THE ANATOMICAL RECORD 298:463–478 (2015)

Incisor Crown Bending Strength Correlates with Diet and Incisor Curvature in Anthropoid Primates ANDREW S. DEANE* Department of Anatomy and Neurobiology, University of Kentucky, College of Medicine, Lexington, Kentucky

ABSTRACT Anthropoid incisors are large relative to the postcanine dentition and function in the preprocessing of food items. Previous analyses of anthropoid incisor allometry and shape demonstrate that incisor morphology is correlated with preferred foods and that more frugivorous anthropoids have larger and more curved incisors. Although the relationship between incisal crown curvature and preferred foods has been well documented in extant and fossil anthropoids, the functional significance of curvature variation has yet to be conclusively established. Given that an increase in crown curvature will increase maximum linear crown dimensions, and bending resistance is a function of linear crown dimensions, it is hypothesized that incisor crown curvature functons to increase incisor crown resistance to bending forces. This study uses beam theory to calculate the mesiodistal and labiolingual bending strengths of the maxillary and mandibular incisors of hominoid and platyrrhine taxa with differing diets and variable degrees of incisal curvature. Results indicate that bending strength correlates with incisal curvature and that frugivores have elevated incisor bending resistance relative to folivores. Maxillary central incisor bending strengths further discriminate platyrrhine and hominoid hardand soft-object frugivores suggesting this crown is subjected to elevated occlusal loading relative to other incisors. These results are consistent with the hypothesis that incisor crown curvature functions to increase incisor crown resistance to bending forces but does not preclude the possibility that incisor bending strength is a composite function of multiple dentognathic variables including, but not limited to, incisor crown curvature. C 2014 Wiley Periodicals, Inc. Anat Rec, 298:463–478, 2015. V

Key words: incisor curvature; diet; anthropoids; feeding biomechanics; preferred foods

Grant sponsor: National Science Foundation; Grant numbers: BCS-0852866 and BCS-0964944; Grant sponsor: National Geographic Society’s Committee for Research and Exploration, The Leakey Foundation, Dian Fossey Gorilla Fund International’s (DFGFI) Karisoke Research Center, Rwanda Development Board’s Department of Tourism and Conservation, Gorilla Doctors, DFGFI, The George Washington University, New York University College of Dentistry, and Institute of National Museums of Rwanda. C 2014 WILEY PERIODICALS, INC. V

*Correspondence to: Andrew Deane, Department of Anatomy and Neurobiology, University of Kentucky, College of Medicine, MN 224 UK Medical Center Lexington, KY 40536-0298. E-mail: [email protected] Received 30 January 2014; Accepted 12 June 2014. DOI 10.1002/ar.23042 Published online 23 August 2014 in Wiley Online Library (wileyonlinelibrary.com).

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INTRODUCTION Diet is one of the most basic and fundamental ecological parameters defining living primate species. Similarly, any detailed understanding of the ecology and evolution of fossil primates relies on the accuracy of dietary reconstructions of fossil taxa. A comprehensive understanding of the feeding biomechanics and dental functional anatomy of living anthropoids is required to accurately reconstruct the diets of fossil primates. Although considerable attention has been devoted to the functional morphology of living and fossil anthropoid molars and premolars (Groves and Napier, 1968; Kay, 1978; Lucas, 1980, 1982; Wood et al., 1983; Benyon, 1986; Ungar and Kay, 1995; Kay and Ungar, 1997; Benyon et al., 1998; Strait, 1998; Ungar, 1998; Smith, 1999; Ungar and Kiera, 2003; 2004, 2004, 2007; Teaford, 2007; Skinner et al., 2008; Kupczik et al., 2009) comparatively little is known about the functional morphology of anthropoid incisors. The significance of incisor function in living anthropoids, and hominoids in particular, is underscored by their large size relative to the postcanine dentition (Jolly, 1970; Hylander, 1975; Kay and Hylander, 1978; Shea, 1983; Ungar, 1996, 1998; Lucas, 2004; McCollum, 2007). Anthropoid incisors do not act uniformly on all foods although most foods are subject to at least a moderate degree of incisal preparation. It is therefore reasonable to predict that the morphology of these teeth are, at least in part, a function of the unique selective pressures imposed by the mechanical loading specific to different diets, or else some combination of factors of which dietary mechanical loading is a significant component (Jolly, 1970; Hylander, 1975; Eaglen, 1984; Deane, 2005, 2007, 2009a,b; 2012). Analyses of anthropoid incisor size relative to post-canine dental proportions and body mass demonstrate that more frugivorous anthropoids (i.e. Pan, Ateles, Cercopithecus) have proportionately larger incisors than do more folivorous anthropoids within the same clade (i.e. Gorilla, Alouatta, Colobus) (Jolly, 1970; Hylander, 1975; Kay and Hylander, 1978; Eaglen, 1984). More recent attempts to identify anatomical correlates between incisor form and diet have employed non-linear measurements of incisor crown shape (i.e. mesiodistal [MD] and cervico-incisal [CI] crown curvature) and demonstrate that there is a significant correlation between anthropoid incisor crown curvature and preferred foods. (Deane et al., 2005; Deane, 2007, 2009a,b; Schubert et al., 2010, 2012). Incisor crown curvature is particularly sensitive to subtle differences in diet among closely related taxa that rely on similar fallback resources (i.e. Gorilla gorilla gorilla vs. Gorilla beringei beringei; Alouatta caraya vs. Alouatta seniculus) (Deane et al., 2005; Deane, 2007, 2009a,b, 2012). Analyses of living anthropoid incisor crown curvature demonstrate that more pronounced MD and CI crown curvatures are positively correlated with a proportionate increase in frugivory. Hard-object frugivores have more pronounced incisal curvatures than soft-object frugivores, and mixed folivore/frugivores exhibit intermediate degrees of mesiodistal and cervico-incisal curvature relative to all frugivores and dedicated folivores who are the least curved (Deane, 2007, 2009a, 2012; Deane et al., 2005). While it is difficult to exclude non-dietary factors as potential influences on anthropoid incisor curvature, sig-

nificant correlations between incisor curvature and the mechanical properties of anthropoid diets suggest that crown curvature is governed, at least in part, by feeding biomechanics and diet and that increased incisal curvature functions to resist the elevated mechanical loading associated with harder object foods. This hypothesis is consistent with prior biomechanical analyses of carnivore incisor crown shape. Biknevicus et al. (1996) modeled carnivore incisors as a cantilever beam and determined that incisor bending strength is largely a function of cross-sectional geometry. Any increase in the maximum LL and MD dimensions of the incisor crown results in a proportionate increase in bending strength (van Valkenburgh and Ruff, 1987; Plavcan and Ruff, 2008). Given that an increase in anthropoid MD and CI crown curvature would effectively increase labiolingual crown dimensions, it stands to reason that incisors with increased crown curvature will be more resistant to bending stresses. In a hypothetical model of a cantilevered beam, a 100% increase in LL breadth when MD length, crown height and the force applied to the model are held constant produces a 300% increase in bending resistance in the LL (y) axis and a 100% increase in bending resistance in the MD (x) axis (Fig. 1). Therefore, the correlation between pronounced incisal curvature and frugivorous diets among anthropoids is consistent with the hypothesis that MD and CI crown curvature function to resist the elevated occlusal loading and bending stresses associated with frugivory (Lucas and Teaford, 1994; Ungar, 1995; Strait, 1998; Elgart-Berry, 2004; Lucas, 2004; Wright, 2005; Norconk et al., 2009). Alternatively, increased incisor crown curvature may (i) function to resist dental wear by increasing the relative incisor crown surface area, (ii) increase dietary efficiency by optimizing incisor orientation and occlusion, (iii). serve multiple functional purposes, or(iv) have no functional significance at all. The objective of the present study is to test the hypothesis that incisor crown curvature contributes to an increase in the crown’s resistance to bending stresses by modeling anthropoid incisors as a cantilevered beam following the methods described by Biknevicus et al. (1996; see also van Valkenburgh and Ruff, 1987; Ruff and Plavcan, 2008). If the incisors of anthropoid taxa with increased incisal curvature (i.e. frugivores) do not consistently have an increased resistance to bending stresses then the null hypothesis, that incisor curvature has no functional significance or is the product of some factor or combination of factors (i.e. digestive efficiency, resistance to wear, phylogeny) unrelated to the prevention of crown breakage, cannot be rejected. Either result would represent a solid contribution to our current understanding of the functional morphology of anthropoid incisors as it relates to feeding biomechanics and the mechanical properties of the foods, and would be of considerable value in future dietary reconstructions of fossil anthropoids. A more refined understanding of the functional significance and relative performance capabilities of anthropoid incisors during ingestion is a critical first step towards a more comprehensive understanding of fossil anthropoid paleobiology. The more accurate the interpretations of a taxon’s diet and feeding adaptation, the greater will be the potential for that information to contribute answers to research questions about why these taxa evolved, what made them successful in some

465

ANTHROPOID INCISOR CROWN BENDING STRENGTH

Fig. 1. Resistance to bending in two hypothetical beams with identical mesiodistal length (MD) and crown height (H) but different labiolingual (LL) breadth when force (F) is held constant. Bending strength (S) is calculated for both the labiolingual (Sy) and mesiodistal (Sx) axes. A 100% increase in the LL breadth of beam B results in a 100% increase in the bending resistance in the mesiodistal axis and a 300% increase in bending strength in the labiolingual axis.

cases, and extinct in others, and the connection between diet and the origins of the lineages of living anthropoids.

MATERIALS AND METHODS Sample Linear crown dimensions were collected from hominoid and platyrrhine individuals (n 5 182; 22 species and 15 genera) housed at the American Museum of Natural History (AMNH; New York), Smithsonian Institution (NMNH; Washington, D.C.), Royal Museum for Central Africa (RMCA; Tervuren, Belgium), Powell-Cotton Museum (PC; Birchington, UK), Field Museum of Natural History (FMNH; Chicago, USA), University of Zurich Anthropological Institute and Museum and the Dian Fossey Gorilla Fund International Karisoke Research Center (DFGFI; Musanze, Rwanda). Table 1 lists the number of each incisor crown type available per taxon. Individual taxa were assigned to discrete dietary categories. Hominoids were identified as a soft-object frugivore (SOF), hard-object frugivore (HOF), mixed folivore/ frugivore (MFF), or dedicated folivore (DF) following the dietary group definitions in Deane (2009a). Platyrrhines were identified as a folivore (FOL), hard-object frugivore/omnivore (HOF-OM), soft-object frugivore (SOF) or sclerocarp forager (SF) following the dietary group definitions in Deane (2012). All dietary classifications are based on dietary proportions derived from standard field observation methods (i.e., the total time spent feeding on a given resource, how often a given resource was eaten, fecal content analysis). Table 2 summarizes the dietary classifications for all anthropoid taxa included in this study.

Data Collection Maximum mesiodistal length (MD), maximum labiolingual breadth (LL) and maximum crown height (H) (measured on the labial surface from the cervical line to the incisal margin) were recorded for all maxillary and mandibular incisor crowns on the right side. The left side was substituted when the right side was unavailable. Similarly, M2 length was recorded for use as a body

size indicator (BSI). M2 length was selected as the study BSI because the linear dimensions of primate post canine dentition exhibit relatively low variability and scale isometrically with respect to primate body mass (Kay, 1973; Gingerich and Schoeninger, 1979; Wood, 1979; Gingerich et al., 1982; Gingerich and Smith, 1985). The use of a molar dimensions also increases the probability that the study methods and resulting dataset can be employed in future analyses of fossil anthropoid incisors where preservation of associated non-dental

TABLE 1. A listing of study sample taxa and the sample numbers for individual incisor crown subsets Taxon Alouatta caraya Alouatta fusca Alouatta seniculus Ateles belzebuth Ateles hybridus Ateles marginatus Ateles fusciceps Ateles geoffroyi Lagothrix lagotricha Sapajus apella Cebus olivaceus Saimiri sciurius Chiropotes satanas Cacajao calvus Pithecia pithecia Pan troglodytes Pan paniscus Gorilla gorilla gorilla Gorilla beringei graueri Gorilla beringei beringei Pongo pygmaeus Hylobates muelleri Hylobates moloch Hylobates lar Hylobates hoolock Hylobates agilis Hylobates klossi Symphalangus syndactylus TOTAL

I1

I2

I1

I2

6 2 6 1 1 2 5 6 6 10 6 6 11 10 7 17 13 13 11 17 13 1 2 3 1 2 1 3 182

6 2 6 1 1 2 5 6 6 10 6 6 11 10 7 15 15 12 11 1 11 1 2 3 1 2 1 3 163

6 2 5 1 1 2 5 6 5 10 6 6 11 10 7 12 12 8 7 1 10 1 2 3 1 2 1 3 146

6 2 5 1 1 2 5 6 6 10 6 6 11 10 7 13 13 9 7 1 10 1 2 3 1 2 1 3 150

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TABLE 2. A listing of study sample taxa and their corresponding dietary category Taxon

Primary Diet

Alouatta caraya Alouatta fusca Alouatta seniculus

Folivory Folivory Folivory

Ateles Ateles Ateles Ateles Ateles

Soft-object Soft-object Soft-object Soft-object Soft-object

belzebuth hybridus marginatus fusciceps geoffroyi

Lagothrix lagotricha Sapajus apella

frugivory frugivory frugivory frugivory frugivory

References Bicca-Marques, and Calegaro-Marques, 1994; Bravo, 2003 Galetti et al. 1987; Garcia Chiarello, 1994 Mittermeier and van Roosmalen, 1981; Sailer et al., 1985; Gaulin and Gaulin, 1982; Julliot and Sabatier, 1993 Fonseca, 1983; Milton, 1984; Strier, 1991 van Roosmalen and Klein 1988 van Roosmalen and Klein 1988 Klein and Klein, 1977 Richard, 1970; Hladik and Hladik, 1969; Sailer et al., 1985; Campbell, 2000; Chapman, 1987 Peres, 1994; Di Fiore, 2004 Wright, 1981, 1994

Saimiri sciurius

Soft-object frugivory Hard-object frugivory/ omnivory Hard-object frugivory/ omnivory Omnivory

Chiropotes satanas

Sclerocarp foraging

Cacajao calvus Pithecia pithecia

Sclerocarp foraging Sclerocarp foraging

Pan troglodytes

SOFT-object frugivory

Pan paniscus Gorilla gorilla gorilla

Soft-object frugivory Mixed folivory/frugivory

Gorilla beringei graueri Gorilla beringei beringei Pongo pygmaeus Hylobates sp.

Mixed folivory/frugivory

Mittermeier and van Roosmalen, 1981; Sailer et al., 1985; Lima and Ferrari, 2003 Mittermeier and van Roosmalen, 1981; van Roosmalen et al., 1988; Hershkovitz, 1985; Sailer et al., 1985; Ayers, 1989; Kinzey, 1992 Ayers, 1986, 1989; Barnett et al., 1997; Kinzey, 1992 van Roosmalen et al., 1988; Kinzey, 1992; Mittermeier and van Roosmalen, 1981; Norconk and Kinzey, 1990 Wrangham, 1977; Hladik, 1977; McGrew et al., 1988; Kuroda, 1992; Tutin et al., 1997; Yamakoshi, 1998 Kano and Mulavwa, 1984; Bradian and Malenky, 1984 Williamson et al., 1990; Tutin and Fernandez, 1993; Nishihara, 1995; Remis, 1997 Casmir, 1975; Goodall and Groves, 1977; Yamagiwa et al., 1994

Folivory

Goodall and Groves, 1977; Fossey and Harcourt, 1977; Watts, 1984

Hard-object frugivory Soft-object frugivory

Symphalangus syndactylus

Mixed folivory/frugivory

MacKinnon, 1974; Rodman, 1977; Galdikas, 1978; Ungar, 1995 MacKinnon and MacKinnon, 1978; Raemakers, 1979, 1984 Ungar, 1995; Palombit, 1997 Palombit, 1997; Chivers et al., 1975; Raemakers, 1979, 1984

Cebus olivaceus

Freese and Oppenheimer, 1981; Sailer et al., 1985; Chapman, 1987

elements is often a limiting factor. Each measurement was taken three times and the mean value was used in the final analysis. All linear measurements were taken directly on the specimens using a digital caliper accurate to 0.01 mm. All individuals were allocated to one of four discrete molar wear stages (MWS 1–4) according to the classification criteria described by McCollum (2007) where MWS 1 indicates minimal molar occlusal wear and MWS 4 indicates extensive molar occlusal wear. Only unworn incisors belonging to individuals allocated to MWS 1 and MWS 2 were included in the study sample. Figure 2 illustrates the linear dimensions used in the present study. Van Valkenburgh and Ruff (1987) have previously demonstrated that teeth with relatively simple crown morphology (i.e. unicuspid incisors and canines) can be modeled as a cantilevered beam that is rigidly fixed at one end to the bone of the maxilla or mandible, although such a model does not consider more nuanced aspects of incisor morphology (i.e. apical wedging). Beam strength is a combined function of material properties and cross sectional geometry. The former is assumed to be roughly equivalent across biologically similar structures, meaning that in the present study incisor bending strength is considered to be an exclusive function of cross sectional geometry. Bending

strength (i.e. resistance to bending stress) was calculated for individual crowns using the equation described by Van Valkenbugh and Ruff (1987; see also Biknevicius et al., 1996; Plavcan and Ruff, 2008). Bending stress is defined as the displacement of an object with respect to its longitudinal axis when an external load is applied perpendicularly to that axis. A beam’s resistance to bending is inversely related to the maximum stress sustained by the beam prior to failure (Timoshenko and Gere, 1972). Maximum bending strength (S) is defined as S 5 Z/Fh where F is the applied force, h is the crown height, and Z is the section modulus in the plane of bending. F was set to a constant of 1. Section moduli were estimated separately for the MD (x) and LL (y) axes as:


Zy 5pðLLÞ MD2 =32
Zx 5pðMDÞ LL2 =32 Maximum bending stress around the MD (x) and LL (y) axes were estimated as:

Sy 5Zy =Fh SX 5ZX =Fh

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ANTHROPOID INCISOR CROWN BENDING STRENGTH

TABLE 3. Ordinary least squares regression analysis results Ind. variable LN LN LN LN LN LN LN LN

1

I I1 I2 I2 I1 I1 I2 I2

Sx Sy Sx Sy Sx Sy Sx Sy

r

B

k-OLS

0.910* 0.909* 0.869* 0.875* 0.860* 0.866 0.886* 0.881*

22.319 22.257 22.054 22.150 23.254 23.848 22.630 23.144

1.759 1.804 1.472 1.501 1.871 2.063 1.688 1.851

“*” indicates a variable with a slope that differs significantly (P  0.05) from isometry (= 2.0)

Fig. 2. Linear crown dimensions used to calculate incisor crown bending strength: maximum mesiodistal crown width (MD); maximum labiolingual crown breadth (LL); incisor crown height (H).

Data Analysis All bending strength variables (n 5 8; bending strength about the MD (x) and LL (y) axes for I1, I2, I1, I2) and body size indicator variables (n 5 1; M2 length) were tested for distribution normality and, if they did not satisfy the assumption of distribution normality, were lognormalized. The scaling relationship between the BSI variable (M2 length) and published sex-specific average body mass values (Smith and Jungers, 1997) was assessed using ordinary least squares regression analysis. Differences in the relative incisor bending strengths of individual taxa were assessed using both ratio and residual analyses. Calculated ratios (i.e. where an independent BSI variable is used as the denominator and a dependent variable as the numerator) and residual values derived from the regression of a dependent against an independent variable are both frequently used to control for the effects of isometric size-related scaling (Albrecht et al., 1993; Corruccini, 1987, 1995; Jungers et al., 1995). Size-adjusted ratios were calculated by dividing the log-normalized relative bending strength values for a given individual by the corresponding log-normalized M2 length. The resulting ratios were analyzed separately for the hominoid and platyrrhine datasets using a one-way ANOVA with a post hoc multiple comparison test (i.e. Bonferroni correction). Residual values were obtained from ordinary least squares (OLS) regressions of log-normalized bending strength values against log-normalized M2 length. OLS regression analysis was used because OLS regression lines are more appropriate for removing the effects of the x-axis variable (i.e. body size as represented by the BSI) in order to evaluate residuals uncorrelated with it and the relationship between any two variables that covary with body size (i.e. bending strength and M2 length) (Smith, 1994). OLS regression analyses were performed for each bending strength variable using combined anthropoid datasets including both platyrrhines

and hominoids. Bivariate scatterplots with OLS regression lines of best fit were generated for each variable. Standardized residuals were analyzed separately for the hominoid and platyrrhine datasets using a one-way ANOVA with a post hoc multiple comparison test (i.e. Bonferroni correction). Owing to limited sample sizes, G.b. beringei was excluded from both the residual and ratio analyses of the I2, I1 and I2 datasets. Box plots representing the median, range and 50% confidence interval for taxon specific bending strength values were plotted for all ratio and residual based variables. A phylogenetically corrected ANOVA was not performed because this method cannot directly compare the terminal branches of phylogenetic trees (i.e. “tip data” or individual species). All study analyses performed here were done using individual species instead of oversimplified dietary groupings in an effort to better represent the dietary complexity of the individual taxa in the study sample.

RESULTS The regression of M2 length (dependent variable) against published sex and taxon specific average body masses (independent variable) (Smith and Jungers, 1997) demonstrates that M2 length is an appropriate BSI that departs only minimially from isometry (r 5 0.333) with a slope of 0.373 (r 5 0.954). The results of the ratio and residual based analyses are broadly similar in their representation of the relationships between individual taxa within the hominoid and platyrrhine samples, however the ratio analyses fail to identify many of the statistically significant differences identified in the residual analyses. The ratio analyses, however, do identify statistically significant differences between groupings of taxa with significantly dissimilar body mass (i.e. hominids vs. hylobatids; Saimiri, Pithecia and Chiropotes vs. all other platyrrhines). This suggests that the results of the ratio analyses are strongly influenced by the effects of size-related scaling. It has been suggested that ratios are better at identifying shape similarities among individuals (Jungers et al., 1995), however they are incapable of removing completely the effects of size related scaling in morphometric data (Albrecht et al., 1993). Regression residuals, however, are independent of size and therefore not influenced by comparisons between sample taxa with dissimilar body masses. Given that the current data sample includes taxa that span a

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Fig. 3. Representative example bivariate scatterplots of LN incisor crown bending strengths for I1 about the x and y axes against LN M2 length. Ordinary least squares regression lines of best fit are passed through the raw data space with the 95% confidence intervals indicated by the curved lines above and below.

ANTHROPOID INCISOR CROWN BENDING STRENGTH

469

Fig. 4. Boxplots of standardized residuals for individual hominoid taxa from ordinary least squares regression analyses incisor crown bending strengths for individual crowns (I1, I2, I1, I2) and crown axes (Sx, Sy) against LN M2 length. Darkened bars represent the median value for each group, while the boxes show the 50% confidence interval and the whiskers extend to the highest and lowest values for each taxon, excluding outliers.

considerable range of body masses (hominoids: 5.3– 175.2 kg; platyrrhines: 0.662–9.16kg), and that the results of the residual analyses identify meaningful and diet-specific differences among taxa and are not subject to the influence of size related scaling, only the results of the residual based analyses will be reported here. All but one bending strength variable scale with negative allometry and have ordinary least squares (OLS) regression slopes that differ significantly (P  0.05) from isometry (k5 2.0). OLS regression slopes range between 1.472 and 2.063 (r 5 0.860 to 0.910). Only the OLS regression slope for the analysis of LN I1 Sy bending strength (k52.063; r 5 0.866) is not statistically different from isometry and negatively allometric. Table 3 reports all OLS regression results for each of the eight incisor crown and bending axis specific strength variables. Bivariate scatterplots of log normalized bending strength variables (dependent variable) against log normalized M2 length (independent variable) demonstrate a general separation of more frugivorous and more folivorous anthropoids (Fig. 3). More frugivorous anthropoids are primarily positioned on or above the OLS regression

line and more folivorous anthropoids are most often positioned on or below the OLS regression line. The majority of the specimens representing Saimiri, Sapajus, Cebus, P. paniscus, P. troglodytes, and Pongo are consistently positioned above the OLS regression line, although for the LN I2 Sx and Sy samples some additional Pongo specimens fall below the regression line. Likewise, the majority of Pithecia, Cacajao, Chiropotes, Alouatta, G.b.graueri, G.g.gorilla, Hylobates, and Symphalangus specimens are consistently positioned on or below the regression line for all variables, however G.g.gorilla and G.b.graueri LN I2 Sx and Sy samples are evenly distributed above and below the OLS regression line. Ateles and Lagothrix specimens are primarily positioned above the OLS regression line, however a limited number of Ateles specimens fall below the regression line (primarily for LN I2 Sx and Sy) and almost all Lagothrix specimens in the LN I1 Sx and Sy samples are positioned on or below the OLS regression line. Although the G.b.beringei I2, I1 and I2 samples are limited to a single individual, the I1 sample is represented by 17 individuals. Nine of these are positioned on or above the OLS regression line

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Fig. 4. (Continued).

in the LN I1 Sx analysis, and five individuals are positioned above the OLS regression line in the LN I1 Sy analysis. This tendency for G.b.beringei to straddle the OLS regression line for analyses of the LN I1 Sx and Sy samples differs from the placement of the majority of G.g.gorilla and G.b.graueri specimens on or below the OLS regression line in those analyses. Results of the one-way ANOVA with a post hoc Bonferroni correction of the standardized residuals derived from the OLS regression analyses mirror the distribution of anthropoid taxa in the bivariate scatterplots and effectively discriminate between more frugivorous and more folivorous anthropoid taxa. Platyrrhine and hominoid taxa were analysed separately. Bonferroni values demonstrate that hominoids generally cluster into more frugivorous (P. troglodytes, P. paniscus, Pongo) and more folivorous (G.g.gorilla, G.b.graueri, G.b.beringei, Hylobates, Symphalangus) groupings where the more frugivorous taxa have higher standardized residual values (Fig. 4; Table 4). Although there is little discrimination within the more frugivorous grouping, Pongo has the highest LN I1 Sx standardized residuals and is significantly different (P  0.05) from all other taxa. Likewise, Pongo has lower residual values

than either species of Pan in both the LN I2 Sx and Sy analyses and is significantly different from both species of Pan but not gorillas and Hylobates. Given low available sample sizes for all incisor crowns except I1, G.b.beringei was excluded from all I2, I1 and I2 analyses. Although most similar to other folivores in the LN I1 Sy analysis, standardized residuals from the analysis of the LN I1 Sx sample identify that taxon as significantly different from G.b.graueri, Hylobates and Symphalangus (but overlapping with G.g.gorilla) and occupying an intermediate position between the more folivorous and more frugivorous groupings. Symphalangus is consistently shown to have the lowest standardized residuals and is significantly different from all taxa, including other folivores, for all analyses except for those specific to I1. In the LN I2 Sx analysis, that taxon and Hylobates are identified as having the lowest residual values and are significantly different from all other taxa. Similarly, Bonferroni values discriminate between the higher standardized residual values of a grouping of more frugivorous platyrrhines (Ateles, Lagothrix, Saimiri, Sapajus, Cebus) and a grouping of more folivorous and sclerocarp foraging platyrrhines (Alouatta, Pithecia, Cacajao, Chiropotes) (Fig. 5; Table 5). This dichotomous

471

ANTHROPOID INCISOR CROWN BENDING STRENGTH

TABLE 4. Bonferroni significance values; standardized residuals from an ordinary least squares regression of hominoid incisor crown bending strengths for individual crowns (I1, I2, I1, I2) and crown axes (Sx, Sy) against LN M2 length LN I1 Sx

Ptrog

Ppan

Ppan Ggg Gbg Gbb Pongo Hylo Symph

0.000 0.000 0.002 0.006 0.000 0.000

0.000 0.000 0.010 0.005 0.000 0.000

Ptrog

Ppan

0.000 0.000 0.000

0.000 0.000 0.000

0.000 0.000

0.000 0.000

Ptrog

Ppan

0.000 0.002 0.033 0.000 0.000

0.000 0.049 0.000 0.000

Ptrog

Ppan

0.000 0.000 0.015 0.000 0.000

0.000 0.000 0.006 0.000 0.000

Ptrog

Ppan

0.000 0.000

0.000 0.000

0.000 0.000

0.000 0.000

Ptrog

Ppan

0.000 0.000

0.000 0.000

0.000 0.000

0.000 0.000

Ptrog

Ppan

0.000 0.000

0.000 0.006

0.000 0.000

0.000 0.000

Ptrog

Ppan

0.000 0.000

0.000 0.000

0.000 0.000

0.000 0.000

1

LN I Sy Ppan Ggg Gbg Gbb Pongo Hylo Symph 2

LN I Sx Ppan Ggg Gbg Gbb Pongo Hylo LN I2 Sy Ppan Ggg Gbg Gbb Pongo Hylo LN I1 Sx Ppan Ggg Gbg Gbb Pongo Hylo LN I1 Sy Ppan Ggg Gbg Gbb Pongo Hylo LN I2 Sx Ppan Ggg Gbg Gbb Pongo Hylo LN I2 Sx Ppan Ggg Gbg Gbb Pongo Hylo

Ggg

Gbg

Gbb

Pongo

Hylo

0.000

0.029 0.000 0.000

0.000 0.000 0.000

0.000

0.000 0.000

0.014

Ggg

Gbg

Gbb

Pongo

Hylo

0.000

0.000

0.000

0.000

0.000

0.000

0.000 0.000

0.001

Ggg

Gbg

Gbb

Pongo

Hylo

0.002

0.020 0.000

Gbg

Gbb

Pongo

Hylo

0.006

0.031 0.000

Ggg

Gbg

Gbb

Pongo

Hylo

0.000

0.000

Hylo

Ggg

0.021

0.000 0.000

Ggg

Gbg

Gbb

Pongo

0.000

0.000 0.000 0.000

0.005 Pongo

Hylo

Pongo

Hylo

Ggg

Gbg

Gbb

0.000 0.000

0.000 0.026 0.000

0.000 0.000

Ggg

Gbg

Gbb

0.000

0.000

0.008

0.003

0.000 0.000

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Fig. 5. Boxplots of standardized residuals for individual platyrrhine taxa from ordinary least squares regression analyses incisor crown bending strengths for individual crowns (I1, I2, I1, I2) and crown axes (Sx, Sy) against LN M2 length. Darkened bars represent the median value for each group, while the boxes show the 50% confidence interval and the whiskers extend to the highest and lowest values for each taxon, excluding outliers.

grouping of primates characterizes all I2, I1 and I2 samples, although Alouatta is significantly different (P  0.05) from all other taxa in the analysis of the LN I2 Sx sample and Chiropotes is significantly different from all other taxa, and intermediate between the more frugivorous and more folivorus/sclerocarp foraging group for the analysis of the LN I2 Sx sample. Only the LN I1 x and y axis samples depart significantly from the dichotomous grouping of taxa observed in all other samples, however more frugivorous taxa are still broadly separated from more folivorous taxa and have higher standardized residual values. In the analysis of the LN I1 Sx dataset, Alouatta has the lowest standardized residuals and is removed from a grouping including all pitheciins and Saimiri that is itself intermediate between Alouatta and a grouping of more frugivorous taxa (Ateles, Lagoithrix, Sapajus, Saimiri). In the analysis of the LN I1 Sy dataset, Alouatta is still removed from all other taxa and Saimiri, Sapajus and Cebus, who have the highest residual values, form a grouping to the exclusion of Ateles, Lagothrix and all pitheciins, however, Sapajus overlaps with Ateles, Lagothrix and Cacajao.

DISCUSSION The results of the OLS regression and residual analyses demonstrate that more frugivorous anthropoids have higher than predicted incisal bending strengths and standardized residuals relative to more folivorous anthropoids. This pattern is observed in two distantly related anthropoid clades (platyrrhines and hominoids) and confirms that an increased reliance on frugivory is associated with a proportionate increase in incisor crown bending strength, presumably as a response to the increased mechanical loading associated with frugivory. In addition, sclerocarp foraging platyrrhines (Pithecia, Cacajao, Chiropotes) have reduced incisal bending strength similar to platyrrhine folivores, presumably as a consequence of that group’s reliance on the canine dentition for propagating cracks in the pericarps of hard object foods (Mittermeier and van Roosmalen, 1981; Hershkovitz, 1985; Sailer et al., 1985; van Roosmalen et al. 1988; Ayers, 1989; Norconk and Kinzey, 1990; Kinzey, 1992). These results are consistent with the hypothesis that increased mesiodistal and cervico-incisal

ANTHROPOID INCISOR CROWN BENDING STRENGTH

473

Fig. 5. (Continued)

curvature functions, at least in part, to increase labiolingual crown dimensions and, by extension, increase incisal crown bending strength. Given that diet specific differences in incisal crown curvature are most pronounced in the maxillary dentition (Deane et al., 2005; Deane, 2007, 2009a,b, 2012) and the strong correlation between diet and incisal bending strength reported here is consistent across both the maxillary and mandibular dentition, it is likely that incisal bending strength is influenced by a combination of variables including, but not limited to, incisal curvature. Likewise, although increased bending stress may be an important factor in preventing crown fracture in frugivores, the inability to discriminate between hominoid HOF’s and SOF’s in the I2, I1 and I2 sample sets suggests that resistance to bending is likely only one of a suite of anatomical characters that may function to prevent incisor crown fracture. Alternatively, the differential mechanical loading associated with HOF and SOF primarily impacts the I1 crowns or some combination of both of these factors. Although discrimination between more folivorous and more frugivorous groupings is relatively consistent across all incisor crown samples, the results of analyses of the hominoid and platyrrhine I1 sample sets segregate taxa

within each of these dietary groupings. Hominoid HOF’s (Pongo) have I1 crowns with additional resistance to anteroposterior bending around the MD (x) axis relative to SOF’s (P. troglodytes, P. paniscus, Hylobates sp.). HOFOM platyrrhines (Cebus, Sapajus) have I1 crowns with increased resistance to MD bending around labiolingual (y) axis relative to SOF (Ateles, Lagothrix) and SF (Chiropotes, Pithecia, Cacajao) platyrrhines. These differences are consistent with an increased reliance on hard-object foods. Similarly, although the G.b.beringei I2, I1 and I2 samples are limited, that taxon is shown here to have increased I1 bending strength around the MD axis relative to other gorillas and more folivorous hominoids. Unlike G.g.gorilla and G.b.graueri, who consume significant quantities of soft-object fruit and rely more heavily on terrestrial herbaceous vegetation (THV) as a fallback resource (Casmir, 1975; Goodall and Groves, 1977; Williamson et al., 1990; Tutin and Fernandez, 1993; Yamagiwa et al., 1994; Nishihara, 1995; Remis, 1997), G.b.beringei diets rely extensively on THV throughout the year (Fossey and Harcourt, 1977; Goodall and Groves, 1977; Watts, 1984). It has recently been reported that the high-elevation THV consumed by G.b.beringei is tougher and grittier than the foods consumed by their lowland

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TABLE 5. Bonferroni significance values; standardized residuals from an ordinary least squares regression of platyrrhine incisor crown bending strengths for individual crowns (I1, I2, I1, I2) and crown axes (Sx, Sy) against LN M2 length LN I1 Sx

Alou.

Atel. Lag. Saim. Ceb. Sap. Pith. Cac. Chiro.

0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000

LN I1 Sy

Alou.

Atel. Lag Saim. Ceb. Sap. Pith. Cac. Chiro.

0.000 0.000 0.000 0.000 0.000 0.000 0.000 0.000

LN I2 Sx

Alou.

Atel. Lag. Saim. Ceb. Sap. Pith. Cac. Chiro.

0.000 0.000 0.000 0.000 0.000

Atel.

Lag.

Saim.

Ceb.

Sap.

0.003

0.008 0.001

0.000

0.032

0.000 0.000 0.000

0.000 0.000 0.000

0.000 0.020 0.000

Atel.

Lag.

Saim.

Ceb.

Sap.

0.004 0.005

0.000 0.000 0.000 0.000 0.000

0.000 0.000 0.000

0.000

0.033

0.000 0.024

Saim.

Ceb.

Sap.

0.000 0.000

0.000 0.000 0.000

0.000 0.003 0.000

0.000 0.000 0.000

0.000 0.000 0.000

0.000 0.000 0.000

LN I2 Sy

Alou.

Atel.

Lag.

Saim.

Ceb.

Sap.

Atel. Lag. Saim. Ceb. Sap. Pith. Cac. Chiro.

0.000 0.000 0.000 0.000 0.000

0.000

0.000

0.000 0.015 0.000

0.000 0.014 0.000

0.000 0.000 0.000

0.000 0.000 0.000

0.000 0.000 0.000

LN I1 Sx

Alou.

Atel.

Lag.

Saim.

Ceb.

Sap.

Atel. Lag. Saim. Ceb. Sap. Pith. Cac. Chiro.

0.000 0.000 0.000 0.000 0.000

0.001 0.018 0.000 0.000 0.000

0.000 0.000 0.000

0.000 0.000 0.000

0.000 0.000 0.000

0.000 0.000 0.000

Lag.

Saim.

Ceb.

Sap.

0.000 0.000 0.000

0.000 0.000 0.000

0.000 0.000 0.000

0.000 0.000 0.000

0.000 0.000 0.000

Atel.

Lag.

Saim.

Ceb.

0.000 0.000 0.000

0.000 0.000 0.000

0.000 0.000 0.000

Alou.

Atel.

0.000 0.000 0.000 0.000 0.000

0.003

LN I2 Sx

Alou.

Atel. Lag. Saim. Ceb. Sap. Pith. Cac. Chiro.

0.000 0.000 0.000 0.000 0.000 0.000

Pith.

Cac.

0.047

Lag.

Atel. Lag. Saim. Ceb. Sap. Pith. Cac. Chiro.

Cac.

0.002

Atel.

LN I1 Sy

Pith.

Pith.

Cac.

Pith.

Cac.

Pith.

Cac.

Pith.

Cac.

Sap.

Pith.

Cac.

0.000 0.000 0.000

0.001

0.001 0.002 0.000 0.000 0.000

475

ANTHROPOID INCISOR CROWN BENDING STRENGTH

TABLE 5. (Continued) LN I2 Sx

Alou.

Atel. Lag. Saim. Ceb. Sap. Pith. Cac. Chiro.

0.000 0.000 0.000 0.000 0.000

Atel.

Lag.

Saim.

Ceb.

Sap.

0.000 0.000 0.000

0.007 0.000 0.000 0.000

0.000 0.000 0.000

0.000 0.000 0.000

Pith.

Cac.

0.000 0.006 0.000 0.000 0.000

counterparts and is responsible for elevated levels of dental wear in mountain gorillas (Glowacka, 2014). Increased I1 resistance to anteroposterior bending around the MD (x) axis is consistent with the habitual consumption of these tougher food items. Overall, the increased dietary resolution obtained from I1 bending strength analyses mirrors the results of prior studies of incisal curvature that also demonstrate that I1 is the incisor crown capable of providing the highest resolution dietary information (Deane et al., 2005; Deane, 2007, 2009a,b, 2012). Although the results of the present study demonstrate a significant correlation between preferred diets and incisal resistance to bending, it is also evident that incisor bending strength can be further influenced by nondietary factors as well as the degree of incisor use during feeding. The results reported here for the hominoid I2 sample are dissimilar from those reported for I1, I1 and I2, not unlike the results of prior analyses of hominoid incisal curvature (Deane et al., 2005; Deane, 2007, 2009a,b). Differences in I2 incisal curvature were attributed to non-dietary influences and, more specifically, the dichotomy between spatulate and peg-shaped incisor crowns (Deane, 2007, 2009a). Only species belonging to the genus Pan and hominins possess spatulate I2 crowns that are mesiodistally elongated and have a relatively flatter labial surface. All other hominoids have peg-shaped I2 crowns that have a rounded cross section (i.e. pronounced labial curvature). Results from the present study suggest that hominoid SOF’s, a group dominated by the genus Pan (75% of all SOF’s in the I2 study sample), have increased bending strength around both the mesiodistal and labiolingual axes with respect to HOF’s and more folivorous taxa which cluster together and are not significantly different from one another. Similar to the results reported from prior analyses of I2 crown curvature, these results may be more representative of the differences between spatulate and peg-shaped incisors and less informative of actual dietary differences among taxa. Spatulate incisors are mesiodistally broader than peg-shaped incisors (Deane, 2007, 2009a) and, given that bending strength is a function of linear crown dimensions, resistance to bending strength may be overestimated in taxa with a spatulate I2. Accordingly, comparisons of I2 bending strength in mixed hominoid samples with both spatulate and peg-shaped crowns should be interpreted with caution. In contrast, the more uniform platyrrhine I2 crown morphology is shown here to be no less capable of discriminating between HOF-OM, SOF, FOL, and SF platyrrhines than are any other platyrrhine incisor samples.

Similarly, although primarily frugivorous, Hylobates is consistently grouped with more folivorous hominoids and Symphalangus in particular. This is almost certainly a consequence of that taxon’s considerably less frequent use of the incisors for pre-processing food. Field observations of hylobatid feeding behaviour indicate that these taxa habitually consume smaller food items and often bypass their anterior dentition altogether (Ungar, 1995), meaning that selection for increased resistance to incisal bending will likely be reduced relative to other hominoids. The placement of Hylobates with Symphalangus and more folivorous hominids may be less reflective of that taxon’s dietary preferences than it is a reflection of the frequency of incisor use, and a possible grade shift between the lesser bodied and great apes.

CONCLUSION The results of the allometric scaling and residualbased analyses of hominoid and platyrrhine incisal bending strength reported here demonstrate a strong and positive correlation between elevated resistance to incisal bending and an increased reliance on frugivory. The results derived from analyses specific to I1 provided the highest resolution dietary information and were capable of discriminating between hard- and soft-object frugivores. The correlation between elevated incisor crown bending strength and increased levels of frugivory is consistent with the hypothesis that increased mesiodistal and cervico-incisal curvature of the labial surfaces of maxillary and mandibular incisors function, at least in part, to increase linear crown dimensions and, by extension, resistance to bending strength which is a direct function of the linear dimensions of the incisor crown. Regardless, it is likely that incisor bending strength is a composite function of multiple dentognathic variables including, but not limited to, incisor crown curvature. Similarly, increased incisor bending strength is likely only one of a number of responses to the variable mechanical loading associated with hard- and soft-object frugivorous diets. Incisor-bending strength may also be influenced by non-dietary factors (i.e. spatulate vs. pegshaped incisors) and frequency of incisor use during ingestion (i.e. hylobatids vs. hominids). Despite this, incisor form and bending strength closely tracks diet within individual primate families (i.e. Hominidae, Hylobatidae, Cebidae) and can differentiate closely related taxa with dissimilar diets (i.e. Alouatta vs. Ateles and Lagothrix; G.b.beringei vs. G.b.graueri and G.g.gorilla) suggesting that diet is the primary influence governing incisor form and bending strength.

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Although it is a reasonable conclusion that incisor curvature influences incisor bending strength, the full extent of the functional role of incisor crown curvature will only be clarified with additional study of anthropoid incisor shape and allometric variation, coupled with an improved understanding of anthropoid feeding biomechanics and the mechanical properties of the foods they consume.

ACKNOWLEDGEMENTS Thank you to Bill Stanley (FMNH), Emannuel Gilissen (RMCA), Eileen Westwig (AMNH), Darrin Lunde (SNMNH), Angela Gill (PC), Marcia Ponce de Leon (University of Zurich), and Shannon McFarlin (DFGFI MGSP) for access to collections in their care. The author gratefully acknowledges the Rwandan government for permission to study skeletal remains curated by the Mountain Gorilla Skeletal Project (MGSP). The MGSP Collection has been made possible by funding from the National Science Foundation (BCS-0852866, BCS0964944), National Geographic Societyoˆ s Committee for Research and Exploration, and The Leakey Foundation, infrastructural support from the Dian Fossey Gorilla Fund Internationaloˆ s (DFGFI) Karisoke Research Center, and the continuous efforts of researchers, staff and students from the Rwanda Development Boardoˆ s Department of Tourism and Conservation, Gorilla Doctors, DFGFI, The George Washington University, New York University College of Dentistry, Institute of National Museums of Rwanda, and other universities in Rwanda and the U.S.A. Thanks also to Magdalena Muchlinski and to three anonymous reviewers for their useful and insightful comments on a previous draft of this article.

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