ANTHROPOLOGICAL SCIENCE Vol. 112, 121–146, 2004

Molar enamel thickness and distribution patterns in extant great apes and humans: new insights based on a 3-dimensional whole crown perspective REIKO T. KONO1*

1Department of Anthropology, National Science Museum, Hyakunincho, Shinjuku-ku, Tokyo, 169-0073 Japan

Received 14 November 2003; accepted 21 December 2003

Abstract Molar enamel thickness is a key feature in the study of hominid evolution. Our understand- ing of enamel thickness and distribution patterns, however, has so far been based mostly on the limited information available from physical cross sections of the crown. In this study, the 3-dimensional (3D) whole crown enamel distribution pattern was explored in 74 extant great ape and modern human molars. Serial cross sections obtained from microfocal X-ray computed tomography were used to gen- erate digital molar reconstructions at 50 to 80 micron voxel resolution, each crown represented by two to five million voxels. Surface data of both enamel dentine junction (EDJ) and outer enamel were extracted to derive volumetric measures, surface areas, curvilinear distances, and whole crown radial thickness maps. Three-dimensional average enamel thickness (AET) was defined as enamel volume divided by EDJ surface area. In 3D AET relative to tooth size, Homo exhibited the thickest, Gorilla the thinnest, and Pan and Pongo intermediately thick enamel. This result differs from previous claims that molar enamel of Pongo is relatively thicker than that of Pan. The discrepancy between three and two-dimensional (2D) values of AET stems from a combination of local differences in within tooth enamel distribution pattern and EDJ topography between Pan and Pongo molars. It demonstrates that 2D AET is not an appropriate substitute or estimator of whole crown AET. Examination of whole crown 3D distributions of molar enamel revealed a pattern common to all four examined species, the “functional” side of the molar having thicker enamel than the opposite side. However, some unique aspects of each species were also apparent. While the Gorilla molar has relatively thin enamel through- out its crown, Pan molars are characterized by particularly thin enamel in the occlusal fovea, and Pongo molars by an accentuation of relatively thin basal and thick occlusal enamel. Human molars are characterized by relatively thick enamel throughout the crown, with relatively large contrasts between buccal and lingual, and between mesial and distal crown portions. The ancestral condition common to the four extant species can be estimated by interpreting molar enamel distribution patterns unique to each genus as likely to be derived. We hypothesize that the last common ancestor likely had interme- diately thick enamel, without particular thickening (or thinning) of enamel either occlusally or basally.

Key words: enamel thickness, molar, hominoid, evolution

Introduction reflects both phylogenetic heritage and the results of selec- tion for functional adaptation. Teeth are also suitable to the Dental elements in general have a greater chance to be study of morphology in relation to its formational processes, preserved and fossilized than other body parts. Therefore, since their developmental history is in part recorded as his- they often constitute a major part of fossil collections. This tological markings. For these reasons, dental morphology is true in the case of primate fossils, including fossil homi- has been intensively studied, as an important source of infor- nids. mation from both functional and phylogenetic perspectives. The dentition is functionally adapted to diet and feeding Molars show great morphological diversity among taxa. behavior. Morphogenesis of the tooth crown is controlled This is thought to be closely related to functional require- mostly by genetic factors, rather than by environmental fac- ments imposed by the physical properties of the masticated tors. While bones continue to remodel throughout an indi- food (e.g., Janis and Fortelius, 1988). For molars of extant vidual’s life, tooth enamel does not regenerate once its great apes and modern humans, morphological studies have formation is completed. Therefore tooth morphology been conducted from various perspectives. Hominoid molars share a generalized morphological pattern compared * Corresponding author. e-mail: [email protected] to those of other mammals, but also exhibit taxonomically phone:
81-3-3364-7132; fax:
81-3-3364-7104 informative differences in details (e.g., Hartman, 1988, Published online 13 April 2004 1989; Kobayashi, 2001). Molar enamel thickness is known in J-STAGE (www.jstage.jst.go.jp) DOI: 10.1537/ase.03106 to vary among the extant hominoids, apparently exhibiting

© 2004 The Anthropological Society of Nippon 121 122 R.T. KONO ANTHROPOLOGICAL SCIENCE substantial functional and/or phylogenetic information (e.g., human molars based on linear measurements. They reported Martin, 1983; Shellis et al., 1998). that enamel was thicker in humans than in apes at multiple Lawrence Martin and his colleagues discussed the evolu- positions of the molar tooth crown. They proposed that the tion of hominoid enamel thickness by comparing extant thick human enamel, together with the low cusps, was great apes, modern humans, and fossil hominoids and homi- adapted to a crushing-grinding function, although no func- nids (Martin, 1983, 1985; Grine and Martin, 1988; Andrews tional rationale was presented (Molnar and Gantt, 1977). and Martin, 1991). Martin physically sectioned molars at a Kay (1981) measured enamel thickness on the worn occlusal plane that passes approximately through the tips of the two surface of molars in a wide range of primate taxa, and plot- mesial cusps (mesial cusp section, MCS), and made various ted thickness against the mesiodistal length of the tooth. He thickness measurements on those sections. He concluded noticed that enamel tends to be thicker in frugivorous spe- that the “average enamel thickness (AET)”, calculated as cies, whereas the more folivorous taxa tend to have thinner enamel area divided by length of the enamel-dentine junc- enamel (Kay, 1981). Among great apes, according to his tion (EDJ), was the most reliable measure of the amount of interpretation, Pongo has relatively thick enamel, which enamel, since it was supposedly less variable than compara- might be an adaptation to eating very hard fruits, while ble measures taken at other section positions (Martin, 1983). Gorilla has relatively thin enamel and well-developed shear- Moreover, he devised a measure called “relative enamel ing crests, which are likely to be adaptations to leaf-eating thickness” as a means to compare thicknesses between taxa (Kay, 1981). with different tooth sizes. Relative enamel thickness is cal- More recently, Macho, Schwartz and colleagues studied culated as the AET standardized by the square root of den- enamel thickness patterns within the molar crown, and dis- tine area of the crown at that section. Using this relative cussed their functional significance (Macho and Berner, thickness value, he proposed four categories of thickness, 1993, 1994; Spears and Macho, 1995, 1998; Schwartz, “thick”, “intermediate~thick”, “intermediate~thin”, and 1997, 2000a, b; Macho and Spears, 1999). Macho and “thin”. He assigned gorilla and chimpanzee molars to “thin”, Berner (1993) showed that the values of “average” and “rel- orangutan molars to “intermediate~thick”, and human ative enamel thickness” introduced by Martin (1983) dif- molars to “thick” categories (Martin, 1983, 1985). These fered between tooth types within the human molar row. They variables, average and relative enamel thicknesses, have thus proposed the necessity to investigate enamel thickness since been used frequently in species comparisons (Grine patterns seen among tooth type, or within a tooth, rather than and Martin, 1988; Andrews and Martin, 1991; Dumont, simply obtaining a representative thickness value for the 1995; Beynon et al., 1998; Shellis et al., 1998). entire tooth and/or species (Macho and Berner, 1993). They Martin furthermore related enamel thickness with prism measured enamel thickness at multiple positions on the packing patterns, and concluded that enamel was thick and MCS, and suggested that the first upper molars have a pat- formed fast in the last common ancestor of extant large-bod- tern of enamel distribution different from that of the second ied hominoids (including humans), while enamel had and third upper molars. Human upper first molars were become thin in the gorilla and chimpanzee because of a sec- found to be characterized by distinctly thicker lingual and ondary decrease in enamel formation speed (Martin, 1983, thinner buccal enamel. The posterior two molars exhibited 1985; Andrews and Martin, 1991). Later, however, Beynon overall thicker enamel than the first molar, and with less dis- et al. (1991) reexamined hominoid molar histology, and crepancy between lingual and buccal enamel thicknesses, so showed that no such decrease in enamel formation speed is that the “non-functional” buccal cusps have somewhat in fact seen in gorilla and chimpanzee molars. In all four spe- thicker enamel. This was interpreted as reflecting different cies that the latter authors examined, enamel formation functional roles of the first and posterior two molars (Macho speed was found to gradually increase from EDJ to the outer and Berner, 1993, 1994). enamel surface (OES). They therefore rejected Martin’s Using finite element analysis, they further investigated interpretations of enamel thickness and speed of formation. stress distribution patterns in the MCS, under load from dif- They further proposed that thin and fast-forming enamel was ferent directions, and compared the molars of Homo, Pan, likely to be the ancestral condition of the last common and Pongo in their capacity to resist such mechanical loads ancestor of humans and extant great apes (Beynon et al., (Spears and Macho, 1995, 1998; Macho and Spears, 1999). 1991). Recently, Shellis et al. (1998) examined, in various According to them, in human lower molars, the buccal cusps primate taxa, the relationship between Martin’s average the so-called “functional cusps” better dissipate occlusal enamel thickness and size measurements made on the mesial loads compared to their lingual counterparts, whereas in cusp section. They presented a somewhat different view of upper molars, the buccal (“non-functional”) cusps generally great ape enamel thickness, showing that, when empirically resist loads as well as the lingual cusps. Moreover, it was scaled relative to tooth size using a taxonomically broader suggested that in the second and third upper molars, the buc- primate data set, AET is actually not so different between cal cusps even better dissipate loads than the lingual cusps. chimpanzee and orangutan molars (Shellis et al., 1998). These results were interpreted by the authors that all lower They then presented the alternative opinion that the last molars act as “pestles”, while the upper molars especially common ancestor possibly had “average” enamel thickness the posterior ones are better suited to act as “mortars” (Shellis et al., 1998). (Spears and Macho, 1995, 1998). While they considered Molnar and Gantt (1977) were the first to discuss the enamel thickness to be part of this structural resistance to functional significance of enamel, by using a numerical mechanical load, such that thick enamel was considered to evaluation of enamel thickness of extant great ape and be an adaptation to larger magnitudes of occlusal load, they Vol. 112, 2004 HOMINOID MOLAR ENAMEL THICKNESS AND DISTRIBUTION 123 later showed that occlusal topography is more responsible tion that the thicker the enamel the greater the load it could for efficient load dissipation and resistance rather than resist (Macho and Berner, 1993, 1994; Spears and Macho, enamel thickness itself (Macho and Spears, 1999). 1995, 1998; Macho and Spears, 1999; Schwartz, 2000b). Schwartz (1997) used computed-tomography (CT) as a However, as already mentioned, Macho and Spears (1999) non-destructive method of measuring enamel thickness in themselves implied that thickness itself may not be a signif- fossil hominids. Combining this with previously published icant factor determining the molar’s capacity to resist data of modern great ape and human molars taken on physi- mechanical load. Other factors such as resistance to wear cal sections at the MCS (Schwartz, 1997, 2000a), he inter- should also be taken into account when examining the func- preted the results on the assumption that regions with tional meaning of enamel distribution patterns. relatively greater functional loads would have thicker molar In order to understand the significance of molar enamel enamel (Schwartz, 1997, 2000a). However, by functional thickness and its patterning, it is necessary to first examine load, whether he meant more wear or greater mechanical and establish enamel distribution patterns of the entire molar load, was not made clear nor kept consistent throughout his crown of each tooth type of each species. Only through this discussions. He further suggested that it is possible to dis- approach, would it become possible to discuss the relation- criminate among hominoid species using enamel distribu- ship between the average thickness of enamel and the char- tion patterns of the maxillary molars at the MCS (Schwartz, acteristics of its distribution pattern, and then to offer more 1997, 2000a). He also analyzed enamel distribution patterns informed hypotheses about the evolution and adaptation of of human lower molars, and concluded that a pattern similar enamel thickness. The aim of this study is thus: 1) to deter- to the one shown by Macho and Berner (1993, 1994) for the mine a variety of “representative” values of enamel thick- upper molar row was not seen (Schwartz, 2000b). In human ness of the whole molar tooth crown, using 3D volumetric lower molars, he found that buccal enamel thickness tended measures, 2) to compare 3D-based average enamel thickness to be consistently thicker in the posterior molars, but with no (enamel volume divided by EDJ surface area) with the relative increase of thickness in the “non-functional” lingual widely used 2-dimensional (2D) measure (enamel cross-sec- cusp. He interpreted this in a framework of functional adap- tion area divided by EDJ length), 3) to investigate and com- tation in relation to the helicoidal occlusal plane, as pro- pare the whole-crown enamel distribution patterns of four posed by Macho and Berner, that all lower molars function extant hominoid species (modern humans, gorillas, chim- as “pestles” regardless of their position along the tooth row, panzees, and orangutans), and 4) to discuss the evolutionary supporting the view that thick enamel is an adaptation to history and functional significance of molar enamel thick- greater loads (Spears and Macho, 1995, 1998; Macho and ness in hominoids. Spears, 1999; Schwartz, 2000b). Although several attempts have been made, as summa- Materials and Methods rized above, to investigate phylogenetic and/or functional significance of molar enamel thickness in great apes and Materials humans, the information so far gained is limited in that most Forty-one permanent molars of Homo sapiens of Jomon previous studies measured thickness only on the specific period Japanese (n
10), Edo period Japanese (n
12), and section which runs through the two mesial cusp tips, as ini- modern Asian (n
19), and a hominoid sample consisting of tially introduced by Molnar and Gantt (1977) and Martin permanent molars of Pan troglodytes (n
22), Gorilla gorilla (1983). Phylogenetically, enamel thickness of each species (n
4), and Pongo pygmaeus (n
7) were analyzed in this has often been evaluated with reference to simple categories study. Molars are either first or second, and upper or lower. such as “thick” or “thin”, by use of a single representative The details of sample compositions are given in Table 1. Sex value of thickness, such as the “average enamel thickness” is unknown for most of the specimens, since they were taken measured at the MCS (Martin, 1983, 1985; Shellis et al., from juvenile individuals. 1998). No effort has been made to test the validity of the use The Jomon and modern Asian human molars were taken of this specific section as representative of enamel thickness from the skeletal collection housed in The University of the entire molar crown. It remains to be seen whether the Museum, The University of Tokyo. The modern Asian “average enamel thickness” measured at the MCS is really a molars were taken from educational skeletal specimens of good estimator of the average thickness of the entire molar unknown origin. The Edo period specimens derive from the crown, as Martin (1983) had intended. Recent studies that skeletal collections housed in the National Science Museum, aimed to investigate enamel distribution patterns have indi- cated that not only a single representative value but also within tooth distribution patterns may also be informative Table 1. Number of molars included in the present study for phylogenetic inferences (Macho and Berner, 1993, 1994; Mandibular Maxillary Schwartz, 1997, 2000a, b). However, these studies were also M1 M2 M1 M2 limited to analyses of the MCS (Macho and Berner, 1993, 1994; Schwartz, 1997, 2000a, b; Spears and Macho, 1998; Homo sapiens total 13 13 8 7 Macho and Spears, 1999). Such results are obviously insuf- Jomon 5 5 Edo 3 3 3 3 ficient to establish the significance of enamel distribution of Modern Asian 5 5 5 4 the entire crown. Pan troglodytes 66 55 As for the functional significance of enamel thickness, Gorilla gorilla 11 11 most interpretations seem to have been based on the assump- Pongo pygmaeus 32 11 124 R.T. KONO ANTHROPOLOGICAL SCIENCE

Tokyo. Although these three populations are from different height method (Spoor et al., 1993). In scanning the molars, ages and/or regions, they are all pooled in the present study they were immersed in a sodium polytungstate (SPT) solu- since apparent population differences were not seen in the tion (Danhara et al., 1992), the concentration of which was preliminary stages of our investigation. Besides, the aim of empirically adjusted so that X-ray absorption was equivalent this study is to investigate differences and patterns seen at to that of dentine. This enabled both OES and EDJ to be the species level. Therefore, it is reasonable to combine pop- optimally defined by the same threshold. ulations representing intraspecific variation. The digitized data of each molar was organized into a set Most of the hominoid teeth are from the collection of the of data formats described below, by use of 3D image analy- Cleveland Museum of Natural History, collected as wild- sis software (3D- and CT-Rugle, Medic Engineering Inc., shot specimens. The rest of the specimens of chimpanzee Kyoto). These applications were in part developed through and orangutan are housed either at the University of Califor- our research project (Kono-Takeuchi et al., 1997; Kono et nia, Berkeley, or The University Museum, The University of al., 1998, 2000; Suwa and Kono-Takeuchi, 1998; Suwa et Tokyo. al., 2000). This data formatting process enables us to handle Molars were chosen to have no wear, or slightest wear. the two (laser and micro-CT based) data types equivalently Although it was possible to obtain a substantial number of in all ensuing measurement procedures. The overall accu- completely unworn human molars, this was quite difficult in racy of both data sets was confirmed to be sufficient and the case of non-human hominoid species. Therefore molars comparable (Kono et al., 2000; Suwa and Kono, 2000; Suwa of these taxa with slight occlusal wear and/or small chipping et al., 2000). of enamel around the cervical region were included. The orientation of the tooth was systematically adjusted For the purpose of inter-specific comparisons, all tooth during the data formatting process, so that regions of interest types were pooled by taxon, because of the limited number could later be defined in relation to the standardized orienta- of gorilla and orangutan molars. For the human and chim- tion. First, each molar was oriented to maximize the pro- panzee samples, comparisons between tooth types were also jected occlusal surface area (Suwa and Kono-Takeuchi, possible. 1998). This was done with the EDJ rather than with the OES, since the occlusal fovea of the EDJ is bounded by a sharp Methods rim of dentine that can be delineated regardless of slight dif- Three-dimensional shape of the enamel cap is delineated ferences in initial orientation (Kono et al., 2002). In orient- by the topographies of the EDJ and OES. In this study, ing the maxillary molars, only the trigon basin was used. enamel cap shape of the molar crown was reconstructed by Once the occlusal view orientation of the molar was obtaining digital representations of these two surfaces. The adjusted, the entire data set of the tooth was rotated around resulting data set of the molar crown was then subjected to the axis of projection, the z-axis, so that the dentine tips of various measurements of enamel thickness and other param- the two mesial cusps were aligned on the same x-coordinate. eters. In the primary acquisition of the digital morphological In order to derive the different kinds of variables that were data, either of two sets of devices was used. These were the analyzed in this study, the original digitized data set of each 3D surface digitizing system using a laser beam (Voxelan molar was transformed into three formats: the xz- and yz- small field model, Hamano-engineering, Kanagawa), and line data, the T-map data, and the VOL data. The line data the micro-focal X-ray CT scanning system (TX225-ACTIS, were used in the calculation of surface area and EDJ length TESCO Corporation, Tokyo). Only the modern Asian speci- (Kono et al., 1998). Both xz- and yz-line data were prepared mens (n
19) were digitized by the former system (Kono et for each molar. Each xz- (or yz-) line data is composed of al., 2002) and a detailed explanation of this method is given lined data points of EDJ or OES cross-section contours, rep- elsewhere (Kono-Takeuchi et al., 1997; Kono et al., 1998, resented by 640 points within each xz- (or yz-) plane, of 2002; Kono, 2002). evenly spaced serial xz- (or yz-) planes. The interval The human molars of the Jomon and Edo period Japanese between planes was set to correspond to unit pixel size, and populations and all molars of the great apes were digitized the number of planes would be around 150 for each xz- (or by means of serial CT scanning. Each molar was scanned yz-) line data. The length of the EDJ contour on a particular with a tube voltage of 90 kV (for Gorilla molars, 100 kV), xz- (or yz-) plane was calculated as the sum of the distances filtered with a 3 mm thick aluminum plate (0.5 mm copper between adjacent points. Surface areas were calculated by plate for Gorilla), with a current of 0.13 to 0.16 mA. Each forming triangular patches between adjacent lines, and sum- molar was scanned perpendicular to its long axis, serially ming their areas. The number of triangular patches used in with intervals of either 0.056, 0.062, 0.068, 0.074, or surface area calculation was typically about 250,000 for 0.084 mm, according to its crown size. The number of each molar. scanned sections was up to 200 for each molar crown. Each The T-map data format takes the form of a thickness map section was reconstructed in a matrix size of 512×512 pixels. (Kono et al., 2002). For each data point of the OES, the min- The size of the pixels was set to half of the slice interval. imum distance from that point to the EDJ surface was calcu- Slice thickness was kept constant at 0.05 mm regardless of lated and allocated to that point. A T-map data format of a tooth size and slice interval. Pixel size, slice interval and molar crown in occlusal view is typically represented by slice thickness were all calibrated to an accuracy of circa about 30,000 points. This data format enables calculation of 0.1% by measuring an aluminum rod of known diameter. representative thickness values of certain crown regions of The boundary between enamel and dentine was determined interest (such as the average thickness of the occlusal sur- by thresholding the CT images using the half maximum face of the protoconid), by averaging or ranking thickness Vol. 112, 2004 HOMINOID MOLAR ENAMEL THICKNESS AND DISTRIBUTION 125 values of all points included in that region. treated not separately but together as “dentine”. This is The VOL data format was used in the calculation of the partly because the molars used in this study were at various volume of a certain part of the crown or enamel cap. This stages of root formation (since they were mostly unworn) format is in 256×256×256 matrix, and each voxel is assigned and had not reached the final proportions of dentine and pulp to be either enamel, dentine (see below), or blank (outside of cavity within the above defined tooth crown. the tooth crown). The algorithm for the volume measure- Two of the measurements, the basal and maximum hori- ment is a simple count of the number of voxels within the zontal areas, were taken on horizontal sections of the crown. region of interest, multiplied by the calibrated size of the Basal area is dentine cross section area measured at the low- voxel. est height where enamel is continuous around the entire cir- The accuracy of volumes, surface areas, and curvilinear cumference of the section. Maximum horizontal area is the distances derived from the above data formats were modeled maximum cross section area in standardized orientation (as by measuring virtual hemi-spheres. Digital data processing defined above). Maximum horizontal area includes both error was estimated to be better than 0.1% for volume, 1.5% enamel and dentine tissue. for surface areas, and 0.5% for curvilinear distances (Suwa and Kono, unpublished study). Group 2: Representative enamel thickness values of the entire crown Measurements Average enamel thickness in the strict 3D sense was Variables studied in this paper are categorized into five derived, that is enamel volume divided by EDJ surface area. groups according to type and objective (Table 2). Brief Enamel volume relative to the horizontal cross section area descriptions of each of these five groups are given below. was calculated as a rough indicator of the durability of tooth against abrasion. The average of the minimum enamel thick- Group 1: Measures of molar crown size ness values was calculated, as an alternative way of repre- This first group consists of several basic size measures of senting mean enamel thickness. the tooth crown, including enamel and dentine volumes, and EDJ surface area. In this study, “tooth crown” is defined as Group 3: Variables measured on the MCS the enamel cap and the dentine and pulp cavity portions In order to compare the 3D variables with their 2D coun- enclosed within it, but here the latter two portions were terparts of previous studies, “average-” and “relative enamel

Table 2. Abbreviations and definitions of the variables analyzed in this study Group 1 Evol Total volume of the enamel tissue Dvol Total volume of crown “dentine”a Dsa Surface area of EDJ BA Basal area (horizontal area of the “dentine”a at the base of the crown) MA Maximum area (maximum horizontal area including both enamel and “dentine”a) Group 2 AET (Evol/Dsa) 3-dimensional average enamel thickness AETBA (Evol/BA) Average enamel thickness in relation to the basal area AETMA (Evol/MA) Average enamel thickness in relation to the maximum area AMT Average of minimum enamel thickness AETSTD (AET/Dvol1/3) 3-dimensional relative enamel thickness Group 3 Earea Enamel area on MCS Darea “Dentine”a area on MCS EDJL EDJ length on MCS 2D AET (Earea/EDJL) 2-dimensional average enamel thickness 2D AETSTD (2D AET/Darea1/2) 2-dimensional relative enamel thickness Group 4 CAET Average enamel thickness of cuspal region BAET Average enamel thickness of cervical region OAMT Average of minimum enamel thickness of the occlusal fovea LAMT Average of minimum enamel thickness of the lateral surface Group 5b OX Average minimum thickness of the occlusal fovea SX95 Maximum thickness of the lateral surface (95 percentile of the minimum thickness values) SX50 Median of thickness of the lateral surface (50 percentile of the minimum thickness values) SXAve Average thickness of the lateral surface (average of the minimum thickness values) a “Dentine” includes the pulp cavity portion. See text. b “X” indicates the abbreviated cusp name (Prdprotoconid, Medmetaconid, Hydhypoconid, Endentoconid, Hldhypoconulid, Paparacone, Prprotocone, Memetacone, Hyhypocone). 126 R.T. KONO ANTHROPOLOGICAL SCIENCE thickness” were calculated from enamel area, EDJ length, Pongo molars were significantly larger than those of Pan and dentine area of the MCS, as defined by Martin (1983). and Homo in all variables, except with enamel volume in Homo. Comparing Pan and Homo, enamel volume was sig- Group 4: Variables representing enamel distribution patterns nificantly greater in Homo, but dentine volume was compa- within the crown rable. Human molars therefore can be described as having a In order to compare overall patterns of enamel distribu- dentine crown the size of Pan, covered with enamel the vol- tion, molar crown enamel was divided into two portions in ume of which equals that of Pongo. EDJ surface area, basal two different ways; cuspal and basal, or occlusal and lateral. area and maximum horizontal area were all greater in Pan Average thickness values were calculated for each of these than in Homo. This reflects differences in molar crown respective subdivisions of the crown. For the cuspal and shape between these two taxa. basal regions, average thickness was calculated as enamel Figure 1 shows the relationship between these variables volume divided by EDJ surface area. The boundary between and dentine volume. There was a strong correlation between cuspal and basal portions was set at the horizontal plane dentine volume and EDJ surface area (r
0.991, with both passing through the lowest point on the 3D occlusal EDJ sur- values log-transformed) (Figure 1a). Coefficient of the loga- face. Occlusal and lateral average thicknesses were obtained rithmic regression line was 0.681±0.022, indicating that the by averaging the minimum distances from OES to EDJ. The relationship did not deviate significantly from isometry. occlusal region was defined on the OES as the area enclosed When viewed in relation to the line of isometry passing by the cusp tips and marginal ridges. through the average of Homo, however, a tendency charac- teristic of each taxon could be seen to exist. Gorilla and Pan Group 5: Representative values of cusp-by-cusp enamel dis- individuals were placed a little above this line, while Pongo tribution individuals tended to be on or below this line. Differences Enamel distribution patterns were investigated in a cusp- between taxa were more clearly shown when enamel volume by-cusp manner, using the T-map data of occlusal and lateral was plotted against dentine volume (Figure 1b). In relation surfaces of each cusp (Kono et al., 2002). For the lateral sur- to the line of isometry passing through the average of Pan, faces, the maximum, median, and the average of minimum enamel volume was relatively greater in Homo and smaller thickness values were calculated for each cusp. The 95th in Gorilla. Pongo was comparable, or isometric, to Pan in percentile value was designated here as the “maximum” this regard. The basal and maximum horizontal areas were thickness for the purpose of eliminating possible effects of also correlated with dentine volume (data not shown). noise. For the occlusal surface, the average minimum thick- The above variables did not differ significantly between ness was calculated for each cusp. tooth type in both Homo and Pan (Appendix 2). The only exception is that, in the upper molars of Homo, enamel vol- Results ume and EDJ surface area were significantly greater in the first than in the second molar. Dentine volume and maxi- Molar crown size mum horizontal area were also greater in the first molar, Variables expressing molar crown size are summarized in although the differences were not significant. These results Appendix 1. In all of these variables, Gorilla molars were imply that the second molars are smaller overall than the significantly larger than those of the other three species. first molars in Homo.

Figure 1. (a) Log-plot of EDJ surface area against dentine volume. The dotted line is the least squares regression line, and the solid line is the line of isometry running through the average of Homo. (b) Log-plot of enamel volume against dentine volume. The two lines are the lines of isom- etry running through the average of Homo and Pan, respectively. Circles, Homo; filled triangles, Pan; open triangles, Gorilla; crosses, Pongo. Vol. 112, 2004 HOMINOID MOLAR ENAMEL THICKNESS AND DISTRIBUTION 127

Table 3. Descrpitive statistics of 2D and 3D average enamel thickness with Pan exhibiting thicker enamel than Gorilla. To further with results of statistical comparisons between taxa investigate the effect of tooth size, 2D AET was log-plotted Mann-Whitney U-test against dentine area, and examined with regard to the line of species N x S.D. isometry running through the average of Pan (Figure 2a). Homo Pan Pongo The Gorilla molars were positioned below the line, and 2D AET (mm) those of Homo and Pongo were distributed above it. Homo 40 1.203 0.138 2D AET was also compared between tooth type within Pan 22 0.717 0.066 0*** Homo and Pan (Table 4). In Pan, there was no significant Pongo 7 1.006 0.187 57* 5*** Gorilla 4 0.938 0.164 13** 4** 11 difference between tooth type. In Homo, the upper molars exhibited greater 2D thicknesses than the lower molars. 2D AETSTD Homo 40 0.199 0.031 Pan 22 0.118 0.015 1*** 3D average enamel thickness Pongo 7 0.148 0.023 21*** 16** Among the four species included in this study, 3D AET Gorilla 4 0.094 0.013 0** 11* 0** was significantly greater in Homo, and smaller in Pan (Table AET (mm) 3). The difference between Gorilla and Pongo was not sig- Homo 41 1.334 0.134 nificant. 3D AET was log-plotted against dentine volume Pan 22 0.811 0.087 1*** and examined with regard to the line of isometry passing Pongo 7 1.006 0.124 8*** 14** through the average of Pan (Figure 2b). Like the pattern Gorilla 4 0.975 0.098 3** 7** 11 seen in the case of 2D AET, Homo and Gorilla molars AETSTD tended to deviate above and below this line, respectively. On Homo 41 0.206 0.027 the other hand, Pongo molars were distributed near the line. Pan 22 0.123 0.016 0*** When the 3D version of relative enamel thickness was statis- Pongo 7 0.129 0.008 0*** 49 tically compared among taxa (Table 3), Pongo and Pan did Gorilla 4 0.095 0.006 0** 2** 0** not differ significantly. This means that, relative to tooth *** P0.001, ** P0.01, * P0.05. size, the 3D determined average thickness is comparable in Pan and Pongo, in contradistinction to the 2D results. In order to further investigate the relationship between enamel thickness and tooth size, correlation coefficients Average enamel thickness between 3D AET and the variables representing tooth crown The conventional 2-dimensional average enamel thick- size were calculated (Table 5). No significant correlation ness (2D AET) and relative enamel thickness (2D AETSTD) was found with any of the size variables when all species were compared between species (Table 3). The results were were pooled, or within Homo or Pan. Several of the size mostly the same as those of Martin (1983). The mean values variables were shown to correlate significantly with 3D AET of 2D AET in Pan and Gorilla, however, were greater in the in Gorilla and Pongo, but these results should be regarded as present study. While 2D AETSTD of Pan and Gorilla did tentative, since the sample sizes were small. not differ significantly in Martin’s data, a significant differ- In Homo and Pan, 3D AET was compared between tooth ence was seen between the two in the present study (Table 3) type (Table 4). There was no significant difference seen

Figure 2. Log-plot of 2D AET against dentine area on the MCS (a), and 3D AET against dentine volume (b). The line of isometry runs through the average point of Pan. Circles, Homo; filled triangles, Pan; open triangles, Gorilla; crosses, Pongo. 128 R.T. KONO ANTHROPOLOGICAL SCIENCE

Table 4. Descrpitive statistics of 2D and 3D average enamel thickness Table 6. Descrpitive statistics of the alternative measurements with results of statistical comparisons between tooth type of average enamel thickness with results of statistical comparison between taxa t-test result species tooth jaw N x S.D. a b Mann-Whitney U-test L vs U vs M1 species N x S.D. Homo Pan Pongo 2D AET (mm) Homo M1 U 8 1.226 0.110 * AMT (mm) L 12 1.128 0.085 Homo 41 1.084 0.096 M2 U 7 1.326 0.168 Pan 22 0.706 0.068 1*** L 13 1.192 0.138 Pongo 7 0.885 0.103 19*** 11*** Pan M1 U 5 0.724 0.112 Gorilla 4 0.881 0.097 6** 6** 13 L 6 0.703 0.051 AETBA (mm) M2 U 4 0.693 0.075 Homo 41 3.47 0.494 L 6 0.742 0.032 Pan 22 2.16 0.238 0*** 3D AET (mm) Pongo 7 2.33 0.247 0*** 50 Homo M1 U 8 1.398 0.113 Gorilla 4 2.91 0.388 31* 3** 3* L 13 1.320 0.122 AETMA (mm) M2 U 7 1.346 0.180 Homo 41 2.66 0.242 L 13 1.302 0.132 Pan 22 1.63 0.131 0*** Pan M1 U 5 0.851 0.141 Pongo 7 1.94 0.173 0*** 10*** L 6 0.780 0.050 Gorilla 4 2.37 0.288 36 0** 2* M2 U 5 0.805 0.092 L 6 0.813 0.058 *** P0.001, ** P0.01, * P0.05. a Compared between upper and lower molars. b Compared between the first and second molars. * P0.05. not exhibit such constancy in relation to dentine volume (Figure 3d). EDJ length measured on the MCS was rela- tively smaller in Pongo than in the other species. Table 5. Correlation coefficients between 3D AET and The 2D variables were compared between tooth type in variables representing tooth crown size Homo and Pan (Appendix 2). In both species, enamel area differed significantly between upper and lower first molars. species n Dvol BA MA The other two variables also tended to be larger in the upper Alla 74 0.183 0.207 0.178 molars. In Homo, EDJ length was longer in the first molars Homo 41 0.217 0.308 0.180 than in the second in both upper and lower jaws. Since there   Pan 22 0.248 0.165 0.209 was no such difference seen between tooth type with the 3D Pongo 7 0.900** 0.829* 0.883** Gorilla 4 0.801 0.962* 0.944 variables, these differences likely reflect shape differences that are emphasized specifically on the MCS. a All species are combined. ** P0.01, * P0.05. Other representative values of enamel thickness of the entire tooth crown As an alternative to the AET, the average of the minimum between jaws or tooth positions, in contradistinction to the thickness values taken from all OES points to EDJ was cal- suggested serial difference of enamel thickness on the MCS culated for the entire tooth crown (AMT, Table 6). The reported for human upper molars (Macho and Berner, 1993, results were similar to those of the 3D AET, in that Homo 1994). and Pan were shown to have the thickest and the thinnest enamel, respectively. The log plot against dentine volume Comparison between 2D and 3D average enamel thick- was also shown to be similar to that of 3D AET, although nesses Pongo deviated a little above the line of isometry running In order to understand the basis of the discrepancy seen through the Pan average (Figure 4). between 2D and 3D results, the variables measured on the Enamel volume was divided by basal or maximum hori- MCS were compared between taxa (Appendix 1). The pat- zontal areas of the tooth crown (AETBA and AETMA, terns seen in the 2D variables were different from those of Table 6). These measures represent the total amount of the corresponding 3D variables. For example, while EDJ enamel available for wear, relative to approximate areas of surface area differed among the four taxa, EDJ contour line occlusion available through time. When divided by the basal length was not significantly different between Homo, Pan area, significant differences were seen between all pairs of and Pongo. Figure 3 shows that these variables are not uni- the four species, except between Pan and Pongo. Similar formly related among the four species. In Pongo, 2D dentine results were obtained for maximum horizontal area of the area and EDJ length were smaller relative to their corre- tooth crown, but the exception was between Gorilla and sponding 3D values. Homo. Both values were greatest in Homo, and decreased in In 3D evaluation, EDJ surface area was shown to change order of Gorilla, Pongo, and Pan. When these measures almost isometrically with dentine volume throughout all were log-plotted against dentine volume, Gorilla and Pongo four taxa (Figure 1a). EDJ contour line length, however, did molars were distributed near the line of isometry running Vol. 112, 2004 HOMINOID MOLAR ENAMEL THICKNESS AND DISTRIBUTION 129

Figure 3. Log-plots of 2D variables measured on the MCS against the respective 3D counterparts: (a) dentine area against dentine volume; (b) EDJ contour length against EDJ surface area; (c) enamel area against enamel volume. To compare with Figure 1(a), EDJ contour length is log-plot- ted against dentine volume (d). The lines are the isometry lines running through the average of Pan. Circles, Homo; filled triangles, Pan; open tri- angles, Gorilla; crosses, Pongo.

through the Pan average, but Homo molars alone deviated from that line (Figure 5). In Homo, enamel volume relative to the horizontal crown areas was larger in the first than in the second molars (Appendix 2), although no difference was seen between tooth type in either the 3D AET or the average minimum thickness of the entire crown. No significant difference was seen between tooth type in Pan (Appendix 2).

Characteristics of within-molar enamel distribution pat- terns The molar crown was divided into two halves, in two dif- ferent ways, and the average enamel thicknesses of each molar region were compared (Table 7 and Figure 6). Cuspal, occlusal, and lateral average thicknesses differed signifi- cantly between each pair of the four species, except between Gorilla and Pongo. Basal average thickness, on the other Figure 4. Log-plot of average minimum thickness against dentine hand, did not differ significantly among taxa. When log- volume. The line of isometry runs through the average of Pan. Circles, plotted against dentine volume, each of these four variables Homo; filled triangles, Pan; open triangles, Gorilla; crosses, Pongo. 130 R.T. KONO ANTHROPOLOGICAL SCIENCE

Figure 5. Average enamel thickness values in relation to horizontal areas, log-plotted against dentine volume. Thickness is standardized by basal area (a) and maximum horizontal area (b). The lines are isometry lines running through the average of Pan. Circles, Homo; filled triangles, Pan; open triangles, Gorilla; crosses, Pongo.

Table 7. Descrpitive statistics of the measurements of regional average thickness with results of statistical comparison between taxa Mann-Whitney U-test species N x S.D. Homo Pan Pongo CAET (mm) Homo 22 2.027 0.202 Pan 22 1.026 0.124 0*** Pongo 7 1.442 0.177 2*** 3*** Gorilla 4 1.232 0.106 0** 9* 4 BAET (mm) Homo 22 0.593 0.098 Pan 22 0.553 0.073 176 Pongo 7 0.514 0.089 43 59 Gorilla 4 0.595 0.071 43 28 6 OAMT (mm) Homo 41 1.390 0.128 Pan 22 0.697 0.093 0*** Figure 6. Schematic depiction of the crown subdivisions. See the Pongo 7 1.124 0.132 22*** 0*** text for further explanations. Gorilla 4 1.013 0.124 0** 0** 6 LAMT (mm) Homo 41 0.992 0.095 showed a distinctive pattern (Figure 7). In Pongo molars, Pan 22 0.710 0.069 11*** cuspal and occlusal enamel were thicker, lateral enamel was Pongo 7 0.791 0.098 15*** 35* comparable, and basal enamel was thinner, in relation to the Gorilla 4 0.825 0.080 13** 8* 10 line of isometry passing through the Pan mean. Gorilla *** P0.001, ** P0.01, * P0.05. molars tended to have thinner enamel than those of Pan for all molar subregions except the occlusal basin. The enamel of Homo molars was thicker than that of Pan in the cuspal, nantly by the amount of enamel around the cuspal region, occlusal and lateral regions, but basal enamel did not differ and the contribution of the basal enamel is relatively small. significantly. In Homo, a weak correlation was seen between As for occlusal and lateral thicknesses, the two thickness basal enamel thickness and dentine volume. measures were comparable in Pan molars, while, in the These variables were then compared with the average molars of the other three species, occlusal thickness was thicknesses of the entire crown (Figure 8). When cuspal and greater than lateral thickness. basal thicknesses were compared with 3D AET, while basal Comparison between tooth type of the average thick- thickness did not show any trend, cuspal thickness changed nesses of the partitioned crown (Appendix 2) showed that, in proportionally with 3D AET. This indicates that the average Homo, enamel of the cervical region was thinner in the sec- thickness of the entire tooth crown is influenced predomi- ond molars than in the first molars in both jaws, while Vol. 112, 2004 HOMINOID MOLAR ENAMEL THICKNESS AND DISTRIBUTION 131

Figure 7. Log plots of regional average enamel thicknesses against dentine volume. The lines are isometry lines running through the average of Pan. Circles, Homo; filled triangles, Pan; open triangles, Gorilla; crosses, Pongo.

occlusal enamel was thicker in the second molars (although Homo, because of the differences seen between tooth type, this difference was not statistically significant in the upper the first and second molars were analyzed separately in the molars). In contrast, no significant difference was seen following comparisons. between tooth type in Pan. The difference between occlusal In the mandibular molars (Figure 10), average thickness and lateral enamel thicknesses, when both are plotted against of the occlusal surface and maximum thickness of the lateral AMT, was greater in the second molars of Homo (Figure 9), surface tended to be thick and thin at the hypoconid and but no such pattern was seen in the sample of Pan (data not metaconid, respectively. This was especially prominent in shown). In Homo, basal enamel was thicker relative to 3D the Homo molars. In Pongo molars, median and average AET in the first molars (Figure 9). thicknesses of the lateral surface were smaller in the buccal cusps than in the lingual cusps. In comparison with the apes, Cusp-by-cusp thickness distribution pattern Homo had relatively thicker enamel at the hypoconulid. In order to analyze enamel distribution patterns in more Also, the average thickness of the occlusal fovea in Homo detail, average minimum thickness of the occlusal fovea, molars was greater in the more distal cusps. Between tooth and maximum, median, and average minimum thicknesses type of Homo, it was shown that occlusal and lateral maxi- of the lateral crown surfaces were calculated respectively for mum thicknesses were greater in the second molars than in each cusp (Appendix 3, Figures 10 and 11). In Pan, only the first, except with the metaconid. All other variables of molars with no wear on the occlusal fovea were included in the metaconid were also relatively thinner in the second the analysis of occlusal thickness, assuming that slight wear molar. On the other hand, occlusal thickness of the proto- in this region may considerably affect the average value. In conid of the first molar was confirmed to be distinctively 132 R.T. KONO ANTHROPOLOGICAL SCIENCE

Figure 8. Regional average enamel thickness values plotted against average values of the entire crown. The lines are arbitrarily drawn for ref- erence. Circles, Homo; filled triangles, Pan; open triangles, Gorilla; crosses, Pongo. thin (Kono et al., 2002). lingual crown portions was most prominent in maximum In the maxillary molars (Figure 11), the overall pattern thickness of the lateral crown wall. can be summarized as thick enamel occurring at the hypo- The several noticeable patterns already described above cone and protocone, and thin enamel at the paracone. The were confirmed by Figures 12 and 13. For example, the thin difference between Homo and the great apes was not as lateral thickness of the buccal cusp in Pongo molars, the striking as that seen in the mandibular molars. Pongo molars markedly thin occlusal enamel in Pan molars relative to lat- were again unique in that, in median and average lateral eral thickness, and the difference between first and second thicknesses, the difference between buccal and lingual cusps molars in Homo, are all well expressed. was far greater than that seen in any other taxa. In Homo, there was a tendency for occlusal average thickness to Discussion increase posteriorly, as seen in the mandibular molars. Finally, thickness variables were rearranged bucco-lin- 3D AET gually to depict enamel thickness pattern in that direction Martin (1983) suggested that the ideal measure of the (Figures 12 and 13). The overall pattern of enamel thickness amount of enamel of a tooth is the volume of enamel, and transition was common in all the species regardless of differ- that, theoretically, average thickness of the enamel of the ence of absolute thickness. The buccal half of the crown is entire crown can be derived by dividing enamel tissue vol- characterized by thicker enamel than the lingual half in the ume with the surface area of EDJ. Because EDJ area is pro- lower molars (Figure 12), while the opposite is true in the portional to the number of ameloblasts producing enamel upper molars (Figure 13). The contrast between buccal and matrix, provided that ameloblast size differs little between Vol. 112, 2004 HOMINOID MOLAR ENAMEL THICKNESS AND DISTRIBUTION 133

Figure 9. Regional average enamel thickness values in human molars plotted against average values of the entire crown. The dotted lines are the least squares regression lines for each molar type. Filled circles, M1; open circles, M2. species, average enamel thickness is equivalent to the aver- it is interesting to note that average thickness values can be age amount of enamel tissue produced by a single amelo- calculated from their reported measurements, and its value blast cell. In the 1980s, however, it was technically difficult in two upper first molars (1.38 and 1.62 mm) do fall within to measure enamel volume or EDJ surface area of the entire the range of variation shown in the present study. tooth crown. Thus, as a substitute, 2-dimensional average The results of the present study, based on accurate 3- enamel thickness was introduced; enamel area was divided dimensional average thickness, provide some new insights. by EDJ contour length measured on a specifically-posi- First, the relationship between 3D AET and conventional 2D tioned section running through the two mesial cusps (Mar- AET is not simple, and may differ among species. It was tin, 1983, 1985). shown that Pan and Pongo are comparable in terms of 3D The present study is the first to achieve, with substantial AET relative to tooth size, in contrast to previous notions accuracy, an assessment of average enamel thickness in 3- based on 2D AET. Additionally, 3D AET appears to vary dimensions, derived from size variables of the tooth crown independently of tooth size within species. These points are such as enamel tissue volume (Suwa and Kono, 2000; Kono, discussed more fully in the following paragraphs. 2002). Earlier, Kimura et al. (1977) attempted 3D recon- Studies of enamel thickness are always met with the diffi- structions of the molar crown, and made rough estimates of culty of obtaining a sufficiently large sample size, because of enamel volume and EDJ surface area by stacking traced out- the usual necessity to analyze unworn or, at most, only lines of nine to 14 serially cut buccolingual sections (Kimura slightly worn teeth. It is especially difficult to obtain speci- et al., 1977). The resolution of their data was less than one- mens of great ape species. Therefore, most previous studies tenth of that of our study, and was not sufficient to discuss dealt with limited sample sizes and included molars with enamel thickness or the exact amount of enamel tissue. Yet, some wear (e.g., Molnar and Gantt, 1977; Martin, 1983; 134 R.T. KONO ANTHROPOLOGICAL SCIENCE

Figure 10. Cusp-by-cusp enamel distribution patterns in the mandibular molars. Filled circles, Homo M1; open circles, Homo M2; filled trian- gles, Pan; open triangles, Gorilla; crosses, Pongo.

Figure 11. Cusp-by-cusp enamel distribution patterns in the maxillary molars. Filled circles, Homo M1; open circles, Homo M2; filled trian- gles, Pan; open triangles, Gorilla; crosses, Pongo. Vol. 112, 2004 HOMINOID MOLAR ENAMEL THICKNESS AND DISTRIBUTION 135

Figure 12. Enamel thickness transition within the mandibular Figure 13. Enamel thickness transition within the maxillary molar molar crown. Variables are aligned in relative buccolingual position crown. Variables are aligned in relative buccolingual position across across the mesial (top) and distal (bottom) two cusps. Buccal side to the mesial (top) and distal (bottom) two cusps. Buccal side to the left. the left. Filled circles, Homo M1; open circles, Homo M2; filled trian- Filled circles, Homo M1; open circles, Homo M2; filled triangles, Pan; gles, Pan; open triangles, Gorilla; crosses, Pongo. open triangles, Gorilla; crosses, Pongo.

Shellis et al., 1998). The present study is not an exception, in to think of the correspondence between body size and tooth that only a limited number of teeth were available for size before considering the relationship between body size Gorilla and Pongo. In order to examine the possibility that and enamel thickness. If the tooth is larger than expected our results were biased by small sample size, conventional from body size, enamel thickness may appear thicker in rela- 2D AET of the present sample was compared with those tion to body size, even if it is proportional to tooth size reported in previous studies (Figure 14). The comparative (Shellis et al., 1998). Therefore it is more reasonable to use data were taken from Martin (1983) and from part of Shellis some kind of dental measure to standardize enamel thick- et al. (1998; provided by D. Reid), and thus include almost ness, instead of using a direct measure of body size (Shellis all the data published so far for the great apes. The results of et al., 1998). While Martin and his colleagues standardized the present study are confirmed not to be biased, although average enamel thickness with dentine area measured on the there are some differences seen among the studies. When MCS (Martin, 1983, 1985; Grine and Martin, 1988; inspecting Martin’s data (1983) in more detail, it is apparent Andrews and Martin, 1991), Shellis et al. (1998) plotted that he often included two or more teeth from the same indi- average enamel thickness against the dentine area. In the vidual. This probably biased the data in terms of variation. present study, both approaches were tried, and it was shown Also, wear must have been heavier in the anterior molars of that 3D AET does not differ significantly between Pan and those individuals. In the case of Pan, especially, it is likely Pongo in relation to tooth size. This differs from what Mar- that these effects lowered the species mean of 2D AET in his tin (1983, 1985) suggested, and also from the results study. obtained for 2D AET in the present study (which is in agree- Body weight is often used as the measure of body size ment with Martin’s results). Although it should be noted that when relative size is to be considered. However, it is not so 3D AET is not the only way to represent an “average thick- simple in the case of enamel thickness, since it is necessary ness”, the present results have meaningful implications. 136 R.T. KONO ANTHROPOLOGICAL SCIENCE

Figure 14. Comparison of 2D AET values. Diamonds, from Martin (1983); circles, this study; crosses, from Shellis et al. (1998; provided by D. Reid). Worn specimens are placed slightly to the right. For the molars included in the study of Martin (1983), presence of wear follows his own notes.

Martin (1983) explained that the reason for using the tooth size as represented by the horizontal areas of the tooth MCS in “estimating” average thickness of enamel was crown. During the course of odontogenesis, the topography because the MCS should be the most “radial” section, and of EDJ is the first to be formed, and apposition of dentine not “oblique”. The assumption is that an “oblique” section and enamel starts at each side of the EDJ proceeding in would not cut the enamel perpendicular to the EDJ or OES, opposite directions. Therefore the size of the tooth crown is and thus would inflate enamel thickness values. Our own 3D intimately related to EDJ formation, while enamel thickness datasets enable an evaluation of this assumption. We find is determined by the extent to which the ameloblasts con- that the 3D topography of the EDJ and OES is sufficiently tinue to deposit enamel matrix. Thus, it is quite reasonable complex, that even with the relatively simply shaped lateral that these two heterochronological processes are controlled crown face the MCS does not necessarily produce a more independently (Hlusko et al., in press). “radial” section relative to other crown sections. Indeed a Total enamel volume relative to occlusal view size of a true “radial” section would take the form of an undulating molar can be considered as a rough measure of durability or “ribbon”-like non-planar section (Kono and Suwa, 2000). longevity of the tooth. The present results show that the We therefore reject the notion that the MCS is superior to above measure increases almost isometrically among taxa other sections in evaluating overall enamel thickness. except with Homo, which conspicuously deviates towards a How then would one interpret the differences observed greater amount of enamel for a given tooth size. This could between 2D AET taken at the MCS and whole-crown 3D be interpreted as revealing that human molars are much AET? It is suggested by this study that local differences in more durable against wear compared to those of great apes. tooth crown shape may be emphasized on specific cross sec- Possibly, human molars might have adapted to different tions, such as the MCS. For example, when cusp steepness functional demands from that of the great ape species. One differs, EDJ length at the MCS would differ proportionately must keep these possibilities in mind when comparing more so than would total EDJ surface area. Therefore, it is enamel distribution patterns within the tooth crown. possible to say that 2D AET is not necessarily a good esti- It is noteworthy that Gorilla molars, from the same crite- mator nor an adequate substitute of 3D AET, even though it ria, are as durable as the relatively thicker enameled Pan and may have its own significance. In as much as 3D AET of the Pongo molars, in terms of potential resistance to wear. present study is considered an ideal overall measure of While an evaluation of 3D AET shows Gorilla molar enamel thickness (e.g., Martin, 1983; Conroy, 1991), both enamel to be relatively thinner than that of the other species, Pan and Pongo molars are characterized by comparable enamel volume per horizontal section area of the crown is overall enamel thickness relative to tooth size. absolutely greater than, and comparable in relation to tooth Previous studies suggest that developmental mechanisms size with, molars of the other ape species. Hypsodonty is that determine tooth size and enamel thickness are not nec- well known in herbivorous mammals such as horses, as an essarily correlated or dependent upon each other (e.g., But- adaptation to high wear rates (Janis and Fortelius, 1988). In ler, 1956; Harris et al., 2001). In the present study, no Gorilla molars, even though enamel is thinly distributed, the significant correlation was seen between tooth (dentine) size total amount is kept sufficient by means of their high cusps and AET, within each of the Homo and Pan molar samples. and greater occlusal relief. Also, no correlation was seen between enamel thickness and Macho and Berner (1993, 1994) suggested that enamel Vol. 112, 2004 HOMINOID MOLAR ENAMEL THICKNESS AND DISTRIBUTION 137 was thicker in the posterior molars than in the first molar of the minor and variable local details of EDJ and OES topog- the human maxillary dentition. They interpreted this as raphy. Slight displacements of section position and/or small showing that posterior molars resist greater loads during amount of wear may affect linear measures considerably, mastication. On the other hand, if enamel thickness in especially those of the occlusal surface. On the other hand, humans is primarily an adaptation to resist tooth wear, the parameters defined to represent thickness of crown regions first molars are expected to have thicker enamel than the are less susceptible to such problems, and were used in the posterior molars, since the first molars erupt earlier and must present study to assess within tooth distribution patterns of function the longest. The present results show that in mea- enamel thickness. sures such as total enamel volume, 3D AET, and thickness In his comparisons of molar enamel thickness of great relative to horizontal crown areas, the first molars do tend to apes and humans, Schwartz (1997, 2000a) proposed that it is exhibit greater values than the second molars, despite its possible to discriminate species from enamel thickness pat- thinner enamel near at certain locations of the crown, as terns on the MCS of the maxillary molars. His data of great reported by Macho and Berner (1993, 1994). apes were taken from Martin (1983), and that of humans The functional interpretation of Macho and Berner (1993, from Macho and Berner (1993, 1994). Since the definitions 1994) was based on the notion that bite force becomes of the measurements are partly different between these stud- greater posteriorly, although this has not yet been conclu- ies, it is doubtful if the results based on the mixed data-set sively shown. The opposite condition was suggested in two are reliable. In addition, according to Schwartz’s interpreta- in vivo studies, that bite force is actually greater at the first tion, enamel thickness measured at the protocone tip is sug- molar than at the second molar position (Mansour and Rey- gested to be a key variable in discriminating Pan and Gorilla nick, 1975; Pruim et al., 1980). In several papers, bite force molars. The sample of Pan molars used in Martin’s (1983) was calculated, using a biomechanical model, to be greater study, however, includes considerably worn molars (judging at the posterior tooth positions (Osborn and Barager, 1985; from his photographs), which renders his thickness values at Koolstra et al., 1988). These simulation studies were based the protocone tip unreliable. Because of these uncertainties, on the assumption that the chewing muscles are potentially it is not clear if the discrimination made by Schwartz was equally active regardless of biting position. Spencer (1998) genuine, or an artifact of methodological limitations. studied the relationship between chewing position and activ- Although it is not possible to compare the present results ity levels of the temporal and masseter muscles, and showed directly with previously published 2D based measurements, that the two muscles are most active when chewing at the it is still worthwhile to see enamel distribution patterns in a first molar position. This does not directly suggest a greater similar manner. When the regional variables of thickness of bite force at the first molar, but does point out that some of each cusp are aligned in buccolingual direction for the two the assumptions of the simulation studies may not be realis- mesial and two distal cusps (Figures 12 and 13), a general tic. Macho and Spears (1999) have recently noted that crown pattern common to all four species is seen, despite the con- topography, rather than enamel thickness, is more important siderable differences in absolute thickness. In the “func- in a molar’s ability to resist mechanical loads. tional” sides of the crown, that is the buccal side in Burak et al. (1999) reported that the speed of abrasion dif- mandibular molars and the lingual side in maxillary molars, fers between enamel and dentine, when each tissue is rubbed enamel is thicker than it is in the other side in all the species. against each other. Their results showed that dentine wears There is no evidence that Pan and Gorilla molars differ faster in general. This means that a greater amount of enamel markedly in terms of occlusal thickness of the protocone for a given crown size would allow the tooth to last longer in (contra Schwartz, 1997, 2000a). function, supporting the view that enamel thickness could be The present results reveal, on the other hand, some dis- an adaptation to resist abrasion. On the other hand, it was tinct aspects of enamel distribution pattern among the four further suggested by Burak et al. (1999) that enamel also species analyzed (Figure 15). Pan molars have relatively wears as fast as dentine when rubbed under certain magni- thin enamel in their occlusal fovea, whereas, in Pongo tudes of load. It is possible that, not only with tooth-tooth molars, enamel is notably thick in the occlusal fovea but contact but also with tooth-food contact, enamel wears faster thins towards the basal cervical region. In Homo molars, the under greater loads (discussed in Maas, 1994). Supposing cuspal region shows thickly distributed enamel while the that the greater the load, the faster the enamel wears, it can basal cervical region is comparable to the condition seen in be said that thickening of enamel does increase a molar’s Pan. In Gorilla molars, enamel is relatively thin throughout “resistance” to mechanical load (e.g., Butler, 2000), the crown. Beynon et al. (1991) reported that enamel depo- although in a way different from mechanical strengthening. sition rate increases from EDJ to the outer surface in great ape and human molars, but that the amount of such increase Enamel distribution patterns of the whole molar crown is less in Pongo and Homo molars cervically. The above out- The present study is the first to compare enamel distribu- lined differences in lateral crown enamel might be based on tion patterns of the whole molar crown, as far as we are such differences of enamel deposition speed. aware. In this study, local measures of enamel thickness Previously, Pan and Gorilla were both treated as “thin were not taken on certain sections but defined so as to repre- enameled” species. The present results distinguish these two sent regions, such as the average thickness of the occlusal species in terms of enamel distribution pattern. Enamel of surface enamel of the protoconid, or maximum thickness of the occlusal fovea is relatively thin in the molars of both spe- the entire lateral surface of the metacone. Linear measure- cies, but that of the lateral crown face is relatively thicker in ments on particular sections are more prone to be affected by Pan than in Gorilla. Pongo was assigned to the “intermedi- 138 R.T. KONO ANTHROPOLOGICAL SCIENCE

Figure 15. Thickness maps of mandibular first molars of the four species. Thickness values are shown in color grading. Top left, human; top right, orangutan; bottom left, chimpanzee; bottom right, gorilla. ately thick” category and regarded as expressing the condi- than fruit-eating species (Kay, 1975, 1977, 1981). tion closest to that of Homo, but the present study shows The present results show that the Gorilla molar has rela- that, on average, its enamel thickness is not different from tively thin enamel throughout its crown. Cusps of the that of Pan. Rather, the distribution pattern in Pongo molars Gorilla molar are relatively high compared to those of the is unique, as described above, and thus differs from either other species (Kobayashi, 2001). The combination of tall Homo or Pan conditions. Interestingly, average or median cusps and thin enamel is likely to be an evolutionary and/or thickness of the lateral surfaces of the buccal cusps was developmental correlate, as part of an adaptation to folivo- found to be notably thin in both upper and lower molars of rous diet. It may be a way to make shearing efficient, at the Pongo. Since the functional significance along the buccolin- same time retaining the functional longevity of the tooth. gual direction is reversed between upper and lower molars, Pongo is known as a frugivore, as with Pan, but differs this common pattern of thickness involving the same side in from the latter in including substantial amounts of hard- molars of both jaws is difficult to interpret in terms of func- shelled seeds (Fleagle, 1999). It is arguable that an occlusal tion. It is likely that this is a unique aspect of the Pongo surface covered with enamel, rather than the more elastic molar, perhaps related to developmental pattern of its cervi- dentine, is advantageous when eating hard and brittle cal enamel. objects, such as nuts or some fruits. Cusps are less steep in Gorilla is known to be dependent on a relatively folivo- Pongo molars compared to Gorilla and Pan (Hartman, 1988, rous diet, with high intake of leaves and stems, than any 1989), and this could also be interpreted as an adaptation to other great ape species (Fleagle, 1999). Teeth of herbivorous the crushing of hard and brittle food stuffs (Spears and animals, in general, are characterized by thin, vertically-ori- Crompton, 1996). ented blade-like enamel ridges on their worn occlusal sur- Pan is highly dependent on softer ripe fruits, but with a faces. Dietary items consisting of cellulose-rich plant parts, significant omnivorous component (Fleagle, 1999). The dis- such as grass, are mechanically broken down by the shearing tribution pattern of enamel in Pan molars is characterized by force exerted when these blades run across each other (Lucas the distinctly thin occlusal fovea enamel. Considering the and Luke, 1984; Janis and Fortelius, 1988). Thus, the effec- fact that the outer surface morphology of the tooth crown is tive length of shearing blades governs the efficiency of mas- determined by a combination of the original EDJ topography tication. It has been shown that among primates, leaf-eating and the amount of enamel deposited onto it, it is reasonable species tend to have higher cusps and longer shearing crests to think that selective pressures would act on enamel thick- Vol. 112, 2004 HOMINOID MOLAR ENAMEL THICKNESS AND DISTRIBUTION 139 ness to regulate crown surface morphology. The occlusal Homo to enhance wear resistance, they both may well repre- fovea of Pan molars is larger than it is in the other three spe- sent derived conditions. If this is the case, then the overall cies in relation to total crown area or molar length, and is rel- enamel thickness in the last common ancestor is likely to atively deep compared to that of Pongo (Kobayashi, 2001). have been intermediate. The observed pattern of enamel distribution in Pan might The results of the present study further show that taxo- have been achieved by thinning the occlusal enamel in order nomic differences are not only manifested in overall enamel to acquire a deep and wide occlusal basin. In this way, thickness, but that the pattern of enamel distribution can be molars of Pan might have increased their crushing capaci- distinct. It can be said that Homo and Gorilla molars tend to ties, while at the same time maintaining some degree of have relatively thick or thin enamel throughout the crown, shearing efficiency. respectively, while the basal crown region in Pongo molars Human molars are distinctive from those of great apes in and the occlusal fovea in Pan molars show markedly thin the overall thickness of enamel. Interestingly, the variation enamel. It is likely that these latter conditions are derived of enamel thickness among cusps is greater than that seen in (judging from published section images of a variety of great ape molars. Buccolingual contrasts are most apparent Miocene hominoid material), in which case molar enamel of in Homo molars, although it is not clear to what extent such the last common ancestor can be hypothesized, in terms of patterns have functional meaning (Kono et al., 2002). Alter- pattern, to be relatively evenly distributed. natively, relative magnitudes of within-tooth differences in The above hypothesized sequence of enamel thickness enamel thickness might be exaggerated because the enamel evolution is schematically depicted in Figure 16. Each of the is simply thicker on the whole. According to Macho and extant four species could be regarded as distinctly derived; Spears (1999), human molars are generally less adapted to that is, in Homo and Gorilla molars, largely in overall thick- resist loads than those of Pan and Pongo. On the other hand, ness, and in Pan and Pongo molars, largely in distribution the present results indicate that human molars are more pattern. Recent discoveries of hominid fossils from the Mio- resistant to abrasion than those of great ape species. Taking Pliocene deposits of Africa (White et al., 1994, 1995; these aspects into account, human molars are most likely Leakey et al., 1995; Haile-Selassie, 2001; Senut et al., 2001; adapted to increase their resistance to abrasion, but not nec- Brunet et al., 2002) are expected to shed light on such essarily to withstand high magnitude of mechanical load. hypotheses of enamel thickness evolution. Based on this assumption, certain portions of the crown with In Homo molars, enamel was shown to be distributed dif- thicker enamel are expected to wear more quickly. The gen- ferently in the first and second molars. When occlusal and eral pattern of molar wear is in accordance with this view, lateral crown enamel is compared, the difference of thick- since the buccal side of lower molars and the lingual side of ness in the two regions is less in the first molar than it is in upper molars wear faster than the opposite sides (e.g., Mur- the second; i.e., human second molars exhibit a relatively phy, 1959; Smith, 1984). It should be noted, however, that, enhanced occlusal thickness. This resembles the condition in the lower molars, the protoconid is the first cusp to wear seen between Pan and Pongo molars. Macho and Berner (Murphy, 1959), although its enamel is not thicker than that (1993, 1994) suggested that, in humans, enamel is thicker in of the hypoconid which begins to wear later. Therefore, not the posterior molars than in the first molar. According to the all patterns seen in human molars are interpretable in terms present data, while the average thickness of the entire crown of adaptation to wear resistance, and developmental con- was not significantly different between first and second straints are surely an important part of this complex set of molars, occlusal thickness was found to be thicker in the sec- relationships. ond than in the first molar. This is in accord with their Previous discussions concerning the evolutionary history results, since the thickness variables they studied were of enamel thickness diversity seen within extant hominoid species focused mainly on the status of the last common ancestor of these taxa in terms of overall thickness, such as “thick” or “thin”, and the mode of enamel formation, such as “fast” or “slow” forming. Overall enamel thickness as judged by 2D AET is known to vary greatly, ranging from thin to very thick among extinct Miocene hominoid species (Nagatoshi, 1990; Andrews and Martin, 1991; Conroy et al., 1995; Beynon et al., 1998; Schwartz et al., 2003; Smith et al., 2003). We have elsewhere suggested that molar enamel thickness is potentially sensitive to selective pressures and thus prone to evolve in parallel (Hlusko et al., in press). Therefore it is difficult to determine the ancestral condition from the pattern seen among extant species. However, it is possible to propose a plausible hypothesis based on the present results. The overall thickness of molar enamel is shown to be comparable between Pan and Pongo, thicker in Homo, and thinner in Gorilla. Considering that the thin Figure 16. Enamel thickness and distribution pattern of the four enamel of the Gorilla molar was likely acquired in order to extant species and the hypothetical last common ancestor (LCA). See increase its shearing efficiency, and the thick enamel of the text for details. 140 R.T. KONO ANTHROPOLOGICAL SCIENCE defined at the occlusal and cuspal region on the MCS. tion patterns of molar enamel. Although the molars of Pan Therefore, for the occlusal region, it can be said that enamel and Pongo are comparable in terms of average enamel thick- thickness increases posteriorly within the human molar row. ness, they differ significantly with regard to enamel distribu- Occlusal enamel also tends to be thicker posteriorly tion patterns. Chimpanzee molars are characterized by within a human molar crown (Kono et al., 2002). Still, when markedly thin enamel of the occlusal fovea. Orangutan comparing the first and second molars, enamel is not thicker molars are characterized by thicker enamel occlusally and in the mesial part of the second molar than it is in the distal thinner enamel toward the basal cervical region. In gorilla part of the first molar. Such details of enamel thickness pat- and human molars, such distinctive thickness patterns were terning, within the molar row, do not conform to the simple not seen. expectation of occlusal load, hypothesized to increase poste- Based on the above enamel thickness and distribution pat- riorly along the molar row. Thus, within-tooth patterning of terns seen among the extant hominoid species, molar enamel enamel thickness in human molars cannot entirely be inter- of the last common ancestor is hypothesized to have been preted as a simple functional adaptation to resist greater intermediately thick and relatively evenly distributed. occlusal load that increases distally, such as was suggested According to this view, each of the extant four species exhib- by Macho and her colleagues. its some distinctly derived condition. From the hypothesized Kono et al. (2002) reported a unique pattern of thickness condition of the last common ancestor, in human and gorilla in human first molars, in revealing enamel to be unexpect- molars, thickness would have changed, and in chimpanzee edly thin around the tips of the mesiobuccal cusps in both and orangutan molars, distribution pattern would have upper and lower first molars. This is not the case in human changed. Such hypotheses of enamel thickness evolution second molars, as visually judged by the occlusal T-map data may be tested by future anatomical, developmental, and (data not shown; see Kono et al., 2002 for methods). Numer- paleobiological studies. ical evaluations also show that average enamel thickness of the occlusal surfaces of the mesiobuccal cusps (paracone Acknowledgments and protoconid) is thicker in the second molars than in the first. These results suggest that factors such as EDJ cusp I would like to thank the following individuals who kindly saliency and topography may have direct developmental allowed access to the specimens: Gen Suwa, The University consequences to enamel thickness patterning, and should be Museum, The University of Tokyo; Yuji Mizoguchi, a focus of future investigations. National Science Museum; Tim D. White, University of Cal- ifornia at Berkeley; Bruce Latimer, Cleveland Museum of Summary and Conclusions Natural History. Don Reid kindly made original data avail- able from previous studies. Special thanks go to Toyohisa In this study, molar enamel thickness and distribution pat- Tanijiri of Medic Engineering Inc., for cooperating with us terns of human, chimpanzee, gorilla and orangutan perma- through the development of the Rugle series, and to Atsushi nent molars were investigated and presented, for the first Murakoshi and people at TESCO Corporation for providing time, for the entire tooth crown. It is demonstrated that thick- technical support with the CT scanner. Finally I thank Gen ness and/or distribution pattern of enamel is not a simple Suwa for his unlimited support, encouragement, and many matter to evaluate. For example, 3D-based assessments of invaluable comments, throughout this painstaking study. whole-crown features, such as enamel tissue volume and EDJ surface area, yield results different from those previ- ously recognized from 2D-based studies. 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Appendix 1. Discriptive statistics of the original variables and results of statistical comparison between taxa 144 R.T. KONO ANTHROPOLOGICAL SCIENCE

Appendix 2. Discriptive statistics of the original variables with results of statistical comparison between tooth type Vol. 112, 2004 HOMINOID MOLAR ENAMEL THICKNESS AND DISTRIBUTION 145

Appendix 2 (continued) 146 R.T. KONO ANTHROPOLOGICAL SCIENCE a cusp h eac f ues o l ness va k c hi t l ve ename i representat f cs o i st i ve stat i pt i scr i . D 3 x i ppend A