maas 1991; Xia et al. 2017) suggesting that crystallites within enamel prisms, which are generally oriented parallel to prism long axes, would be more easily “…removed, or plucked, from the surface” when enamel prisms approach occlusal surfaces at lower angles (Foster and Constantino 2020, 79). Indeed, Foster and Constantino (2020) found that enamel was easier to scratch in regions where prisms were at low angles to the enamel surface and harder to scratch when prisms were at higher angles. Thus, high prism angles to wear surfaces may not only afford protection against fracture and improve the transfer of bite forces into food, but also, at the level of the enamel crystallite, they may protect against abrasion.

In their study, Macho and Shimizu (2009) measured prism angles relative to wear surfaces in a sample of Potamochoerus porcus , two extant primate taxa, and two extinct South African hominins. Across all taxa except pigs, Phase II wear facets had similarly high prism angles relative to wear surfaces, congruent with the idea that the vertically‐oriented loads produced during crushing at the end of Phase I of the chewing cycle create selection pressures for higher prism angles. The most marked difference across taxa occurred in the prism angles relative to Phase I wear facets. Macaca fuscata and Australopithecus africanus were found to have relatively low prism angles relative to Phase I facets. P. robustus , however, was found to have high prism angles relative to both Phase II as well as Phase I facets, which Macho and Shimizu (2009) interpreted as an adaptation for processing hard foods requiring vertically oriented crushing loads.

Here, we compare enamel prism angles relative to wear surfaces in three cercopithecoid taxa with known diets (see below): Cercocebus atys, Lophocebus albigena, and a combined sample of three Cercopithecus species. Our purpose was to: (1) test whether high prism angles in both Phase I and Phase II wear facets are present in those taxa known to consume hard objects (as per Macho and Shimizu 2009), and (2) determine whether there are differences in prism angles relative to wear facets between the habitual ( Cercocebus atys ) and fallback ( Lophocebus albigena ) hard‐object‐feeding taxa. We would expect no difference in prism angles if fallback and routine hard‐object feeding create the same selection pressures on teeth.

The following overarching hypothesis is investigated: If hard object feeding leads to similar enamel prism orientation in both fallback ( Lophocebus albigena ) and routine ( Cercocebus atys ) hard‐object feeders, then prism angles relative to wear surfaces are expected to be high in both species for both Phase I and Phase II wear facets relative to soft‐object feeders (Cercopithecus). This prediction is based on Macho and Shimizu's argument that both Phase I and Phase II wear facets are used to process vertically oriented loads and that the presumed hard‐object feeder, P. robustus , has high prism angles relative to wear surfaces in both Phase I and Phase II wear facets.

2. Materials and Methods

The study sample consisted of 13 upper molars from adult Cercocebus atys , 13 from adult Lophocebus albigena , and 11 from three guenon species, Cercopithecus cephus , Cercopithecus petaurista , and Cercopithecus diana. Although originally lower molars were included, there were too few (sample sizes under 10) for sufficient comparisons across taxa. Thus, this study focuses on upper molars. The Cercocebus atys , Cercopithecus petaurista , and Cercopithecus diana samples were procured from the Taï Forest of the Ivory Coast. The Lophocebus albigena and Cercopithecus cephus sample was collected near the Mambili River in the Republic of the Congo approximately 50 km north of the town of Makoua. All samples are housed in the Primate Lab at the Department of Anthropology at The Ohio State University.

Molars were physically sectioned across mesial cusps following the steps of Reid et al. (1998). Teeth were first embedded in Buehler Epoxicure epoxy resin. A Buehler IsoMet low‐speed saw with a diamond‐wafering blade of 5‐in diameter was used to cut teeth. An irregular sample chuck was used to mount the teeth to the saw to align the marked plane to the blade. After the first cut, Gorilla epoxy was used to mount the side of the block with the sharpest dentin horn onto a slide and then cut a second time parallel to the first. The sample was then ground in a target holder using CarbiMet abrasive papers with progressively finer grit until enamel prisms were visible. Buehler alumina micropolish was used to polish the sample before the slide was dehydrated in an ethanol series and rinsed in Histoclear. Immersion oil was then used to cover‐slip the slide. A Motic BA 310 Microscope fitted with a Moticam camera was used to take 10× montages for measurements of prism and wear angles (Table 1).

TABLE 1.

Full dental sample.

Genus Species Specimen Teeth
Cercocebus atys 2008 ULM3
Cercocebus atys 2016 ULM3
Cercocebus atys 2106 ULM3
Cercocebus atys 2108 URM2
Cercocebus atys 16–9 ULM3
Cercocebus atys 2010–2 ULM2
Cercocebus atys 22–29 ULM2, ULM3
Cercocebus atys 23–10 URM2
Cercocebus atys 24–3 URM2
Cercocebus atys 94–7 ULM2
Cercocebus atys 94–9 URM2
Cercocebus atys TP‐91 URM2
Lophocebus albigena 640 ULM2, ULM3
Lophocebus albigena 642 ULM3, URM2, URM3
Lophocebus albigena 643 URM2, URM3
Lophocebus albigena 692 ULM2, ULM3
Lophocebus albigena 85–1 ULM3
Lophocebus albigena 85–17 ULM3, URM2
Lophocebus albigena 85–7 URM2
Cercopithecus diana 1051 ULM3, URM2
Cercopithecus diana 2127 URM3, URM3
Cercopithecus diana 22–26 URM3
Cercopithecus diana 27–5 URM2, URM3
Cercopithecus diana 94–3 ULM3
Cercopithecus petaurista 22–14 ULM3, URM2
Cercopithecus diana 22–24 ULM2
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The computer software ImageJ FIJI was used to measure prism angles relative to wear surfaces as well as the angle of tooth wear. Our inclusion of wear facet angles in our analyses of prism angles (see below) was intended to take variation in wear angles among genera into account. In other words, we aimed to assess whether prism angles differed among genera across the range of wear angles that our samples exhibited.

The angle between the flat surface of the wear facet and the enamel prisms (which run parallel to each other and extend from the EDJ to the outer surface of the enamel) was used for the measurement of prism angles relative to wear surfaces (Figure 4). Wear angles were measured as the angle at which the line extending across the flat surface of the wear facet intersects the line extending along the EDJ. The line along the EDJ was drawn between two points: a point on the EDJ 0.2 mm cervical to the dentin horn—or at the tip of the dentin breach, if exposed—and a point on the EDJ 1 mm cervical to the first point. The first author measured all molars that were used in the analysis after multiple training sessions in which measurements were compared for consistency on a sample of teeth measured by both the first and last authors.

FIGURE 4.

FIGURE 4

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Images of Specimen 16–9 of a Cercocebus atys third molar (top) and Specimen 22–26 Cercopithecus diana third molar (bottom) with prism and wear angle guiding lines. The red line is drawn along the enamel prism path, the green line along the Phase II wear facet, and the blue line along the EDJ. Lines are drawn more thickly than were used during measurement to highlight them. The angle between the red line (prism path) and green line (wear facet) is the enamel prism angle, while angle between the green line (wear facet) and blue line (EDJ) represents the wear angle.

3. Statistical Methods

The data were sorted into those obtained from functional vs. non‐functional cusps. The Phase II facets are on the functional cusps, while the Phase I facets are located on the non‐functional cusps. Two first molars (M1) were removed from the sample so that only second (M2) and third (M3) molars were included. Two outlier measurements were also removed from the sample. Descriptive statistics were first produced for four sets of upper molar data: upper functional cusp prism angle, upper non‐functional cusp prism angle, upper functional cusp wear angle, and upper non‐functional cusp wear angle.

We first graphed these relationships using scatter plots with convex polygons. Repeated measures regression analysis was then used to analyze differences among genera in prism and wear angles of upper molars. Repeated measures analyses take the correlation structure of repeated measures (angles of M2 and M3 for the same individuals) into account. The Mixed procedure in SAS 9.4 was used to perform these regressions. First, a repeated‐measures regression of prism angles on tooth, genus, and the interaction of tooth and genus in upper functional cusps was used to test for fixed effects. Next, pairwise comparisons between each genus were conducted. A second regression analysis was then conducted for prism angle as a function of tooth, genus, and wear angle. Following that, we again calculated the pairwise differences among genera. All tests were then performed for non‐functional cusps. The residuals for every regression were saved and tested for normality. In all cases, the Shapiro–Wilk statistics had p values greater than 0.05, indicating no significant departures from normality for any of these regression analyses.

4. Results

Descriptive statistics for prism angles and wear angles of upper molars are provided in the Tables 2 and 3.

TABLE 2.

Descriptive statistics for prism angles.

Genus N (total) Wear facet Mean SD
Cercocebus 12 Phase I (on NF cusp) 47.6 12.8
Cercocebus 13 Phase II (on F cusp) 55.3 10.3
Lophocebus 13 Phase I (on NF cusp) 36.4 14.6
Lophocebus 11 Phase II (on F cusp) 39.5 13.0
Cercopithecus 8 Phase I (on NF cusp) 31.3 12.2
Cercopithecus 10 Phase II (on F cusp) 37.9 7.5
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TABLE 3.

Descriptive statistics for wear angles.

Genus N (total) Wear facet Mean SD
Cercocebus 13 Phase I (on NF cusp) 83.5 17.4
Cercocebus 13 Phase II (on F cusp) 83.6 11.0
Lophocebus 13 Phase I (on NF cusp) 76.4 25.5
Lophocebus 11 Phase II (on F cusp) 60.8 15.2
Cercopithecus 7 Phase I (on NF cusp) 92.5 12.07
Cercopithecus 7 Phase II (on F cusp) 84.0 10.4
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Plotting of prism angles relative to wear angles in Figures 5 and 6 reveals a separation of prism angles relative to wear angles among genera, which is especially apparent in the functional cusp as can be seen in Figure 5. Across a range of similar wear angles in the functional cusp, prism angles are higher in Cercocebus than they are in Cercopithecus with no overlap between the two genera. Lophocebus prism angles overlap with those of Cercopithecus, but show minimal overlap with Cercocebus. Figure 6, the scatterplot of prism angles vs. wear angles for the non‐functional cusp, shows greater overlap among genera, but with Cercocebus angles generally greater than those of Lophocebus and Cercopithecus. It is important to note that there appear to be differences among genera in prism angles across the range of wear angles in our sample. In other words, it does not appear that prism angle differences among genera are simply the result of wear angle differences among them. It is also notable that in Figure 6, for the non‐functional cusps, there appears to be an inverse relationship between prism angle and wear angle: as wear angles increase, prism angles tend to decrease.

FIGURE 5.

FIGURE 5

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Scatterplot of prism angles vs. wear angles for the functional cusp (Phase II wear facet). This graph shows separation of prism angles among genera across a range of wear angles. Note the higher angles for Cercocebus.

FIGURE 6.

FIGURE 6

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Scatterplot of prism angles vs. wear angles for the non‐functional cusp (Phase I wear facet). This graph shows greater overlap in prism angles on non‐functional cusps compared to functional cusps and appears to reveal an inverse relationship between prism angle and wear angle: As wear angles increase, prism angles decrease. Again, note the higher angles among Cercocebus.

The regression of functional cusp (Phase II wear facet) prism angle on tooth and genus shows that only genus has a statistically significant (p = 0.0015) fixed effect on prism angle. Pairwise comparisons of this effect reveal significant differences between Cercocebus and each of the two other genera (Cercocebus vs. Lophocebus, p = 0.0082; Cercocebus vs. Cercopithecus, p = 0.0037). There is no significant difference between Lophocebus and Cercopithecus. Table 4 shows the results of the repeated measures regression analysis in the Mixed procedure. Table 5 shows the results of pairwise comparisons among genera.

TABLE 4.

Repeated measures regression analysis for fixed effects of tooth, genus, and the interaction of tooth and genus on functional cusp (Phase II) prism angles.

Effect DF numerator DF denominator F value p
Tooth 1 3 0.66 0.4759
Genus 2 24 8.66 0.0015
Tooth*Genus 2 3 0.39 0.7047
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TABLE 5.

Pairwise comparisons of each genus for fixed effects in Table 4.

Effect Genus Genus Estimate Standard DF t value Pr > |t| Adjust. Adj p
Genus Cercocebus Cercopithecus 17.9787 4.8606 24 3.66 0.0012 Bonferroni 0.0037
Genus Cercocebus Lophocebus 16.3877 4.9064 24 3.34 0.0027 Bonferroni 0.0082
Genus Cercopithecus Lophocebus −1.4101 5.2499 24 −0.27 0.7905 Bonferroni 1.0000
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The regression of non‐functional cusp (Phase I wear facet) prism angle on tooth and genus reveals no statistically significant fixed effects on prism angle. Pairwise comparisons demonstrate no significant differences among genera (for Bonferroni‐adjusted p values). Table 6 summarizes the results of the repeated measures regression analysis in the Mixed procedure, while Table 7 summarizes the results of the pairwise comparisons among genera.

TABLE 6.

Repeated measures regression analysis for fixed effects of tooth, genus, and the interaction of tooth and genus on non‐functional cusp (Phase I) prism angles.

Effect DF numerator DF denominator F value p
Tooth 1 4 0.20 0.4759
Genus 2 22 3.34 0.0543
Tooth*Genus 2 4 0.91 0.4728
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TABLE 7.

Pairwise comparisons of each genus for fixed effects in Table 6.

Effect Genus Genus Estimate Standard DF t value Pr > |t| Adjust. Adj p
Genus Cercocebus Cercopithecus 16.0695 6.5419 22 2.46 0.0224 Bonferroni 0.0672
Genus Cercocebus Lophocebus 10.9068 6.2141 22 1.76 0.0932 Bonferroni 0.2795
Genus Cercopithecus Lophocebus −5.1627 6.8763 22 −0.75 0.4607 Bonferroni 1.0000
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A regression of functional cusp (Phase II wear facet) prism angle on tooth, genus, and wear angle reveals that only genus (p = 0.0002) has a statistically significant fixed effect on prism angle. Pairwise comparisons of this effect reveal significant differences between Cercocebus and each of the two other genera. Bonferroni‐adjusted p values for each comparison were Cercocebus vs. Lophocebus, p = 0.0025 and Cercocebus vs. Cercopithecus, p = 0.0007. There is no significant difference between Lophocebus and Cercopithecus. Table 8 summarizes results of the repeated measures regression analysis in the Mixed procedure while Table 9 contains results of the pairwise comparisons among genera.

TABLE 8.

Repeated measures regression analysis for fixed effects of tooth, genus, and wear angle on functional cusp (Phase II) prism angles.

Effect DF numerator DF denominator F value p
Tooth 2 2 0.17 0.8533
Genus 2 23 13.07 0.0002
Wear angle 1 2 3.19 0.2159
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TABLE 9.

Pairwise comparisons of each genus for fixed effects in Table 8.

Effect Genus Genus Estimate Standard DF t value Pr > |t| Adjust. Adj p
Genus Cercocebus Cercopithecus 22.3241 5.1120 23 4.37 0.0002 Bonferroni 0.0007
Genus Cercocebus Lophocebus 22.6185 5.8764 23 3.85 0.0008 Bonferroni 0.0025
Genus Cercopithecus Lophocebus 0.2943 6.5250 23 0.05 0.9644 Bonferroni 1.0000
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Regarding the non‐functional cusp (Phase I wear facet), the regression of prism angle on tooth, genus, and wear angle yielded statistically significant fixed effects for both genus and wear angle. Bonferroni adjusted p values are p = 0.0163 for genus and p = 0.0272 for wear angle. Comparisons among genera demonstrate a significant difference only between Cercocebus and Cercopithecus (p = 0.0400). Table 10 summarizes the results of the repeated measures regression analysis in Mixed procedure while Table 11 provides the results of the pairwise comparisons among genera.

TABLE 10.

Repeated measures regression analysis for fixed effects of tooth, genus, and wear angle on non‐functional cusp (Phase I) prism angles.

Effect DF numerator DF denominator F value p
Tooth 1 6 0.00 0.9933
Genus 2 21 5.04 0.0163
Wear angle 1 6 8.43 0.0272
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TABLE 11.

Pairwise comparisons of each genus for fixed effects in Table 10.

Effect Genus Genus Estimate Standard DF t value Pr > |t| Adjust. Adj p
Genus Cercocebus Cercopithecus 15.8513 5.8649 21 2.70 0.0133 Bonferroni 0.0400
Genus Cercocebus Lophocebus 31.2584 5.2138 21 2.54 0.0190 Bonferroni 0.0569
Genus Cercopithecus Lophocebus −2.5965 6.2516 21 −0.42 0.6821 Bonferroni 1.0000
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5. Discussion

This study had two main objectives. The first was to examine enamel prism angles relative to wear surfaces in three cercopithecoid genera to test whether hard‐object feeding is associated with high prism angles in both Phase I and II wear facets. The second was to determine whether there are differences between the habitual hard‐object feeding Cercocebus atys and the fallback hard‐object feeding Lophocebus albigena in prism angles relative to wear facets. It was hypothesized that if hard‐object feeding resulted in similar prism orientations in fallback and routine hard‐object feeders, prism angles relative to Phase I and Phase II wear facets would be high in both Cercocebus atys and Lophocebus albigena relative to soft‐object feeders.

Our data did not fully support our overarching hypothesis. We did find that across both Phase I and Phase II prism angles, Cercocebus atys had higher prism angles than Cercopithecus, both with and without incorporating wear angle into the regressions. However, there were no statistically significant differences between the fallback hard‐object feeder Lophocebus albigena and the soft‐object feeder Cercopithecus in any of the pairwise comparisons. Thus, our expectation that higher prism angles relative to both Phase I and Phase II wear surfaces would be associated with hard‐object feeding compared to soft‐object feeding held only for Cercocebus atys as compared to Cercopithecus.

We also found an inverse relationship between prism angle and wear angle, but only for Phase I wear facets. A relationship between wear angle and prism angle was anticipated because these two measurements share one leg of the same angle (Figure 4). Indeed, our inclusion of wear facet angles in the analysis of prism angles was intended to take variation in wear angles among genera into account so that we could assess prism angle differences among them that were not simply due to differences in the angles of their wear facets. Figures 5 and 6, together with the regression analyses that included wear angles as a predictor of prism angles all suggest that differences between Cercocebus and the other two genera are not merely a function of wear angle differences among these genera.

We note that our study included only upper molars. O'Hara (2021) found that across a sample of catarrhine species, durophagy correlated with tooth size, tooth shape, and enamel thickness more strongly in lower molars than in upper molars. Thus, it is possible that lower molars might carry stronger signals of features associated with durophagy, although several features related to durophagy in terms of fracture resistance have previously been found in the upper molars of Cercocebus atys (Guatelli‐Steinberg et al. 2022, 2023).

Our findings are generally consistent with those of Macho and Shimizu (2009). In their analysis of enamel prism angles, the presumed hard‐object feeding hominin Paranthropus robustus demonstrated higher prism angles across both Phase I and Phase II facets than any of the other taxa (Macho and Shimizu 2009). In the present study, the known habitual hard‐object feeding Cercocebus atys also was shown to have higher prism angles across both wear facets than the other taxa. These data lend further support to the idea that vertically oriented loads produced during the crushing of hard foods are associated with high prism angles in both Phase I and Phase II wear facets (Macho and Shimizu 2009). However, as noted earlier, abrasion may also be thwarted by high prism angles, hindering the removal of enamel crystallites from the enamel surface (Foster and Constantino 2020). Given that Cercocebus atys consumes fruit that has fallen on the forest floor, gritty adherents are likely to abrade enamel when these fruits are masticated (Daegling et al. 2011; Geissler et al. 2018). Thus, although the high prism angles of Cercocebus atys in both Phase I and Phase II wear facets are consistent with our hypothesis that they are related to hard‐object feeding in terms of conferring greater stiffness and strength to the enamel, they are also consistent with affording resistance to abrasion.

One difference between our results and those of Macho and Shimizu's (2009) is the lack of uniformity in Phase II prism angles across primate taxa. While these authors found similarly high Phase II prism angles across all primates surveyed (Macho and Shimizu 2009), the present study found that Phase II prism angles varied across taxa (see Figure 5). Macho and Shimizu recorded average Phase II prism angles between 74.4 ( A. africanus ) and 82.2 degrees in T. oswaldi across sampled primate taxa, while the present study found average Phase II prism angles of 55.3 in Cercocebus, 39.5 in Lophocebus, and 37.9 in Cercopithecus. Phase I prism angles in the present study also differed from Macho and Shimizu's. The authors found that M. fuscata exhibited the smallest Phase I prism angles at 34.8 degrees and that P. robustus exhibited the largest average Phase I prism angles at 74.4 degrees. In the present study, Cercocebus was found to have average Phase I prism angles of 47.6 degrees, Lophocebus of 36.4 degrees, and Cercopithecus of 31.3 degrees.

The findings of the present study are consistent with Guatelli‐Steinberg et al.'s (2022, 2023) studies on the same taxa. These authors found that various aspects of molar form suggested enhanced resistance to fracture in Cercocebus atys as compared with Lophocebus albigena and Cercopithecus. In terms of crown strength, these authors found greater Absolute Crown Strength (ACS: Schwartz et al. 2020) as well as greater estimated PMF (the load at which margin fracture is estimated to lead to crown failure) in Cercocebus vs. both Lophocebus and Cercopithecus. They also found greater proportional enamel thickness in the molar occlusal basins of Cercocebus as compared to Lophocebus and Cercopithecus. Enamel within the trigon basin of Cercocebus atys molars also appears to be more decussated (Guatelli‐Steinberg et al. 2023), which would thwart the propagation of cracks. As noted by these authors, although the hardness of Cercocebus atys and Lophocebus albigena diets has not yet been directly compared, the higher frequency with which Cercocebus atys consumes hard foods would expose its molars to greater opportunity for fracture as well as increase their probability of fatigue failure (Guatelli‐Steinberg et al. 2022).

While the aforementioned features appear to be associated with fracture resistance, enamel within the trigon basin of Cercocebus atys appears to be more wear resistant than that of the other two genera. Cercocebus atys trigon basin enamel was found to have greater hardness and a greater hardness/elasticity index than that of Lophocebus albigena and Cercopithecus (Guatelli‐Steinberg et al. 2023). In the context of these previous studies and the hypothesized link between abrasion resistance and high prism angles (Foster and Constantino 2020), it is not clear if the evolution of high Phase I and Phase II prism angles in Cercocebus atys had more to do with hard‐object feeding per se or simply with wear resistance, but they may have been related to both.

Given the possibility of equifinality—that high prism angles may be associated with selective pressures related to hard‐object feeding or wear resistance, or both—the value of prism angles in fossil hominin dietary reconstruction is limited. This is similar to the problem of evaluating the dietary signal of thick enamel (Pampush et al. 2013). Additional evidence, from enamel microwear would be necessary to address this question. For example, Macho and Shimizu's (2009) finding of high prism angles across both wear facets in P. robustus is consistent with the presence of deep pitting microwear, indicative of hard food consumption (Grine and Kay 1988; Scott et al. 2005). In this regard, it is interesting that the complexity of microwear textures on P. robustus molars resembles that of Cercocebus atys (Daegling et al. 2011). Both species have similarly complex microwear and high prism angle orientations relative to wear surfaces.

Despite similarities in the craniodental morphology of P. robustus and P. boisei, microwear and stable isotope data suggest significant differences in diet. Microwear analyses of P. boisei reveal fine striations but none of the deep pitting that would indicate the consumption of hard foods nor the deep striations that would indicate grazing of tough foods (Ungar et al. 2008). P. boisei's carbon isotope signal indicates a diet consisting of 80% C4 foods (Cerling et al. 2011), which typically include tropical grasses and sedges and the animals that consumed these foods (Strait et al. 2013). Obdurate foods such as hard fruits, nuts, and seeds are C3 foods; thus, it has been argued, if hard objects were a dietary staple, we would expect to see a sizeable C3 isotope signal in the enamel of P. boisei (Cerling et al. 2011; Ungar and Sponheimer 2011).

The consumption of hard objects as a fallback food during times of resource scarcity has been proposed as a solution to the problem of mismatch between the highly robust craniodental features of Paranthropus robustus and evidence from microwear and stable carbon isotopes (Strait et al. 2013). Proponents of this perspective argue that the available direct indicators of diet do not provide conclusive evidence against the infrequent, yet evolutionarily critical consumption of hard foods. Dental microwear is limited to dietary signals produced the weeks or even days before an individual's death (Grine 1986) and the high proportion of C4 foods in P. boisei's isotope signal does not exclude the possibility of hard C3 foods constituting some portion of the remaining 20% of its diet (Strait et al. 2013) or the inclusion of hard C4 foods, such as the hard seeds of grasses or corms of some C4 plants, in its diet. It is possible that some of the aspects of molar form that differ between Cercocebus atys and Lophocebus albigena , such as enamel decussation, occlusal basin enamel thickness, and crown strength, might ultimately help distinguish fallback from habitual hard‐object feeding in fossil species. However, our finding that the prism angles of the fallback hard‐object feeding Lophocebus albigena and soft‐object feeding Cercopithecus were not significantly different suggests that prism angles would not be useful for discriminating between fallback hard‐object feeding (as has been suggested for P. boisei) and soft‐object feeding in the fossil record.

6. Conclusion

This study compared enamel prism angles relative to wear facets across five taxa: the habitual hard object feeding Cercocebus atys, the fallback hard‐object feeding Lophocebus albigena, and three soft‐object feeding Cercopithecus species. Our objectives were: (1) to test whether hard‐object feeding was associated with higher prism angles and (2) to test whether fallback and habitual hard‐object feeding were associated with similar prism angles. We hypothesized that if the latter proposition were true, both Cercocebus atys and Lophocebus albigena would have high prism angles relative to wear facets. Our data showed that while Cercocebus atys does have significantly higher prism angles than the other taxa, those of Lophocebus albigena were indistinguishable from the pooled sample of soft‐object feeding Cercopithecus. Further, unlike Macho and Shimizu's (2009), we found that both Phase II and Phase I prism angles varied across taxa. Our findings suggest that high prism angles may be associated with habitual hard‐object feeding but not with fallback hard‐object feeding. Additional data on prism angle orientation in taxa with greater dietary diversity would help clarify relationships between primate enamel prism angles and diet.

Author Contributions

Jacob Scheinblum: conceptualization, investigation, funding acquisition, writing – original draft, methodology, validation, visualization, writing – review and editing, formal analysis. W. Scott McGraw: conceptualization, investigation, funding acquisition, writing – review and editing. Kaita Gurian: investigation, methodology, validation. Debbie Guatelli‐Steinberg: conceptualization, investigation, funding acquisition, writing – original draft, methodology, validation, visualization, writing – review and editing, data curation, supervision, formal analysis.

Conflicts of Interest

The authors declare no conflicts of interest.

Acknowledgments

This project was funded by NSF grants # 1945008, BCS 0921770, and 0922429 and Emory National Primate Research Center. Additional funding was provided by Ohio State University's Honors and Scholars Program, as well as OSU's Anthropology Department's Hughes Memorial Fund and the DEM3 funds to J.S. Thanks to Dwayne Arola, for his helpful suggestions in the development of this work.

Scheinblum, J. , McGraw W. S., Gurian K., and Guatelli‐Steinberg D.. 2025. “Enamel Prism Angle Variation and Hard‐Object Feeding in Cercopithecoids With Known Diets.” American Journal of Biological Anthropology 188, no. 3: e70167. 10.1002/ajpa.70167.

Funding: This project was funded by NSF grants # 1945008, BCS 0921770, and 0922429; the Ohio State University College of Arts and Sciences; and Emory National Primate Research Center. Additional funding was provided by Ohio State University's Honors and Scholars Program, as well as OSU's Anthropology Department's Hughes Memorial Fund and the DEM3 funds to J.S.

Data Availability Statement

The data that support the findings of this study are available from the corresponding author upon reasonable request.

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Associated Data

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Data Availability Statement

The data that support the findings of this study are available from the corresponding author upon reasonable request.

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