American Journal of Primatology 72:481–491 (2010) RESEARCH ARTICLE Dental Wear, Wear Rate, and Dental Disease in the African Apes ALISON A. ELGART Department of Biological Sciences, Florida Gulf Coast University, Fort Myers, Florida The African apes possess thinner enamel than do other hominoids, and a certain amount of dentin exposure may be advantageous in the processing of tough diets eaten by Gorilla. Dental wear (attrition plus abrasion) that erodes the enamel exposes the underlying dentin and creates additional cutting edges at the dentin-enamel junction. Hypothetically, efficiency of food processing increases with junction formation until an optimal amount is reached, but excessive wear hinders efficient food processing and may lead to sickness, reduced fecundity, and death. Occlusal surfaces of molars and incisors in three populations each of Gorilla and Pan were videotaped and digitized. The quantity of incisal and molar occlusal dental wear and the lengths of dentin–enamel junctions were measured in 220 adult and 31 juvenile gorilla and chimpanzee skulls. Rates of dental wear were calculated in juveniles by scoring the degree of wear between adjacent molars M1 and M2. Differences were compared by principal (major) axis analysis. ANOVAs compared means of wear amounts. Pearson correlation coefficients were calculated to compare the relationship between molar wear and incidence of dental disease. Results indicate that quantities of wear are significantly greater in permanent incisors and molars and juvenile molars of gorillas compared to chimpanzees. The lengths of dentin–enamel junctions were predominantly suboptimal. Western lowland gorillas have the highest quantities of wear and the most molars with suboptimal wear. The highest rates of wear are seen in Pan paniscus and Pan t. troglodytes, and the lowest rates are found in P.t. schweinfurthii and G. g. graueri. Among gorillas, G. b. beringei have the highest rates but low amounts of wear. Coefficients between wear and dental disease were low, but significant when all teeth were combined. Gorilla teeth are durable, and wear does not lead to mechanical senescence in this sample. Am. J. Primatol. 72:481–491, 2010. r 2010 Wiley-Liss, Inc. Key words: dental wear; African apes; wear rate INTRODUCTION Gorillas (Gorilla gorilla and Gorilla beringei beringei) are presumed to possess numerous adaptations to deal with the communition of an herbivorous, tough diet [e.g., Blower, 1956; Carroll, 1988; Cousins, 1988; Groves, 1966, 1971; Remis, 1994; Sarmiento et al., 1996; Schaller, 1963]. In the absence of any gorilla fossil evidence, it is not possible to trace the historical genesis of these adaptations, but the three gorilla populations are assumed to have similar dietary ‘‘selective regimes’’ in comparison to other taxa that would determine the fitness of certain traits [Baum & Larson, 1991]. Adaptations will be defined here as traits that enhance performance in an individual. This will be tested by their ‘‘current utility’’ [Baum & Larson, 1991; Gould & Vrba, 1982; Greene, 1986; Losos & Miles, 1994]. Performance, defined as how an individual carries out a task, determines what resources can be used, and in turn will have an impact upon reproduction and survival (fitness) [Wainwright, 1994]. Traits that affect the processing of food and test durability, such as dental wear rate, r 2010 Wiley-Liss, Inc. quantity of dental wear, and presence or absence of dental pathology related to dental failure, were chosen to test performance. This study was part of a wider study examining masticatory functional morphology using the phylogenetic method in which Gorilla is compared to its sister taxon, Pan. Like any tool, teeth are subject to surface wear from use. To date, no studies have correlated the true toughness of food to the quantity of dental wear in animals, although such wear and friction studies are carried out in materials science. Previous studies have demonstrated that excessive dental attrition can have dire effects in organisms, from reduced Contract grant sponsor: Mario Einaudi Center of Cornell University, Kosciusko Foundation. Correspondence to: Alison A. Elgart, Department of Biological Sciences, Florida Gulf Coast University, 10501 FGCU Blvd. South, Fort Myers, FL 33965. E-mail: email@example.com Received 19 May 2009; revised 8 December 2009; revision accepted 12 December 2009 DOI 10.1002/ajp.20797 Published online 13 January 2010 in Wiley InterScience (www. interscience.wiley.com). 482 / Elgart fecundity to early mechanical senescence [Lanyon & Sanson, 1986; Raupp, 1985]. Once the enamel is worn away, the processing of food on the underlying dentin is very inefficient in comparison to enamel, and an animal has to either consume more food or chew more in order to survive [Lanyon & Sanson, 1986; Pérez-Barberı́a & Gordon, 1998]. The mountain gorilla (Gorilla beringei beringei) diet is highly herbivorous and is presumed to be tough relative to other gorilla populations [see Elgart-Berry, 2004]. Gorillas in general possess molars with higher cusps and ‘‘greater shearing’’ capabilities than other African apes [Kay, 1975, 1981; M’Kirera & Ungar, 2003; Shea, 1983; Uchida, 1996], as is expected with a tough diet. They have the thinnest enamel of any ape [Kay, 1981; Kono, 2004; Olejiniczak et al., 2008; Vogel et al., 2008], which may be advantageous because it wears quickly creating additional cutting edges between the enamel and dentin [Aiello et al., 1991; Kay, 1985; Kono, 2004; Mills, 1978; Vogel et al., 2008]. Whether this constitutes an adaptation in Gorilla or G. b. beringei, in particular, will be tested by examining if teeth are worn to a theoretical optimal level. It has previously been reported that Gorilla has greater quantities of dental wear than Pan and Pongo, mainly due to an earlier weaning age [Aiello et al., 1991], but studies are not conclusive as to which gorilla species demonstrates the greatest amount [Cousins, 1988; Welsch, 1967]. This study will examine whether mountain gorillas have greater dental wear than other African apes and whether this is correlated with dental disease. High degrees of wear may either be directly fatal, affecting food processing, or indirectly fatal by causing disease, which in turn affects food consumption. The overall quantity and position (anterior vs. posterior) of dental wear between two species each of gorillas and chimpanzees were calculated by measuring the mean percent area of dentin exposure on the occlusal surface of the teeth for each molar tooth and for the incisors using digital imaging. Quantity of wear is, of course, correlated with age; therefore, rates of dental wear were also calculated in juvenile Pan and Gorilla by scoring the quantity of wear between adjacent molars M1 and M2. eating brittle food. At the very least, this would cause the teeth to come into contact more often with the abrasives found either outside the food plants (dust) or inside the food plants (phytoliths), causing greater dental wear [Fortelius, 1985; Janis, 1995; Lucas et al., 1986]. Raupp  demonstrated that beetles wore their mandibles faster when they fed on ‘‘tougher’’ leaves, and consequently, worn mandibles slowed ingestion rates and lowered fecundity. According to Fortelius , Laws observed that hippopotami graze on grass and water plants, but have evolved from mammals that were not grazers. Their diet is tougher and more abrasive than that of their ancestors, and they incur such high degrees of wear on their teeth that they often die of mechanical senescence at ages older than 30 years. Hypothetically, a similar situation may be present in some gorillas. Gorilla Morphology at the Species Level Like hippopotami, gorillas have evolved from primates that were not strict herbivores. Miocene hominoids were probably frugivorous [Andrews, 1981; Kay, 1977; Nelson, 2003] and most extant apes have a diet consisting predominantly of ripe fruit. Gorillas have larger molars with higher cusps, greater shearing, crushing, and grinding capabilities than other African apes [Kay, 1975, 1978, 1981; Kay & Hylander, 1978; Shea, 1983; Uchida, 1996], and about 6% have fourth molars [Schultz, 1950]. Gorillas also have higher, narrower dentin horns, extensions of dentin that present as pointed cusps due to the thin enamel, in comparison to orangutans and chimpanzees [Shellis et al., 1998]. Relative to the molars, gorillas have smaller, narrower incisors than do other apes [Kay & Hylander, 1978; McCollum, 2007]. Morphological distinctions exist at the gorilla species level as well. Mountain gorillas (G. b. beringei) may exhibit adaptations to a herbivorous diet such as larger teeth, more developed jaw musculature, higher crowned molars, extra cusps five and six on the upper teeth and an extra cusp six on the lower teeth, and a longer tooth row in comparison to western lowland gorillas (G. g. gorilla) [Booth, 1971; Cousins, 1988; Groves, 1970; Uchida, 1996]. Wear and Physical Properties of Food In certain dental wear studies, physical properties are inferred, albeit not directly tested. Smith , investigating dental wear in several human populations, found a high correlation between the rate of wear and the ‘‘properties of the diet,’’ although these are not detailed. Welsch  concluded that folivorous primates had more wear on their posterior teeth than did frugivorous primates. Animals that masticate tougher foods would have to chew these foods more thoroughly than those Am. J. Primatol. Gorilla Dental Wear and Pathological Conditions Previous studies have reported moderate amounts of periodontal disease in gorillas. Mountain gorillas suffer from heavy calculus deposits, which result in 100% of adult museum specimens exhibiting alveolar destruction [Cousins, 1988; Lovell, 1990]. Lovell  reported that out of 22 individuals in Fossey’s mountain gorilla collection, 18% suffered from periapical abscesses and 45% had Dental Wear in African Apes / 483 interdontal abscesses, and each individual had lost approximately one tooth ante-mortem. Schultz , whose study collection did not include mountain gorillas, concluded that abscesses were found in similar frequency in gorillas and in other apes. Lowland gorillas have smaller teeth and mandibles than the highland species, and their premolars and molars are crowded. They also suffer from alveolar abscesses [Elgart-Berry, 2000]. Cousins  reported less dental wear in mountain gorilla teeth compared to lowland gorilla teeth, due to the extra cusps, but conversely Welsch [1967, p 989] reported ‘‘especially heavily worn teeth’’ in mountain gorillas in comparison to other apes. A certain amount of wear on molars is advantageous to gorillas. Attrition will wear the enamel covering the molar cusps and the dentin below will be exposed, thereby creating additional cutting edges at the dentin–enamel junction [Aiello et al., 1991; Kay, 1985; Kono, 2004; Mills, 1978; Vogel et al., 2008]. Tools are often made with a hard, wearresistant material next to a softer one, so that differential wear has the effect of sharpening the structure [Rabinowitz, 1995], which is akin to the positioning of enamel (hard and wear resistant) next to dentin (soft) in worn teeth. An animal example of this is found in rodent central incisors, which lack enamel on the lingual aspect thereby maintaining a sharp edge. As teeth wear, additional enamel–dentin cutting edges increase until a certain time, when the ‘‘dentin lakes’’ begin to merge. Further wear blunts and obliterates the enamel edges until finally the whole occlusal surface is exposed dentin, all the cutting edges are gone, and wear is very rapid through the soft dentin. The molars are worn down to stubs and they are virtually useless in processing food, as demonstrated in koalas and red deer [Lanyon & Sanson, 1986; Pérez-Barberı́a & Gordon, 1998]. Animals with excessive dental wear exhibit a higher number of chews per amount of food ingested, lower food intake, spend longer periods of time chewing, and have larger fecal particles. Lanyon and Sanson [1986, p 171] conclude ‘‘tooth wear is (thus) ultimately responsible in determining the physiological well-being and hence longevity of an animal.’’ In this study, gorillas are expected to have a greater degree of wear than chimpanzees, but it is hypothesized that the position of this wear will differ. Generally, frugivores exhibit greater wear of anterior teeth than of posterior teeth, as demonstrated in colobus [Janis, 1984] and chimpanzees [Dean et al., 1992]; therefore, it is expected that gorillas will have more posterior wear in comparison to chimpanzees. However, confounding variables include the ingestive positioning of food and ambient dust. For example, Bwindi gorillas (G. b. beringei) were observed to pull stems and bark through their incisors as well as postcanine teeth [Elgart-Berry, 2000], and therefore, not all incisal wear can be attributed to fruit ingestion. If the attrition of the thin enamel of the gorilla is an adaptation, gorillas should have a higher wear rate than chimpanzees and should have more teeth at optimal wear states, although optimality is not a necessity for identifying adaptations [Greene, 1986]. If performance is not affected, gorilla teeth should be durable; pathological conditions related to dental failure should not be correlated with the amount of dental wear in individuals. METHODS Skeletal collections were accessed from the National Museum of Natural History, Washington, DC, The Cleveland Museum of Natural History, Cleveland, and the Musée Royal de L’Afrique Centrale, Tervuren, Belgium. This study did not involve any living primates; therefore, the research protocols and ethical standards for working with such primates do not apply. The research did adhere to all legal requirements. Dental wear (attrition plus abrasion) was quantified on the incisors and molars of 39 Gorilla beringei beringei, 32 Gorilla gorilla graueri, 69 Gorilla gorilla gorilla, 19 Pan paniscus, 53 Pan t. troglodytes, and 8 Pan t. scheweinfurthii adult crania (Table I). Wear of deciduous dentition (aged 3–6 years) was measured in 5 G. b. beringei, 5 G. g. graueri, 13 G. g. gorilla, and 8 P. t. troglodytes. Using a method similar to Uchida , the occlusal surface of the dentition was videotaped using a Sony Hi-8 video camera fitted with a macro-lens positioned on a tripod perpendicular to the cervical line of the teeth. A horizontal plane was achieved by placing a line level on the occlusal surface of the teeth. A scale was placed either on the teeth or next to them at the level of the occlusal surface and the scaled image of two teeth was digitized using the program NIH Image (developed by W. Rasband). Each dentin lake TABLE I. Dental Wear Measurements Taken Areas of dentin quantified (in mm) Adults 1. Right I1 and I2 (or left where right is missing) 2. Lingual half of M1, M2, M3 3. Buccal half of M1, M2, M3 4. Right I1 and I2 5. Lingual half of M1, M2, M3 6. Buccal half of M1, M2, M3 7. Occlusal surface area 8. Dentin area percentage: ((lingual1buccal dentin)/occlusal surface area) 9. Perimeter of dentin exposures Juveniles: all the above measurements except (a) Right i1, i2, i1, and i2 where present (b) Right m1, m2, m1, m2 (c) Right M1 and M1 only Am. J. Primatol. 484 / Elgart TABLE II. Index of Dental Pathology Dental disease categorization 1. No dental pathology observed 2. Minor dental pathology present, e.g., calculus or roots partially exposed 3. Moderate dental pathology present, e.g., one abscess, or two minor conditions or two or more teeth lost premortem 4. Three or more pathological conditions present in dentition including at least one abscess 5. Severe dental pathology, e.g., multiple abscesses Fig. 1. Digitized image of two mandibular molars with dentin lakes traced. was traced (Fig. 1). Image calculated the area and perimeter of the whole tooth and the area of dentin exposure. Quantity of wear is measured in two dimensions only, so total wear will be underestimated. This type of study ignores the wear of the enamel before dentine is exposed, as Mayhall and Kageyama  point out, but gorillas and chimpanzees have thin enamel. Other measurements include the lengths of dentin–enamel junctions (the ‘‘blades’’) on all molars to test how many individuals exhibit the ‘‘optimum’’ in length [Alexander, 1996; Lanyon & Sanson, 1986]. These lengths were measured and calculated as the perimeter of enamel on M1–M3, and the optimal length was defined as the maximum amount that the perimeter measures before the junctions are obliterated by further wear and the lengths decrease. Dental wear that has not reached the optimum in length is referred to as ‘‘suboptimal,’’ while wear that is past the optimum is ‘‘supra-optimal.’’ A polynomial regression of the second order was run to examine the relationship between the perimeter and the mean amount of wear across the three molars, the latter of which loosely estimates age. A regression plot depicts the optimum at maximum y where x 5 xmax and the slope of the line is zero [Alexander, 1996]. The mean percent area of dentin was calculated for each molar and incisor. Mean and standard deviations of percent wear were calculated for each tooth per species, and ANOVAs contrasted the means of dentin exposure of the Pan species, the three populations of adult gorillas, and the juveniles. Incisal to molar wear ratios comparing wear on the maxillary first incisor (I1) to the maxillary first molar (M1) were tested for significant differences by a paired t-test. Ante-mortem tooth loss and dental disease (abscesses, caries, and excess calculus) were recorded in all specimens. Severity of pathology was categorized according to an index (Table II), with 1 scored if there is no pathology related to the dentition and 5 scored if severe dental disease is present. Pearson correlation coefficients were calculated first between Am. J. Primatol. the quantity of wear on maxillary M1 and the pathology index and second between the quantity of wear on the maxillary I1 and the index to test whether a linear relationship exists between each pair. A Fisher’s r to z transformation was carried out on the correlations and 95% confidence intervals were calculated to test for significance. Wear Rate Compromising this wear study is the lack of known ages for most museum specimens; therefore, an ageindependent measurement, dental wear rate, was calculated [Molnar et al., 1983; Rose & Ungar, 1998; Scott, 1979; Smith, 1972]. Rate of wear was compared in juvenile Pan and Gorilla by the principal axis technique [Benfer & Edwards, 1991; Scott, 1979], which is based on measuring the amount of wear on M1 when M2 comes into occlusion, and represents approximately 2.7 years of wear in apes [Aiello & Dean, 1990]. It employs Model II regression, which does not assume that the X variable is measured without error [Sokal & Rohlf, 1995]. Furthermore, there is no causal relationship between each x and y (wear on M1 and M2 in this case) warranting least-squares regression analysis. Model II regression defines an ellipse of points and fits a line through the principal axis of it. The slope of this line indicates the wear rate and may be compared to other slopes, with a high slope indicative of a high rate of wear [Scott, 1979]. To test for precision of measurement, the dentition of ten specimens was measured twice. Forty-six different measurements were compared in a paired sample t-test. The correlation coefficient was 0.99 and P-values were nonsignificant (P40.05). RESULTS The results of an intergeneric comparison of the quantity of dental wear are presented in Table III and are depicted in Figure 2. Unpaired t-tests (df 5 160–198) compared permanent and deciduous dentition of all Gorilla and Pan samples. Adult gorillas have significantly (Po0.05) greater attrition on their M1, M3, and on their first incisors compared to adult chimpanzees. In juveniles, gorillas have Dental Wear in African Apes / 485 significantly greater amounts of wear on m1 and m2, but significantly less wear than chimpanzees on i1. The mean amount of wear (percent of exposed dentin) and the standard deviation for each tooth by species is presented in Table IV. The highest percentiles are found in the upper first incisor: Pan paniscus exhibits the greatest mean quantity of wear on this tooth (67.2%), followed by Gorilla g. gorilla (66.7%), and G. g. graueri (61.7%). The wear on the mandibular incisors is greatest in western lowland gorillas (G. g. gorilla) while eastern lowland gorillas (G. g. graueri) have the greatest wear on the first molars. Dental wear of mountain gorillas (G. b. beringei) is very low, even lower than any Pan measurement (Fig. 3). All standard deviations in this table are very high, as there is much variation in mean quantity of wear. It is age-dependent and not very informative. The mean percent perimeter, which is the length of the dentin–enamel junctions divided by the perimeter of the whole tooth, is given for each species as well. This number is an average across the maxillary molars M1 to M3. Eastern lowland gorillas have the maximum perimeter length for M1–M3 followed by Pan t. schweinfurthii. The polynomial regression revealed a significant (Po0.0001) relationship between the perimeter and the mean percent wear across the molars (R2 5 0.799). In the regression plot (Fig. 4), the optimum is positioned at 50% wear. Only 4% (N 5 23) of G. b. beringei, 15% (N 5 47) of G. g. gorilla, 21% (N 5 31) of G. g. graueri, and 13% (N 5 50) of Pan have supra-optimal perimeters, meaning that the vast majority of individuals have less than an optimal quantity of dentin–enamel junctions (Fig. 4). TABLE III. Results of a Gorilla-Pan Comparison by Student’s t-Tests of the Quantity of Wear on the Mandibular Permanent Molars (M) and Incisors (I) and the Deciduous Molars (m) and Incisors (i) Tooth I1 I2 M1 M2 M3 i1 i2 M1 M2 Gorilla X7SD Pan X7SD P-value of t-test 49.7730.5 35.1728.4 33.3724.9 20.5720.1 13.7720.6 15.573.1 21.474.5 61.5719.8 81.6720.8 37.2726.1 33.1724.4 25.8723.9 15.7720.3 8.2712.9 19.974.1 22.774.1 29.473.7 45.577.8 o0.01 0.64 o0.05 0.11 o0.05 o0.05 0.51 o0.001 o0.0001 P-values are two-tailed. Values are percent wear on a tooth relative to the occlusal surface. Fig. 2. Comparison of the percent dentin exposure on the occlusal surface of mandibular permanent incisors (I) and molars (M) and deciduous incisors (i) and molars (m) in Pan and Gorilla. TABLE IV. Means and Standard Deviations of Degree of Wear, by Tooth and by Species Tooth Species N M3 X7SD M3 X7 SD M2 X7 SD M2 X7 SD M1 X7 SD M1 X7 SD G. b. beringei G. g. gorilla G. g. graueri Pan paniscus P. t. schweinfurthii P. t. troglodytes 29 68 35 15 9 52 1.373.0 11.8717.9 12.4718.6 7.279.1 14.3712.9 6.1713.4 11.7725.6 16.8721.9 17.6723.8 5.675.8 15.6717.5 7.3712.4 7.3711.2 25.6725.8 27.7726.4 11.5715.0 28.1728.4 13.6720.4 8.0714.7 24.2721.4 24.9722.4 12.3714.1 31.7728.6 14.6720.2 22.1724.5 38.2726.4 48.1732.1 28.7724.2 36.7727.8 25.1723.5 14.3718.9 37.6725.8 37.9725.6 21.9718.9 31.1728.3 25.1724.9 Tooth Species G. b. beringei G. g. gorilla G. g. graueri Pan paniscus P. t. schweinfurthii P. t. troglodytes I X7SD I2 X7SD I X7SD I1 X7SD Mean % perimeter, M1 M37SD 21.6721.8 46.9732.3 37.6735.1 58.2734.6 46.7737.4 40.7731.0 17.2721.2 40.5730.9 34.0729.8 35.4722.0 32.7726.5 31.7724.3 30.2728.8 66.7732.8 61.7730.6 67.2727.5 53.3737.5 51.6728.5 32.5732.7 52.9730.7 46.8729.2 47.8724.6 35.3728.5 32.6724.8 11.4713.5 25.6722.9 29.0723.8 17.0716.1 26.6721.4 14.8718.2 2 1 Values are percents. Mean percent of perimeter is the average perimeter of the dentin lakes from M1–M3. Bold indicates highest value for each tooth. Am. J. Primatol. 486 / Elgart Fig. 3. Means of percent attrition on occlusal surface of mandibular molars (M) and incisors (I) for all species measured. Fig. 4. Plot of the polynomial regression of the second order for all individuals. The x-axis is the mean percent wear on the maxillary molars M1–M3, and the y-axis is the length of the dentin-enamel junctions (perimeter). The regression equation and R2 is given below the graph. An ANOVA: F 5 6.1, df 5 91, P 5 0.003 examined the differences in the quantity of wear within the Gorilla genus (Table V). Significant differences (Po0.05) were found between G. b. beringei and G. g. gorilla, and often between G. b. beringei and G. g. graueri. In each of these cases, G. b. beringei has the least amount of wear, G. g. gorilla has the greatest amount of wear on the incisors, and G. g. graueri the greatest amount on the molars. Another ANOVA: F 5 4.7, df 5 2, P 5 0.02 demonstrates that this pattern is already present in the juveniles in the second deciduous molar. In both ANOVAs, the variation within a group is larger than the variation between groups. The mean percent and standard deviation of wear on the maxillary first incisor and molar, incisor to molar ratios, and results of the paired two-tailed ttests (df 5 22–103) are shown in Table VI. All ratios are greater than one because incisal wear is greater than molar wear in each species. Mountain gorillas have the lowest mean ratio (1.4), followed by Gorilla g. graueri (1.6), while all other species have means above 3.0, which means these latter species have approximately twice as much wear on their incisors as on their molars. An ANOVA: F 5 3.03, df 5 5, P 5 0.01 deemed the differences between the eastern gorillas on one hand and the western gorillas and Pan species on the other significant. To examine wear rate, major axis equations from Model II regression of the wear on the maxillary first and second molar were calculated and plotted for each species (Fig. 5). Slopes of each line (Table VII), indicating the wear rate, are similar, and range from 1.1 to 1.49. Ninety-five percent confidence limits were calculated and the only slopes TABLE V. Results of ANOVAs and Student’s t-Tests of Mean Degree of Wear by Gorilla Subspecies and by Upper Tooth Species ANOVA I1 t-tests I2 t-tests M1 t-tests M2 t-tests M3 t-tests m2 Perimeter M1–M3 t-tests G. b. beringei X7SD G. g. gorilla X7SD G. g. graueri X7SD 30.2728.8 G. b. beringei–G. g. gorilla G. b. beringei–G. g. graueri 21.6721.7 G. b. beringei–G. g. gorilla 21.5724.5 G. b. beringei–G. g. gorilla G. b. beringei–G. g. graueri 7.3711.2 G. b. beringei–G. g. gorilla G. b. beringei–G. g. graueri 1.373.0 G. b. beringei–G. g. gorilla G. b. beringei–G. g. graueri 5.5 11.4713.5 G. b. beringei–G. g. gorilla G. b. beringei–G. g. graueri 66.7732.8 61.7730.6 46.9732.3 37.6735.1 38.2726.4 48.1732.1 25.6725.8 27.7726.4 11.8717.9 12.4718.6 12.1 25.6722.9 9.4 29.0723.8 Bold numbers show highest values per tooth. Am. J. Primatol. P value 0.0002 o0.0001 0.002 0.008 0.001 0.002 0.004 0.0009 0.002 0.0006 0.0002 0.020 0.020 0.020 0.060 0.003 0.002 0.0008 Dental Wear in African Apes / 487 TABLE VI. Means and Results of Paired t-Tests on Incisor vs. Molar Wear for Each Species Subspecies N % wear I17SD Gorilla b. beringei Gorilla g. graueri Gorilla g. gorilla Pan paniscus Pan t. troglodytes P. t. schweinfurthii 21 21 66 13 44 5 30.2733.1 62.2728.9 77.1729.5 68.1726.7 52.6730.0 53.2737.4 P value G. b. beringei G. b. beringei G. g. graueri G. g. gorilla Pan paniscus Pan t. troglodytes P.t. schweinfurthii – 0.67 o0.01 0.001 0.04 0.04 % wear M17SD G. g. graueri 0.67 – o0.01 o0.01 o0.001 0.03 26.7726.3 46.3730.1 38.2727.1 28.8724.2 25.3724.4 29.3725.7 G. g. gorilla o0.01 o0.01 – 0.10 0.18 0.62 I1/M1 X 1.4 1.6 3.1 4.4 3.8 3.6 Pan paniscus 0.001 o0.01 0.10 – 0.42 0.62 Pan t. troglodytes 0.04 o0.001 0.18 0.42 – 0.88 Pan t. schwein-furthii 0.04 0.03 0.62 0.62 0.88 – Means, standard deviations, and the mean ratio of maxillary incisal to molar (I1/M1) wear is presented in the upper table. In the lower table, the significance of the test is given as a P-value. Significant P-values are in bold. TABLE VIII. Amount of Tooth Loss and Dental Disease, by Percentage, for Each Species Fig. 5. Comparison of major axis lines for each species. Wear on the second maxillary molar (M2) is contrasted with wear on the first maxillary molar (M1). The equations of the lines are in Table VII. TABLE VII. Equations of the Principal or Major Axis, from Model II Regression Group N Equation of principal axis 95% confidence interval of slope Gorilla b. beringei Gorilla g. graueri Gorilla g. gorilla Pan paniscus Pan t. troglodytes P.t. schweinfurthii 16 28 68 16 52 7 y 5 3.911.29x y 5 9.011.14x y 5 7.711.24x y 5 4.611.49x y 5 6.611.30x y 5 3.911.10x 1.2–1.5 1.0–1.5 1.1–1.4 1.0–2.0 1.2–1.5 0.8–1.1 Sample size, N, and 95% confidence intervals for the slopes are given. that have separate intervals with reasonable certainty are G. g. gorilla and Pan t. schweinfurthii. Pan paniscus has the highest wear rate, while P. t. troglodytes and G. b .beringei have moderately high rates. The lowest wear rates are found in P. t. schweinfurthii and G. g. graueri. These rates are opposite what one would expect from the quantity of Species N Tooth loss (%) Dental disease (%) G. b. beringei G. g. gorilla G. g. graueri Pan paniscus Pan t. troglodytes 29 68 35 15 52 21 26 5 27 24 45 28 8 33 6 wear; however, the regression’s intercept indicates that the amount of wear is highest in eastern lowland gorillas when M2 comes into occlusion and lowest in mountain gorillas. Only two of the rates, that of G. g. gorilla and Pan t. schweinfurthii, are significantly different. Among gorillas, mountain gorillas have the highest rate of wear, followed by western lowland gorillas and eastern lowland gorillas. Table VIII displays the percentage of antemortem tooth loss and dental disease, including abscesses, caries, excess calculus, and root resorption, for each species. Mountain gorillas display the greatest amount of dental disease (45%) due to a high frequency of abscesses and problems associated with excessive calculus deposits, and bonobos the greatest amount of tooth loss (27%). Common chimpanzees have the second highest percent of individuals with tooth loss at 24% and a high incidence of caries. For a similar reason, Western lowland gorillas also have a high incidence of dental disease (28%). Eastern lowland gorillas have lower incidence of missing teeth (5.3%) and dental disease (8%). Pearson correlation coefficients expressing the relationship of wear on individual teeth (M1, M2, etc.) and dental disease for all teeth measured were Am. J. Primatol. 488 / Elgart TABLE IX. Pearson Correlation Coefficients for the Relationship between the Wear on (A) the Maxillary First Molar and Pathological Conditions, and (B) the Maxillary First Incisor and Pathological Conditions in All Individuals and Broken Down by Species Maxillary M1-pathology Group Overall Gorilla b. beringei Gorilla g. graueri Gorilla g. gorilla Pan paniscus Pan t. troglodytes P. t. schweinfurthii N 202 25 35 71 15 50 6 Correlation coefficient 0.19 0.20 0.05 0.34 0.39 0.43 0.81 Maxillary I1-pathology P-value N o0.01 0.370 0.760 0.030 0.157 o0.01 0.051 171 21 25 57 12 50 6 Correlation coefficient 0.133 0.36 0.15 0.33 0.23 0.37 0.64 P-value 0.080 0.111 0.491 0.010 0.487 o0.01 0.192 Sample size and P-values are given. Bold P-values indicate significance at the Po0.05 level. approximately 0.20. All were significant at Po0.05 according to a Fisher’s r to z transformation and a confidence interval calculation except for the correlation between I1 wear and pathology. When the correlation coefficients are examined by species, all are low (under 0.5) with the exception of Pan t. schweinfurthii and many are not significant, with P-values above 0.05 (Table IX). The only significant relationships in which the confidence interval does not include zero are found between the correlations of M1 and I1 wear to the disease indices of Gorilla g. gorilla and Pan t. troglodytes. DISCUSSION Some hypotheses were supported while others were not. As was predicted, adult gorillas have significantly greater amounts of wear on their molars and on their first incisors than adult chimpanzees, and greater wear is found on the posterior teeth. Correlations between dental disease and the amount of dental wear were low, and no significant correlation was found in mountain gorillas, although one was found in western lowland gorillas and common chimpanzees. Contrary to what was predicted, gorillas do not have a higher wear rate nor do they have more teeth with an optimal dento–enamel junction length than chimpanzees, nor do mountain gorillas display the greatest amount of wear among gorillas as was expected with a tougher diet. The greater amount of wear in adult gorillas compared to chimpanzees confirms the results of other studies [Aiello et al., 1991; M’Kirera & Ungar, 2003; Welsch, 1967]. Juvenile gorillas have greater wear than juvenile chimpanzees on their deciduous molars but not on their incisors. Aiello et al.  also found greater attrition in deciduous Gorilla dentition compared to Pan and Pongo, but they did not test this statistically. They attributed this finding to an earlier weaning age: gorillas are reported to eat solid food at one to two months of age [Fossey & Harcourt, 1977], and dentin exposure begins at Am. J. Primatol. about six months [Aiello et al., 1991] while chimpanzees do not eat solid food until about four to six months [Goodall, 1986]. The difference in the amount of wear in adults is presumably due to dietary differences: if gorillas are processing tougher foods, then more power strokes of the mandible are necessary, which translates into more cutting by the ‘‘blades’’ of the dentition. More data are required on the physical properties of gorilla and chimpanzee foods to conclude this definitively. Increasing occlusal dental wear usually has the effect of increasing the occlusal area of a tooth [Pérez-Barberı́a & Gordon, 1998], which would be advantageous to gorillas. Confounding this simple relationship is the fact that due to thin enamel and high cusps, Gorilla has very steep intercuspal angles while Pan has shallow angles [M’Kirera & Ungar, 2003; Spears & Crompton, 1996]. With age, these differences in relief are maintained even with increasing dental attrition [M’Kirera & Ungar, 2003; Ungar & M’Kirera, 2003], indicating that functional morphology is maintained with wear. Mountain gorillas exhibited the least amount of wear among gorillas, which is probably not attributable to their diet because eastern lowland gorillas consume many of the same items [Elgart, 2010], yet exhibit the greatest amount of wear. The reason for low amounts of wear in mountain gorillas remains unclear. It may be due to the ages of the sample, and the fact at least some of them were the victims of poachers, to less ambient dust in their environment, or to an unknown variable. Cousins  concluded that mountain gorilla teeth have less wear than western lowland gorilla teeth because their teeth have accessory cusps, but conversely, Janis and Fortelius  demonstrated that larger teeth will have more rapid wear. No difference was found between the amount of wear in males and females in this study, even though males would have larger teeth. Welsch  reported the opposite of Cousins  and of this study, concluding that G. b. beringei have especially worn teeth, but his sample is unknown, and may now be named G. g. graueri. Dental Wear in African Apes / 489 Bonobos and western gorillas have the highest degree of wear on I1, which is significantly greater than mountain gorillas. This may be due, in part, to the processing of fruit, stems, and bark, which requires utilization of the spatulate first incisor. Kinzey  also found greater incisal wear in P. paniscus compared to P. t. troglodytes, which he attributed it to the eating of fibrous plant matter. The incisal to molar wear comparison confirms the distinction in wear between those species that process more food at the anterior of the mouth compared to the posterior. Pan paniscus, P. t. troglodytes, and G. g. gorilla have about twice as much wear on their incisors as they do on their molars. The western lowland gorilla (G. g. gorilla) eats more fruits than do the eastern gorilla species. Other studies also reported greater anterior wear than posterior wear in African apes [Dean et al., 1992; Kinzey, 1984; Nichols & Zihlman, 2002]. It was expected that Pan as a frugivore would have greater wear on the incisors compared to the more folivorous Gorilla because there is evidence that folivorous primates have more wear on their posterior teeth compared to frugivores [Welsch, 1967], but the results here were inconclusive. Mountain gorillas and eastern lowland gorillas had the lowest ratios, which is expected from the amount of tough vegetation in their diet [Elgart-Berry, 2004]. All species had predominantly suboptimal wear, not supra-optimal, meaning that for most individuals, dentin–enamel junctions were still increasing and had not reached their peak. The lowland gorilla species displayed the greatest average wear across the molars, yet there was only a maximum of 21% individuals with supra-optimal wear. A significant (Po0.05) relationship was found between dental disease and wear overall on each of the incisors and molars except for the first incisor; however, the coefficients are all very low. A significant relationship was found for wear and dental disease in western lowland gorillas and common chimpanzees. Both species had high amounts of tooth loss and incidence of caries. In general, wear is not a good predictor of incidence of dental disease. The wear rates were opposite what one would expect from the comparison of the amount of wear, but can partially be explained by the y-intercept, which indicates the amount of wear on M1 when M2 comes into occlusion [Benfer & Edwards, 1991]. There is approximately 2.7 years between eruptions of M1 and M2 and no difference has been found in eruption times between gorillas and chimpanzees [Aiello & Dean, 1990; Aiello et al., 1991; Shea, 1983] even though gorillas grow faster [Shea, 1983]. Eastern lowland gorillas have the highest wear on M1 at time zero (9.0), while western lowland gorillas are second highest, at 7.7, which explains why the amount of wear is greater in these species. Mountain gorillas have the second lowest amount of wear at time zero and have low amounts overall. The wear rates of all African apes are similar, ranging from 1.1 to 1.49, with bonobos at the high end of the range followed by central chimpanzees and mountain gorillas. The lowest wear rates are found in western chimpanzees and eastern lowland gorillas. For comparison, the wear rate in three human populations ranged from 1.06 to 1.43 (mandible and maxilla, respectively) for Indian Knoll, 0.63 to 0.87 for the Campbell Site, and 1.14 to 1.19 for the Hardin Site [Scott, 1979]. One might attribute a lower rate in the eastern lowland gorillas to the enlarged teeth of this species [Benfer & Edwards, 1991; Elgart-Berry, 2000]; however, because eastern lowland gorillas have a more confined gape than mountain gorillas [Elgart-Berry, 2000; Taylor, 2003], they may process less food per chew, which would lead to a lower wear rate than mountain gorillas. The presumed tougher diet of Pan paniscus compared to the other Pan species may be the cause for the high wear rate in this species, but the rate of P. paniscus has the largest confidence interval as well. McCollum  noted that the bonobo sample at the Royal Museum in Tervuren, which was measured here, suffered extreme periodontis and premature tooth loss. The fact that Pan t. troglodytes and P. t. schweinfurthii, whose diets are similar, do not have more similar wear is additional evidence that something other than diet is a factor. Factors that were not measured here and may be important are the levels of ambient dust and the age at weaning. Abrasives in a diet are an important factor in dental wear [Aiello et al., 1991; Ungar et al., 1995]: the communition of dust and grit accumulations on plants can be equal to the impact of masticating silica in grass. Both have caused the evolution of wearresistant teeth [Janis, 1995]. Mountain gorillas start eating solid food earlier than chimpanzees at Gombe, but weaning ages of each species are not known [Aiello et al., 1991 and references therein]. It is also important to keep in mind that in each individual, wear will be affected by tooth loss, and that the wear rates are calculated from juvenile dentition. It is possible that wear rates of adults would be different. High wear rates were found where there was a high incidence of tooth loss. This sample of Pan paniscus has the greatest amount of tooth loss (27%) along with a high frequency of dental disease (33%), and the highest wear rate. Pan t. troglodytes, with a wear rate second to P. paniscus, has the second highest percent of individuals with tooth loss (24%). Mountain gorillas (G. b. beringei) have a high rate and the highest frequency of dental disease (45%). Western lowland gorillas (G. g. gorilla) have moderate-to-high rates of wear, and display excessive quantities of wear: 29% of M1s had no cutting surfaces remaining. Similar to G .b. beringei and P. paniscus, they have poor dental health (26% tooth loss and 28% dental disease). Eastern lowland gorillas, G. g. graueri, have a low wear rate, and also have fewer incidence of Am. J. Primatol. 490 / Elgart missing teeth (5%) and dental disease (8%) than do the other species, even though they demonstrate the greatest quantity of wear of all species on their first molars. Thirty percent of G. g. graueri molars were worn down to dentin. This study neglects to take into account the wear on the enamel that occurs before dentin is reached, which would be slightly greater in Pan than in Gorilla [Kay, 1981; Kono, 2004; Olejiniczak et al., 2008; Vogel et al., 2008]. It also fails to quantify additional wear once all the dentin has been exposed: the maximum amount of wear is 100% of the dentin in this study. However, quantifying dentin exposure on a digital image is a more objective method than utilizing wear stages. Results of this study agree with McCollum  who also used digital imaging, but not with earlier studies [e.g., Welsch, 1967], who fitted wear into stages. Do gorilla teeth demonstrate current utility and high performance that suggest adaptation to their diet? Evidence in this study that gorilla teeth are durable despite a mechanically demanding diet includes: teeth are not at an optimum in wear, but they have yet to reach the optimum and are not past it. In addition, dental disease cannot be predicted by dental wear in any species, which indicates that excessive wear is not causing mechanical senescence in this sample. On the other hand, gorillas are not characterized by a high wear rate in comparison to chimpanzees, and it was postulated that a certain amount of wear in gorilla teeth would be advantageous to the processing of their diet. Despite their thinner enamel and more mechanically demanding diet, gorilla teeth are as durable as chimpanzee teeth according to the results of this study. 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