AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 98:307-321(1995) Dental Pathology in Pongo satyrus borneensis KATHRYN ELIZABETH STONER Museum of Natural History, Department of Systematics and Ecology, University of Kansas, Lawrence, Kansas 66045-2454 KEY WORDS Dental disease, Horizontal bone loss, Orangutan, Osseous defects, Pongo, Premortem tooth loss ABSTRACT The Selenka orangutan collection obtained from 1892 to 1896 from wild-shot specimens in West Borneo, provides a n excellent opportunity to examine dental pathology in free-ranging primates. Two hundred and twenty-three skulls from this collection were analyzed for dental conditions, including carious lesions, local infections (infra-alveolar and periapical osseous defects), horizontal bone loss, and premortem tooth loss. Specimens were sexed, divided into three broad age groups, and compared to ascertain sexrelated or age-related differences in occurrence of dental pathology. None of the subadults displays any evidence of dental disease. One individual (2%)in the young adult group has a periapical osseous defect and evidence of horizontal bone loss, and another (2%) has two adjacent interproximal carious lesions. The old adults have a much higher prevalence of individuals afflicted with dental pathologies, including 6% carious lesions, 26% local infections, 23% horizontal bone loss, and 3%premortem tooth loss. The differences between the young and old adults in number of individuals afflicted with dental pathologies is statistically significant for local infections and horizontal bone loss. When compared by sex, the old adult group reveals that females have a higher occurrence of dental pathologies than males in all types of lesions recorded and these differences are statistically significant for local infections and horizontal bone loss. Considering the importance diet plays in the development of dental disease, it is suggested that ecological separation of the sexes, with the subsequent dietary differences, could be a n important factor determining the higher prevalence of dental lesions observed in female orangutans. Additionally, the importance of local ecological factors, which may affect dietary patterns, are recognized as a potential source of variation in dental pathologies among different samples of orangutans. 0 1995 Wiley-Liss, Inc. Dental pathologies in non-human primates have been recognized in many species (Arnold and Baram, 1973; Bramblett, 1965, 1967; Cohen, 1960; Colyer, 1936; Hershkovitz, 1970; Jones and Cave, 1960; Kakehashi et al., 1963; Kilgore, 1989; Lovell, 1990a,b; Page and Schroeder, 1982; Page et al., 1975; Rohrer-Ertl et al., 1985; Schultz, 1935,1939; Skinner, 1986; Smith et al., 1977), and some non-human primates have been used in dental disease research (Navia, 1977; Page and 0 1995 WILEY-LISS, INC Schroeder, 1982). A current, comprehensive review of dental pathologies in non-human primates is provided by Lovell (1991). In spite of these data, few studies have associated variation in prevalence of dental pa- Received February 19, 1993; accepted April 13, 1995. Address reprint requests to Dr. Kathryn E. Stoner at her current address: Palo Verde Biological Station, Organization for Tropical Studies, Interlink 341, P.O. Box 02-5635, Miami, FL 33152. 308 K.E. STONER thologies in wild primates with dietary factors. The effect of diet on dental disease has been extensively studied in humans, in both living (Brunelle and Carlos, 1982; Page and Schroeder, 1982; Schluger et al., 1977; Toth, 1970) and prehistoric groups (Alexandersen, 1967; Brabant, 1967; Costa, 1980; Frayer, 1984; Hildebolt et al., 1988; Molnar and Molnar, 1985; Powell, 1985). Many of the studies of human dental disease have attempted to identify dietary patterns that affect the prevalence of dental disease in different groups. In recent years, the important role a high carbohydrate diet plays in the occurrence of oral diseases has been well documented with experimental evidence (Hillson, 1986; Kreitzman, 1976; Newbrun, 1982; Rugg-Gunn, 1983; Sreebny, 1982; Theilade and Birkhead, 1986). Although no clear associations of food types with prevalence of dental disease have been made for free-ranging non-human primates, data collected on dental lesions in primates in the wild have all revealed a general trend of increasing frequency of dental pathologies with older individuals (Bramblett, 1965, 1967; Colyer, 1936; Hershkovitz, 1970; Kakehashi et al., 1963; Kilgore, 1989; Schultz, 1935, 1939). In spite of this agedependent relationship, great variation between and within populations has been observed (Bramblett, 1965, 1967; Lovell 1990a,b; Schultz, 1935). Some of the variation in frequency of dental disease within populations has been attributed to differences between the sexes. For example, differences in the occurrence of dental disease affecting male and female baboons (Papio cynocephalus) have been documented (Bramblett, 1965,1967). Older male baboons frequently (29%) have severe alveolar destruction which is often associated with decayed or damaged teeth. Alternatively, female baboons rarely (5%) show signs of periodontal disease. In contrast to baboons, male and female gorillas (GorilZu gorilla) have approximately the same frequency of periodontal disease (Kakehashi et al., 1963). No studies have focused on sexual variation of dental disease in orangutans, but field studies have revealed much about orangutans diets in the wild that may, in turn, prove useful in interpreting the prevalence of dental pathology in these primates. Orangutans can be characterized a s primarily frugivorous, but there is substantial diversity in orangutan diets which, in addition to fruit, include flowers, leaves, buds, bark, and insects (Galdikas, 1978, 1979, 1988; MacKinnon, 1974; Rodman, 1977, 1988). Ecological differences between the sexes have been reported by Galdikas (1978), who found t h a t adult males range farther per day and occupy a larger area throughout their lives than do females. This behavior relates to males spending much more time on the ground, consequently eating less bark and young leaves, but more termites and other foods found predominantly on the ground. Conflicting results have been reported from other areas (Rodman, 1977, 1988); a s a result, it is unclear whether this variation in resource use is a reflection of idiosyncratic habits of some males, regional differences, andlor sampling techniques. The purpose of this paper is to describe dental pathologies in a sample of orangutans and to determine whether there are significant differences between the sexes in the frequency and severity of dental pathologies. In addition, the previously established pattern that, within species, older individuals have more dental pathologies than younger ones is tested. Finally, qualitative comparisons are made of these results with previous reports on dental lesions in orangutans (Lovell, 1990b; Schultz, 1935) and other apes (Kilgore, 1989; Lovell, 1990a; Schultz, 1935). MATERIALS AND METHODS Study sample The Selenka sample was obtained during 1892-1896 from wild-shot orangutans (Pongo satyrus borneensis) from Skalua, West Borneo. This collection represents one of the largest series of orangutans preserved in museums and is currently housed a t the Anthropologisches Staatssammlung, Munich. A summary of the material in this sample and a brief history of the collection is given by Rohrer-Ertl(l984).A historical review of the problems surrounding the nomenclature of the orangutan and the proper designation of the species satyrus (synonymous with pygnaeus), a s well as evidence 309 DENTAL PATHOLOGY IN PONGO TABLE 1. Number of individuals with dental pathologies in the Selenka sample of Pongo satyrus borneensis from Skalua, West Borneo, stratified by age class and sex Carious lesions M F M F Local infections M F M F Subadultl Young adult 35 36 0 0 0 0 0 0 0 0 22 33 0 1 0 1 0 1 0 0 Old adult 32 62 1 5 4 1 21 0 3 N 20 Horizontal bone loss M F Premortem tooth loss ' Three unsexed subadults are not included for the recognition of the subspecies borneensis is also provided by Rohrer-Ertl (1983, 1988). Two hundred and twenty-three skulls from the Selenka orangutan collection were examined for dental pathologies. The subadult sample included 35 males, 36 females, and 3 unidentified sex. The young adult sample consisted of 22 males and 33 females and the old adult group contained 32 males and 62 females (Table 1). The orangutans were sexed based on the distinctively large canines characteristic of males (Mahler, 1973; Swindler, 19761, as well as cranial morphology. The development of the sagittal crest is consistently more pronounced in adult males than females. Some discrepancies between my observations and sex identifications recorded directly on the specimens were resolved by Rohrer-Ertl (personal communication). The sample was divided into three broad age groups based on dental eruption and degree of occlusal wear. Similar to most other primates, orangutan molar wear occurs primarily on the lingual cusps in the upper jaw and the buccal cusps in the lower. However, according to Welsch (1967), orangutans seldom show dentine bridges between the lingual and buccal cusps, in contrast to humans (Smith, 1984) and gorillas (Welsch, 1967). With these unusual patterns of attrition in mind, the following aging criteria were developed. Subadults consisted of all individuals in which the permanent dentition was not completely erupted. Young adults were recognized as having a complete permanent dentition with no more than small areas of dentine exposure on the lingual cusps of the Fig. 1. Maxillary occlusal view of a young adult female with little wear on the lingual cusps of M1, characteristic of the young adult age class. A periapical osseous defect surrounds the left P3. Also note the crowding in the maxilla. Missing teeth were considered lost postmortem (specimen 251). first upper molar (Fig. 1). Old adults included individuals that had enough wear on the first upper molar to create two large areas of dentine exposure on the lingual cusps, which were frequently connected; if separated, it was only by a very narrow enamel bridge (Fig. 2). Recognizing dental pathologies Dental pathologies were categorized a s (1) caries, (2) local infections (infra-alveolar osseous defects and periapical osseous defects), (3) horizontal bone loss, or (4)premortem tooth loss. Standards for recognizing the 310 K.E. STONER Fig. 2. Maxillary occlusal view Of an old adult female with the right showing much wear On the lingual cusps, which have been worn down and are connected through dentine exposure. The left M1 shows large dentine exposures on both lingual cusps, but they are still separated by a small enamel bridge. Also note the periapical osseous defect associated with the left M1 lingual root (specimen 185). ~ i 3, ~occlusa1 , view of a young adult female with a large occlusal cavity on the right maxillary M2 (specimen 114). presence and seventy of pathological states in these orangutans were based on previous methodology applied to humans (Alexandersen, 1967; Brothwell, 1963; Koritzer, 1977; Molnar and Molnar, 1985). Caries. Carious lesions were recorded by position on the affected tooth and were categorized into occlusal, interproximal, or root caries types (Molnar and Molnar, 1985). The presence of occlusal caries was initially determined by macroscopic inspection followed by further inspection with a hand lens and probe. Carious lesions were recorded only when the crown surface had collapsed and a cavity was formed that could be probed (Fig. 3). This is the sixth phase of development of enamel caries and represents a late stage in the disease (Hillson, 1986); earlier stages of enamel caries are difficult to detect macroscopically (Howat et al., 1981). Interproximal caries, limited to the enamel surface, were recognized in a similar fashion to occlusal caries (Figs. 4,5). I t was sometimes difficult to evaluate the presence of interproximal lesions due to the close in- Fig. 4. Occlusal view of interproximal caries affecting maxillary right and left central incisors of an old adult female (specimen 101). terproximal articulations between the teeth that allow little space for probing to ascertain the status of the coronal wall on the interproximal surface. Therefore, interproximal caries may have been underestimated in this study. Severity of interproximal and occlusal caries was recorded using a 1 4 scale developed by Koritzer (1977), who considered 1a small pit or fissure lesion; 2 a moderate pit, fissure, or smooth surface lesion; 3 any lesion that DENTAL PATHOLOGY IN PONGO Fig. 5 . Occhsal view of an old adult female with a small interproximal cavity on the mesial surface of 311 Fig. 7. Left lateral view of a n old adult male maxilla with several periapical osseous defects and horizontal bone loss. A large periapical defect is located at the root tip of the left canine which is connected to another osseous defect associated with the third premolar. Two more osseous defects are located around the first molar, one on the mesial buccal root and another on the distal buccal root (specimen 238), maxillary left P4. The buccal roots of left M1 were lost premortem and this area has been resorbed. The left I1 and P3 were considered lost postmortem due to the lack of remodeling in the tooth sockets (specimen 84). Fig. 8. Left lateral view of a young adult female maxilla with horizontal bone loss and periapical osseous defects above P4 and the distal buccal root of M2 (specimen 251). Fig. 6. Mandibular lingual view of cemental root caries affecting the distal root of right M1 and the mesial root of right M2 in an old adult female (specimen 243). endangers the pulp; and 4 exposure of the dental pulp. Root caries were recognized as dark, invaginated lesions surrounding one or more root surfaces of a tooth. When present, these occurred near the cemento-enamel junction and proceeded apically for varying distances (Fig. 6). Although two types of root caries have been observed in human skeletal sam- ples including cemental type and cervical type (Molnar and Molnar, 19851, only the cemental type was identified in this sample. Local infections. Local infections included periapical osseous defects and infra-alveolar osseous defects. Periapical defects were recognized as discrete areas of bone resorption surrounding root tips. These usually had regular borders and were approximately round or oval in shape with a variable depth (Figs. 1, 7, 8). Infra-alveolar defects occasionally were found interproximally, but 312 K.E. STONER Fig. 9. Right lateral view of mandible from old adult female with an infra-alveolar osseous defect surrounding M1 and M2 and horizontal bone loss in the entire mandible (specimen 181). Fig. 10. Left lateral view of maxilla and mandible from an old adult female with horizontal bone loss in the upper and lower jaw (specimen 201). were primarily located on the lingual and buccal borders of the alveolar margin between the cemento-enamel junction and the apex of the root. These defects had regular borders similar to periapical defects, but instead of being completely round or oval, the resorbed area was usually semilunar in shape with the open side directed toward the alveolar border (Fig. 9). When one defect encompassed the area between two teeth it was considered associated with the more mesial tooth to avoid counting the defect twice. Areas of bone fenestrations and dehiscences were not considered pathological (Hall e t al., 1967; Page and Schroeder, 1982).No attempt was made to measure the depth of the defects due to time constraints. The present study focused on the molar teeth in the maxilla and mandible and conservatively recognized only condition 4 a s evidence for horizontal bone loss. When horizontal bone loss was present under the molars it usually continued around the entire margin of the mandible or maxilla, therefore, recording horizontal bone loss in the molar region appeared to be representative of the entire maxilla or mandible (Figs. 7, 9, 10). Given time constraints, it was not possible to analyze each individual tooth €or the presence of periodontal pockets or irregular porous surfaces for direct evidence of periodontitis. Premortem tooth loss. Premortem tooth loss was identified by examining the alveolus for each missing tooth to determine that involves a n even lowering of the alveo- whether it was lost postmortem from hanlar margin has been described a s horizontal dling andfor the preparation processes or bone loss (Hillson, 1986; Karn et al., 1984). was lost during the life of the individual. In this study horizontal bone loss was scored As a first step, each vacant tooth socket was a s present or absent based on a modified examined to see if any bone remodeling had version of procedures described by Alexan- occurred (Ortner and Putschar, 1981). If the dersen (1967) and Koritzer (1977). These re- margins were sharp with no evidence of bone searchers measured horizontal bone loss be- in-filling, it was considered to be lost posttween the cemento-enamel junction and the mortem (Fig. 1).If the alveolus was partially alveolar margin and designated four discrete filled with bone and the socket walls were categories. The categories ranged from remodeled so that the sharpness of the “bone-loss not exceeding 2 millimeters” in socket contour was lost or the socket was category 1, to category 4, which included filled completely with bone, the tooth was “bone-loss of approximately half the root considered to be lost premortem (Fig. 11)or length or exposure of any molar root furca- congenitally absent. When present, the teeth tion” (Koritzer, 1977). surrounding a completely closed alveolus Horizontal bone loss. Alveolar resorption 313 DENTAL PATHOLOGY IN PONGO RESULTS Fig. 11. Occlusal view of maxilla from old adult female with extensive premortem tooth loss. Teeth lost premortem with resorption of the socket include right M2, M1, P4, P3, I1 and left M3, M2, M1, and P4 (specimen 92). were examined for interproximal wear facets to rule out the possibility of congenital absence. Missing teeth due to congenital absence, a s well as teeth that had been broken premortem but still retained the root or roots, were not included in the category of premortem tooth loss. Comparisons To test for sexual dimorphism of dental pathologies, the number of males and females affected by each category of dental pathology in the old adult group were compared with a Fisher exact test (Sokal and Rohlf, 1981). I n addition, a Fisher exact test was used to compare the young adult and old adult samples to determine if the proportion of individuals amicted with dental pathologies varied significantly with age. Finally, teeth afflicted by carious lesions, local infections, and premortem tooth loss, were described within the old adult group to recognize any patterns of teeth affected by pathologies. No statistical comparisons were made between teeth amicted with various dental lesions because of the problem of assuming independence of teeth. Caries Within the old adult group, a slightly higher proportion of females (8%) are affected by carious lesions than males (3%) (Table l ) , but this difference is not statistically significant (Fisher P = 0.63). In the subadult age group no individuals have carious lesions, while one individual (2%) in the young adult group, and six (6%) in the old adult group have at least one carious lesion (Table 1). The difference between the old and young adults is not statistically significant (Fisher P = 0.38). Given the low occurrence of caries found in the Selenka sample, it is difficult to observe any regularity in teeth affected by carious lesions a t the level of individual teeth (Table 2); nevertheless, some possible patterns are discernible when the teeth are combined into anterior (canines and incisors) and posterior (premolars and molars) tooth classes or separated as to their location in the maxilla as opposed to the mandible (Table 3). The trends suggested include (1)in females, carious lesions are more common in the posterior and maxillary teeth than in the anterior and mandibular teeth, and (2) in males, caries are only found in the anterior maxillary teeth. The most common types of caries observed in this sample are interproximal and root caries, each accounting for 40% of the total carious lesions observed, followed by occlusal caries, which account for the remaining 20% (Table 4). The severity of enamel caries is most commonly category 2 (Koritzer, 1977), which is defined a s a moderate-sized fissure or surface lesion (Figs. 4,5).One category 3 occlusal cavity destroyed a large part of the occlusal surface and appears to be approaching the pulp cavity (Fig. 3). Additionally, one category 4 lesion penetrated the entire occlusal surface, pulp cavity, and root (Fig. 12). More than half (57%) of the individuals aMicted with caries have more than one such lesion, with a n average of two cavities per individual (Table 4). I t is also apparent that adjacent teeth are frequently involved in carious lesions. The most extreme example of this is found in specimen 243, which has root 314 K.E. STONER TABLE 2. Dental lesions in the old adult orangutans by dental element and sex (females n Maxilla Females No. of teeth Carious lesions Local infections Premortem tooth loss = 62; males n = 32) I1 I2 C P3 P4 M1 M2 M3 108 2 0 1 112 0 3 0 110 0 3 114 2 116 2 4 2 118 2 8 3 120 116 2 2 1 1 61 62 0 3 0 62 0 1 0 62 0 0 0 120 0 0 5 1 0 Males No. of teeth Carious lesions Local infections Premortem tooth loss Mandible Females No. of teeth Carious lesions Local infections Premortem tooth loss 54 2 3 0 58 0 0 0 54 0 109 0 2 0 114 0 5 0 Males No. of teeth Carious lesions Local infections Premortem tooth loss 58 0 4 0 58 0 62 0 3 0 1 0 0 0 0 109 0 4 1 121 0 4 0 120 0 1 0 121 120 1 1 7 0 0 0 55 0 2 60 0 60 0 2 60 0 60 0 0 2 60 0 0 0 0 0 0 0 0 1 0 1 0 1 0 TABLE 3. Dental pathologies according to anterior or posterior categories and upper or lower jaws stratified by sex (only old adults) Pathology Female Carious lesions Local infections Horizontal bone loss Premortem tooth loss Male Canous lesions Local infections Horizontal hone loss Premortem tooth loss Anterior Posterior Maxillary Mandibular 2 17 9 32 2 10 9 26 14 10 2 23 16 2 2 11 0 11 0 0 2 11 1 0 0 11 1 0 caries on the maxillary right P3 and P4 (not pictured) and the mandibular right M 1 and M2 (Fig. 6). With the exception of root caries, carious lesions are not associated with periapical or infra-alveolar osseous defects. Local infections There is a statistically significant difference (Fisher P = 0.05) in the frequency of individuals with local infections between the old adult females (32%)and males (13%) (Table 1). In addition, the proportion of individuals afflicted with local infections is significantly different (Fisher P = 0.00004) between the young and old adult groups. None of the subadults and only one (2%) of the young adults (Figs. 1,8)have local infec- tions, while 24 (26%) of the old adults have infra-alveolar or periapical osseous defects (Table 1). Local infections were also recorded by affected tooth in order to discern any patterns of areas in which osseous defects occur (Table 2), although, again, patterns are hard to discern. When the teeth affected were grouped into anterior versus posterior and maxillary versus mandibular (Table 3) the following patterns emerged: (1) posterior teeth are more often affected (65%)than anterior (35%) in females, while in males they are equally affected (50% each); and (2) maxillary and mandibular teeth are involved approximately the same in females (53% DENTAL PATHOLOGY IN PONGO 315 dence of this pathology (Table l).When compared to the young adults, the old adult group h a s a significantly (Fisher P = 0.001) higher proportion of individuals with horizontal bone loss. None of the subadults, and only one (2%) of the young adults (Fig, 8) have horizontal bone loss; however, 22 (23%) of the individuals in the old adult group have horizontal bone loss (Table 1). Premortem tooth loss There are no significant differences in the frequency of individuals with premortem tooth loss between males and females (Fisher P = 0.51). No instances of premortem tooth loss are found in the males and only three females (5%)have lost teeth premortem (Table 1).Similarly, there are no significant differences between the young and Fig. 12. Lingual view of t h e right side of t h e maxilla old adult groups in the frequency of premorfrom a n old adult female with a n extensive carious lesion tem tooth loss (Fisher P = 0.90). Premortem on M2, which penetrates t h e occlusal surface and continues into the lingual roots of M1 and M 2 (specimen 999). tooth loss does not occur in the subadult or young adult groups and is relatively rare (3%) in individuals in the old adult sample (Table 1). TABLE 4. Caries type, severity, and tooth affected The most extreme case of premortem tooth per indiuidual’ loss of the three old adult females is found Specimen Tooth 5Pe Severity in specimen 92 (Fig. 11). A total of 10 teeth LP‘ Interproximal 84 2 were lost premortem, including maxillary LPA 101 Interproximal 2 right 11, P3, P4, M1, M2 and left P4, M1, 101 RI’ Interproximal 2 LI’ Interproximal 101 2 M2, M3, and mandibular right M3. The other 114 RM2 0cc1usa 1 3 two cases of premortem tooth loss affected LM1 176 Occlusal 2 RI’ 242 single teeth. Specimen 84 has lost the two Interproximal 2 242 LI’ Interproximal 2 buccal roots of the upper left M1 premortem Root 243 RPj and the area has been resorbed (Fig. 5). The Root RP‘ 243 Root 243 last example of premortem tooth loss is RMI Root 243 RM2 found in specimen 223, which has lost the RM’ 999 Occlusal and root 4 Root lower left canine with subsequent complete 999 RM’ ’ Specimen 114, young adult female; specimen 242, old adult male; resorption in the area (not pictured). When specimens 84, 101, 176, 243, 999, old adult females. all dental elements were considered by location, the teeth most often affected by premortem loss in the old adult females are the and 47% respectively), a s well as in males posterior maxillary teeth (Tables 2, 3). (50% each). DISCUSSION Horizontal bone loss General trends that can be identified reA statistically significant difference garding dental pathologies in the Selenka (Fisher P = 0.003) between the sexes is orangutan sample include the following. found in the frequency of individuals with First, sex differences occur in the proportion horizontal bone loss. Thirty-four percent of of individuals affected by dental pathologies, the old adult females have horizontal bone the females showing a higher prevalence in loss, while only 3% of the males have evi- all types of dental lesions recorded. This sex 316 K.E. STONER difference is statistically significant for horizontal bone loss and local infections. Second, the occurrence of dental pathologies in subadults and young adults is extremely rare, but increases markedly with old age. This increase is statistically significant for local infections and horizontal bone loss. Third, individuals aMicted with local infections or horizontal bone loss are much more common than those with carious lesions or premortem tooth loss. Fourth, maxillary teeth may be more often affected by carious lesions and premortem tooth loss than mandibular teeth. Local infections and alveolar resorption occur in the upper and lower jaw with approximately the same frequency. Fifth, caries, local infections, and premortem tooth loss may aMict the postcanine teeth more than the anterior teeth. Although these results reveal some sex-related and age-related differences in dental pathologies in orangutans, the ultimate causes of this observed variability are difficult to discern given the complex etiology of oral disease (Navia, 1977). Causes of dental disease Dental disease is a multifactorial problem with many possible variables affecting its development and expression. Caries. Dental caries is a consequence of the fermentation of carbohydrates by oral bacteria (Rugg-Gunn, 1983). The process of fermentation produces organic acids as a byproduct that lowers the pH in the dental plaque and causes demineralization of the enamel, dentine, and cementum resulting in the development of caries (Hillson, 1986). Several factors contribute to the development of caries, but the most important is the consumption of fermentable carbohydrates (Kreitzman, 1976; Newbrun, 1982; RuggGunn, 1983; Sreebny, 1982; Theilade and Birkhead, 1986). penetrating the pulp cavity, severe attrition, or a traumatic fracture of the coronal surface of the tooth (Hillson, 1986). Infra-alveolar osseous defects are most often due to a periodontal infection (Costa, 1980; Karn et al., 1984) but occasionally result from trauma to the area (Hillson, 1986). Horizontal bone loss. In addition to creating local infections which cause infra-alveolar osseous defects, periodontitis is one of the primary causes of horizontal bone loss (Hillson, 1986).Although there is little doubt that bacteria in dental plaque are the underlying cause of periodontitis (Page and Schroeder, 1982; Schluger et al., 19771, the etiology of this disease is multifaceted and many factors influence its development. Soft carbohydrate-rich foods cling to teeth and dental plaque, thus enhancing the supply of nutrients for bacteria (Hillson, 1986; Schluger et al., 1977). Other factors correlated with periodontitis include crowding of teeth and malocclusion, (Hillson, 1986; Schluger et al., 19771, root caries (Newbrun et al., 1984) and pregnancy (Hillson, 1986). Finally, the influence of heredity on the development of periodontitis has not clearly been established, but is believed to be an important variable (Schluger et al., 1977). Horizontal bone loss has also been attributed to extensive chewing forces produced by mastication. Watson (1986) argues that alveolar recession in humans should be considered indicative of age-related phenomenon associated with heavy masticating and not necessarily a result of periodontal disease. However, a study of howler monkeys by Hall et al. (1967)found no association between extensive tooth wear and alveolar resorption. In addition, a study of gorillas and humans came to the conclusion that there is no significant relationship between occlusal wear and horizontal bone loss (Baer et al., 1963). Local infections. Local infections may result from various disease processes. Periapical abscesses and ultimately periapical osseous defects can occur when the pulp chamber is exposed and infected with bacteria from the mouth which migrate down the root canal to the apex of the root. Exposure of the pulp canal can result from a carious lesion Premortem tooth loss. Premortem tooth loss can also result from a variety of dental diseases that are very difficult to separate (e.g., advanced caries, severe attrition, and periodontal infections) (Hillson, 1986). The most likely cause of premortem tooth loss is the cumulative effect of these variables DENTAL PATHOLOGY IN PONGO 317 (Koritzer, 1968). Advanced attrition or a seAge differences vere cavity may allow the pulp chamber to The significantly higher proportion of old become infected, resulting in a periapical ab- adults afflicted with local infections and scess and bone loss surrounding the root tip. horizontal bone loss, compared to young However, according to Koritzer (19681, most adults, as well a s the higher (but insignifiperiodontal disease results in bone loss sur- cant) number with carious lesions and prerounding the sides of the teeth, not apically. mortem tooth loss is not unexpected. ObserKoritzer (1968) argues that i t is the combina- vations in various primate species have tion of these processes that loosens the tooth revealed that the occurrence and severity of enough to be lost from the socket. In a sample dental pathologies increases in older individof Egyptian human skeletal material which uals (Bramblett, 1965, 1967; Colyer,, 1936; had a very low caries rate, Koritzer (1968) Hershkovitz, 1970; Kakehashi et al., 1963; noted that premortem tooth loss occurred Kilgore, 1989; Lovell, 1990a, 1990b; Schultz, when both advanced attrition and periodon- 1935, 1939). In the Selenka sample there are two extal disease (measured by presence of calculus deposits) were present. Premortem tooth ceptions to this phenomenon of increasing loss was rarely observed when only one of dental pathologies with age. One young adult female (specimen 25 1)exhibits alveothese pathological conditions was present. lar bone resorption and one periapical abWith these inherent difficulties of identiscess above the left upper P3 (Figs. 1,8).This fying and interpreting dental lesions in may be a result of the crowding apparent in mind, some possible explanations for the rethe maxilla. The other exception to the agesults of the dental pathologies observed in related development of dental disease in this the Selenka orangutan collection are presample is a young adult female with a large sented below. occlusal cavity on the upper left M2 (Fig. 3). This condition could be due to any combination of factors affecting the development of Sex differences in old adults dental caries mentioned above or simply to The higher frequency of dental pathologies idiosyncratic variation. in females than males may result from the exploitation of different microhabitats and Sample differences subsequent dietary differences in terms of Comparisons of the old adults in the Selthe proportion of types of foods eaten. At the Kutai Nature Reserve, East Borneo, Rod- enka orangutan collection with observations man (1977, 1988) noted that males eat less of dental pathologies in other orangutan fruit and more bark than females. Although samples show that there is variability in Galdikas (1978, 1979, 1988) did not observe prevalence of dental pathologies among the this same pattern at the Tanjung Puting Re- available data. Although I recognize the difserve, Central Borneo, she did note that ficulties of comparing dental pathology data males spend more time using a variety of collected from various investigators (Alexandersen, 19671, I would like to summarize the ground resources that females do not regudifferences and discuss some factors that larly exploit. Due to the significant effect a may be responsible for these differences. The soft carbohydrate-rich diet has on the devel- frequency of individuals afflicted with caries opment of periodontal disease (Hillson, in different orangutan samples was 2% of 1986; Schluger et al., 19771, a higher con- all individuals (N = 255) (Colyer, 1936),29% sumption of fruit by the females might affect of old adults (N = 45) (Schultz, 1935), and the development of caries and periodontitis 20% of old adults (N = 15) in a sample of and the subsequent horizontal bone loss and Bornean orangutans (Lovell, 1990b).No carlocal infections. Similarly, a less varied diet ious lesions were found in the young adults in terms offood items eaten might contribute or juveniles (N = 11) in Lovell’s sample, to the processes affecting the development while 6% of the young individuals from the of dental disease. Schultz sample had caries. 318 K.E. STONER Schultz recorded osseous defects (abscesses) in 62% of old adults and 26% of young adults while Lovell recorded the frequency of individuals with osseous defects in her total sample as 26% (N = 27); 71% of the osseous defects were in old adults, and 29% were found in young adults. Using a comparable technique to the one used here, Lovell found that 15% of her total orangutan sample had a similar level of horizontal bone loss to that observed in the Selenka collection (Lovell’s scale, moderate or severe). All individuals that had horizontal bone loss in her sample were old adults. Premortem tooth loss was observed in only one individual from Lovell’s Bornean sample. Compared to the old adults in the Selenka collection, Lovell, in a considerably smaller sample, found a much higher proportion of individuals with carious lesions. The frequencies of premortem tooth loss, local infections, and horizontal bone loss were more similar between the Selenka and Lovell samples, but Lovell found a much higher frequency of osseous defects in young adults and juveniles. The old adults in the Selenka sample have a much lower proportion (6%)of individuals affected by carious lesions than those (29%) reported for old adults by Schultz (1935). Similarly, a lower proportion of old adults in the Selenka sample are affected by local infections (26%) when compared to the Schultz sample (62%). This is difficult to interpret for various reasons. First, although Schultz divided his sample into young and old adults, no division was made between the sexes. Because the Selenka orangutans show sex differences in the frequency of dental pathologies, it is possible that unequal sex distributions in the two samples may account for the intergroup differences. Second, exact locality information for the Schultz sample is not provided. Orangutan specimens from both Borneo and Sumatra were included in the analysis by Schultz (1935) without separating individuals collected from different areas. Thus, the Schultz sample appears to be drawn from a wider and perhaps ecologically more diverse area. Surely, some of the variation in dental pathologies among these samples is due to dif- ferences in the ages and possibly proportion of sexes within each sample, a s well a s various criteria for recognizing dental lesions. However, the considerable variation in the prevalence of dental pathologies among different orangutan samples may also relate to the varying ecological conditions from which the samples were drawn. One important factor could be ecological constraints that lead to dietary differences among various areas. Rodman (1988) stated that “despite a superficial appearance of uniformity of the southeast Asian forest, there is considerable variation between locations and within smaller areas.” Although orangutans are characterized by frugivory, much variation has been found in the time spent utilizing different food resources (Galdikas, 1978, 1979, 1988; MacKinnon, 1974; Rodman, 1977, 1988). Local dietary habits in wild orangutan populations have been noted by Galdikas (19781, who found that the greatest difference between the Tanjung Puting Reserve and other areas of orangutan studies was the absence of large fig trees in this region. Yet, figs comprise a major portion of orangutan diets a t many other locations (Galdikas, 1978). Exploitation of different types of foods in different areas might account for the variation observed in the occurrence of dental lesions between the Selenka and Schultz samples. For example, the ingestion of trace elements (Hildebolt e t al., 1988; Leverett, 1982; Ludwig and Bibby, 1969) or particularly sticky fruits (figs) are known to affect the development of caries in humans (Theilade and Birkhead, 1986). They may well influence the onset of dental disease in orangutans from different populations. Unfortunately, the precise location of where these samples came from is not available, so it is impossible to test this ecological hypothesis. Differences between primates Finally, comparisons of the prevalence of dental pathologies observed in this sample of orangutans to the frequency of individuals with dental lesions in some other apes, indicate that orangutans have a slightly higher occurrence of caries (6%)than gorillas, which range from 1%to 3% (Lovell, 1990a; Schultz, 1935), but lower than observations of chim- DENTAL PATHOLOGY IN PONGO panzees, which range from 6% to 15% (Kil gore, 1989; Lovell, 1990a; Schultz, 1935; Schuman and Sognnaes, 1956).Ahigh occurrence of infra-alveolar or periapical osseous defects (26%)and severe horizontal bone loss (23%) is evident in the old adults in the Selenka sample, which parallels results from studies of gorillas and chimpanzees (Kilgore, 1989; Lovell, 1990a; Schultz, 1935). Premortem tooth loss is somewhat rare in the Selenka orangutans (3%),unlike observations on chimpanzees and gorillas (Kilgore, 1989; Lovell, 1990a, 1990b; Schultz, 1935), in which premortem tooth loss is much higher. In sum, compared to gorillas and chimpanzees, orangutans may have a relatively intermediate level of caries, a rare frequency of premortem tooth loss, and a n approximately comparable amount of osseous defects and horizontal bone loss. ~ CONCLUSIONS This study demonstrates significant sexual differences in frequency of dental pathologies in orangutans. It is suggested that these differences may be related to dietary differences resulting from ecological separation of the sexes and exploitation of different resources. In addition, this study supports earlier observations which have documented a n increase in dental pathologies with age in wild primates. Finally, I suggest that differences in expression of dental disease between the Selenka orangutan sample and other samples of orangutans are likely a result of local ecological differences that, in turn, affect patterns of food consumption and subsequent dental disease. Due to the absence of specific dietary components for all samples it is impossible to explicitly test this hypothesis with the current available data. Additional long-term studies of foraging in wild orangutans documenting differences between the sexes and differences between populations will help identify some of the dietary factors affecting oral pathologies in these animals. Furthermore, it would be useful to collect foraging data and dental disease data from populations of orangutans from known localities, for direct comparison of the occurrence of oral disease with regional ecological factors. 319 ACKNOWLEDGMENTS I would like to thank P. 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