An evolutionary framework for assessing illness and injury in nonhuman primates.код для вставкиСкачать
YEARBOOK OF PHYSICAL ANTHROPOLOGY 34~117-155(1991) An Evolutionary Framework for Assessing Illness and Injury in Nonhuman Primates NANCY C . LOVELL Department of Anthropology, University of Alberta, Edmonton, Alberta, Canada T6G 2H4. KEY WORDS ductive success Paleopathology, Skeletal biology, Natural selection, Repro- ABSTRACT It is well established that primates suffer and may survive illness and injury in the wild, but more equivocal is our understanding of how these affect reproductive fitness. This paper presents a functional and evolutionary framework for assessing nonhuman primate illness and injury by examining their timing in primate life history and their associations to subsistence, locomotion, and social behavior. The selective impact of illness and injury may take several forms, by affecting reproductive success through subadult mortality, mortality during reproductive years, restriction of a female’s ability to care for her offspring, and impairment of male and female competition for mates. Analysis may be made at the individual, local populational, or phylogenetic level. The available data indicate that there is considerable variability in the reproductive impact of illness and injury, and that the time of their occurrence in the life cycle is crucial. Broad distinctions in dietary strategies, locomotion, and social behaviors among primates are shown to be of limited use in interpreting evolutionary effects, and the observed variability in pathological profiles at the phylogenetic level suggests that smaller scale distinctions should be employed in future analyses. In addition, methodological inconsistencies seriously hamper these comparative studies. With the steady increase in information on health and mortality patterns emerging from long-term field studies, integrated research efforts in ethology and osteology should permit us to go beyond this theoretical framework and demonstrate empirically the role of illness and injury in primate evolution. One cannot but feel certain that disease in its various manifestations has played a much greater part in the evolution of different forms of life in this world than the biologists have ever realised. JCM Given (1928:166) It can hardly be doubted that this great variety of pathological conditions, found among apes and monkeys of today, is not a sudden, new development, but existed a t all stages of primate evolution with only detailed and no principal change. In the early history of mankind diseases and injuries must also have played important roles. AH Schultz (1956:984) 0 1991 Wiley-Liss, Inc. 118 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 34, 1991 Descriptive narratives about medical curiosities and anomalies in the skeleton and dentition of nonhuman primates have been reported regularly in the literature since the late 1800s (e.g., Bolau, 1877; Ranke, 1899; Rollet, 1891; Sutton, 18841, and systematic reviews of pathological conditions appeared more than 50 years ago (e.g., Moodie, 1923; Colyer, 1936; Schultz, 1935). Only very recently, however, has problem-oriented research been attempted, although earlier identification of related pathological conditions in humans and nonhuman primates and the exploration of behavioral links to patterns of injury and illness are seen in the works of Adolph Schultz. Schultz was the founder of systematic research into skeletal and dental diseases of nonhuman primates and the only authority in this field for several decades. The 1960s and 1970s saw little interest in comparative primate osteopathology, with only a few papers appearing in the physical anthropological literature (e.g., Bramblett, 1967; Buikstra, 1975). Recent work, however, which aims to elucidate more clearly the interrelationships between way of life and health status in nonhuman primates, indicates that this area of study presents promising avenues for research (e.g., DeRousseau, 1985a,b, 1988; Kilgore, 1989; Jurmain, 1989; Lovell, 1990a,b; Morbeck et al., 1991; Sumner et al., 1989; Zihlman et al., 1990). Traditionally, the examinations of relatively large skeletal series have attempted to identify differences in pathological profiles between taxa, and it is only recently that studies focusing on illness and injury in local populations have appeared (e.g., Jurmain, 1989; Kilgore, 1989; Zihlman et al., 1990). The nonhuman primate literature has always contained valuable information on illness and injury in local populations, but this information has been buried in broader discussions of demography, for example, and is usually mentioned only peripherally, in the context of mortality. Thus, populational frequencies of pathological conditions or causes of death have rarely been reported. Now is the time for studies to focus explicitly on illness and injury in nonhuman primates-the data are there, from a number of long-term field studies, and it remains now for these data to be integrated with the existing and forthcoming data from skeletal and dental series. The significance of this research is that a comparative approach to illness and injury in nonhuman primates can provide important information on selective pressures in primate evolution, through the study of the associations of illness and injury to subsistence, locomotion, and social behavior and their timing during primate life history. While skeletal lesions may be used to infer clinical processes affecting the origin and development of disease, they also provide a n insight to adaptive mechanisms that have influenced primate evolution. A particular advantage of free-ranging nonhuman primates for research into the evolutionary significance of illness and injury is that they exhibit manifestations of illness and injury that are not buffered by intervention. Thus, long- and short-term biological adaptations to illness and injury, and the significance of these stressors as selective factors, may be more easily evaluated in nonhuman primates than in humans. The selective impact of illness and injury may take several forms, since the reproductive success of injured and ill animals may diminish even if they do not die of their afflictions, both directly, when physically incapable of reproductive behavior, and indirectly, such as when rank is lost a s a consequence of ill health. Illness and injury, then, may have significant selective impact by affecting reproductive success through subadult mortality, mortality during reproductive years, restriction of a female’s ability to care for her offspring, and impairment of male and female competition for mates. Assessment of the environmental and social associations of illness and injury and their impact on reproductive success can be made a t three levels: individual, local populational, and phylogenetic. An important paper by Zihlman and colleagues (1990) identified individual variation in nutritional, injury, and disease experience among seven Gombe chimpanzees, and the impact of these on survival and reproduction. Since natural selection operates at the level of the individual, a n understanding of the causes of variation in survival and reproductive success is Love111 ILLNESS A N D INJURY IN NONHUMAN PRIMATES 119 essential for the interpretation of processes in primate evolution. Injury and disease were shown in that study, for example, to have permanent effects in adulthood, t o affect future mating opportunities and the survival of offspring, and to have little impact on reproductive success, all in different individuals within the same local population. The recognition of environments, behaviors, or events that affect local populations is therefore important for identifying selective pressures, and the recognition of the timing of these pressures is important for identifying individual variation in their impact. Life history approaches t o primate evolution are relatively new, and an excellent compendium has recently appeared (DeRousseau, 1990). Life history approaches, which emphasize individual variation, complement traditional approaches, which emphasize normative data, and when integrated these provide considerable breadth and depth to the assessment of the evolutionary significance of illness and injury. At the phylogenetic level, patterns or central tendencies in pathological profiles are examined with the objective being the explanation of these patterns in terms of evolutionary processes, and the identification of the direction of genetic change over time. Broad distinctions in patterns may be related to variation in social structure and behavior and dietary and other environmental adaptations. This paper uses a functional and evolutionary framework to review current knowledge of primate skeletal and dental pathology, describes approaches to such study and their limitations, and identifies areas in which further research is needed. For two reasons, skeletal and primatological field study evidence for illness and injury in free-ranging animals is emphasized, rather than the biomedical literature that relies almost exclusively on captive animals. First, the theoretical perspective in this paper is evolutionary, because the role of illness and injury as selective factors in primate evolution are of ultimate concern. Thus, experimental inoculations, for example, while often of great benefit in medical and pharmacological research, have less relevance to the question of the impact of injury and illness on reproductive success in a natural setting (although the assumption that modern primate populations and settings represent naturalistic ones is not necessarily a good one, as will be discussed later in this paper). Second, practical considerations prevent the review of the vast biomedical literature. A comprehensive review of the skeletal manifestations of infectious diseases in controlled settings may serve as a powerful aid to the understanding of disease processes and the interpretation of pathological lesions observed in dry bone specimens, but this is beyond the scope of this paper. PATHOLOGICAL CONDITIONS OF THE TEETH Pathological lesions Pathological conditions described here are caries, abscesses, periodontal disease, antemortem tooth loss, enamel wear, and enamel hypoplasia, and their frequencies are summarized in Table 1. All but the last represent localized oral pathology and have significance for evaluating an animal’s ability to maintain the dental structures necessary to consume enough food to ensure survival. As will be discussed in later sections of this paper, populational patterns of these lesions may be interpreted as reflecting responses to environmental stressors or behavioral characteristics with an impact on nutritional health and consequently fertility as well as survival. Aberrations may reflect a group’s unusual diet or habitual use of teeth as tools, and may also be interpreted in the context of an individual animal’s life history. Enamel hypoplasia is believed to be a retrospective indicator of stress during the subadult years, reflecting periodic episodes of anomalous enamel development triggered by one or more systemic disease states, and can thus be interpreted in both an individual and populational sense. Table 1 provides frequencies of these conditions in various taxa, as obtained from the literature. The following sections provide a critical analysis of these data. Erythrocebus Macaca Cercopithecus Cercopithecidae Cercoceb us Hylobatidae Hylobates Pongo Gorilla Pongidae Pan 99 277 112 318 1473 1533 42 39 185 588 365 439 623 10 12 37 78 110 123 465 22 75 119 245 292 689 28 66 194 225 Sample size 6 2 0 - 4 - 0 1 7 10 1 3 2 11 12 5 2 1 0 <1 - 0 3 15 5 - % % 10 8 14 6 Abscesses Caries % Periodontal disease % AMTL - - - 17 moderate - - 8 76 moderate - 11 - 58 - - moderate - - moderate -1 50 severe 96 Enamel hypoplasia - Enamel wear TABLE 1 . Dental disease in nonhuman primates . I - - 2 ~~ ~ Colver. 1947 Colyer, 1936 Schultz, 1935, 1956 Colyer, 1947 Colyer, 1936 Colyer, 1936 Colver. 1936 Sch”uman and Sognnaes, 1956 Schultz, 1935, 1956 Colyer, 1936 Colyer, 1936, 1947 Schultz, 1956 Schultz. 1944 Kilgore, 1989 Jones and Cave, 1960 Lovell, 1990b Schuman and Sognnaes, 1956 Skinner, 1986 Schultz, 1935 Colyer, 1936, 1947 Lovell, 1990a Lovell. 1990b Skinner, 1986 Schultz, 1935 Kakehashi et al., 1963 Colyer, 1936, 1947 Lovell, 1990b Schultz, 1935 Selenka, 1898 Colyer, 1936, 1947 Source 137 255 781 64 131 186 122 69 84 538 82 148 47 54 100 222 86 682 59 1205 67 272 311 36 74 288 21 1 1 17 15 4 - - 9 8 7 - 1 - - - 6 - 10 8 - 2 - - <1 <1 15 26 25 173 - 3 - 34 11 9 8 - - lo2 - - a3 - 273 33 10 3 - 3 3 11 - 7 2 4 3 10 - 2 5 7 - 15 - - 12 0 - 14 - 15 2 <1 <1 <1 8 - 0 <1 0 - 0 - 0 4 - - - - - 2 - - - - - - 2 - - - Smith et al., 1977 Schultz, 1960 Colyer, 1936 Smith et al., 1977 Schultz, 1960 Colyer, 1936 Colyer, 1936 Schultz, 1960 Smith et al., 1977 Colyer, 1936 Colyer, 1936 Colyer, 1936 Schultz, 1935 Schultz, 1956 Colyer, 1936 Hershkovitz, 1970 Schultz, 1956 Hershkovitz, 1970 Schultz, 1935, 1956 Colyer, 1936 Schultz, 1935, 1956 Schultz, 1956 Colyer, 1936 Colyer, 1936 Schultz, 1935, 1956 Colyer, 1936 Colyer, 1936 'A dash indicates that data are not reported for this sample 'These frequencies are for caries, abscesses, periodontal disease, and AMTL combined. Separate frequencies for each category cannot be determined from the available data. 3These frequencies are for alveolar destruction that may be attributed to either abscessing or periodontal disease. Lagothrix Pithecia Saimiri Callicebus Cebus Ateles Cebidae Alouatta Callitrichidae CaZlithrix Saguinus Nasalis Presbytis Theropithecus Colobidae Colobus Mandrillus Papio 122 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 34, 1991 Caries. Among the apes, carious lesions appear to be more prevalent in chimpanzees and orangutans, but considerable variability is reported within taxa, with frequencies ranging from 5% to 15%in chimpanzees and from 2% to 12% in orangutans. The lack of consistency for chimpanzees, however, may be due to a higher proportion of young animals, who exhibit few or no carious lesions, in some samples (e.g., Colyer, 1936; Schuman and Sognnaes, 1956), to small sample sizes (e.g., Jones and Cave, 1960), or to confounding factors such as extreme tooth wear andlor loss in aged animals (Kilgore, 1989). In addition, although approximal carious lesions have been observed in chimpanzees (Fig. 1)and orangutans (Lovell, 1990b1, approximal lesions on incisor crowns could not be positively identified as carious in the Gombe chimpanzees (Kilgore, 19891, and this may artificially lower the observed frequency of caries for these animals. The frequency of lesions in orangutans also ranges widely for different samples, and both variable sample sizes and the inclusion of subadults in one or more samples could be factors. The results for gorillas are more consistent. Lesions are rare: the highest frequency is 3% (Lovell, 1990b), and frequencies of 1% or less were obtained for several large samples (Colyer, 1936, 1947; Kakehashi et al., 1963; Schultz, 1935). Low caries frequencies were also noted in gibbons (Colyer, 1936, 1947; Schultz, 1944, 1956). Old World monkeys have consistently low frequencies of caries, with none exceeding 10% and seven of the ten genera having frequencies of 1% or less. Among platyrrhines, howler monkeys have a very low frequency of caries involvement, with <1% of animals affected (Colyer, 1936; Schultz, 1960; Smith et al., 19771, as do woolly monkeys and sakis (Colyer, 1936). Capuchins have a high frequency, 15-26% (Schultz, 1960; Smith e t al., 19771, but frequencies for other New World species are variable. The age distribution of these samples may be a factor in these discrepancies, however, since subsamples of aged animals were shown to have the highest caries frequencies (Schultz, 1960) but ages are not reported by all workers. Similarly, a low percentage of diseased teeth may be due to a n unreported number of juveniles and subadults in the sample. Hershkovitz 119701, for example, found that the frequency of oral disease in subadult tamarins and marmosets was almost nil. Most authors note that carious lesions appear mainly on approximal surfaces of anterior teeth in chimpanzees, gorillas, and New World monkeys (Colyer, 1936, 1947; Hershkovitz, 1970; Lovell, 1990b; Schultz, 19351, but there is no discernable pattern in orangutans (Lovell, 1990b) and carious lesions in gibbons are found mainly on molars (Schultz, 1944). The one lesion in the Gombe sample t h a t was identified as carious is located on a mandibular molar (Kilgore, 1989). Similarly, a spider monkey displays lesions on molars and capuchins a r e affected mainly on the upper and lower first molars (Smith et al., 1977). A carious lesion and subsequent abscess was observed a t the left lower first molar in a senile male Japanese monkey (Tasumi, 1969). Extreme anterior tooth wear and loss, such as noted in the Gombe sample, should be considered factors that possibly bias the location data in some studies. Abscesses Abscesses are common sequels to carious invasion of a tooth’s pulp cavity; however, the frequencies of periapical and interdontal abscesses are variable and do not necessarily mimic those of caries. The percentage of chimpanzees, gorillas, and orangutans with abscesses are extremely variable (Colyer, 1936, 1947; Jones and Cave, 1960; Kilgore, 1989; Lovell, 1900a,b; Schultz, 1935, 1941), but the highest figures may be due to small sample sizes and/or to the preponderance of aged animals in samples, since age has been shown to be a n important factor in the accumulation of abscesses (e.g., Kilgore, 1989). A possible complication of oral abscesses, maxillary sinus infection, was found in three of 35 adult chimpanzees, one of 118 gibbons, six of 38 gorillas, and in one orangutan (Schultz, 1939, 1956). Fig. 1. Interproximal carious lesions of the maxillary and mandibular anterior teeth in a female chimpanzee. Note also the carious lesion in the maxillary left canine, which appears to be secondary to breakage of the tooth and exposure of the pulp cavity. (Reprinted by permission of the Smithsonian Institution Press from Patterns of Injury and Illness in Great Apes: A Skeletal Analysis, by Nancy C. Lovell. 0 Smithsonian Institution 1990. Fig. 5, p. 196.) Fig. 2. Calculus and alveolar resorption in the mandible of a male mountain gorilla. (Reprinted by permission of the Smithsonian Institution Press from Patterns of Injury and Illness in Great Apes: A Skeletal Analysis, by Nancy C. Lovell. 0 Smithsonian Institution 1990. Fig. 7, p. 202.) 124 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 34, 1991 A study of fleshed howler monkey skulls revealed the presence of abscesses, with food or hair debris often impacted in the soft tissue (Hall et al., 1967). Howler monkeys have the highest frequency of abscesses among New World monkeys, with a s much as 33% of a sample affected, while tamarins and squirrel monkeys have comparatively low frequencies at <lo% (Schultz, 1935, 1956, 1960; Smith et al., 1977). Frequencies for spider monkeys are very inconsistent (Schultz, 1960; Smith et al., 1977). Old World monkeys tend to have lower frequencies of abscesses than do New World monkeys. In great apes, periapical abscesses are found five times more often anteriorly than posteriorly, while interdontal abscesses are found more frequently in association with the posterior teeth (Lovell, 1990b). A striking expression of interproximal craters, associated with extensive calculus deposits, was observed in mountain gorillas (Fig. 2). Seventy-nine abscesses are present interdontally in that sample, affecting 11 animals (50%), with a mean number of lesions of 3.6 per animal (Lovell, 1990a).Catarrhines displayed abscessing in no discernable pattern (Schultz, 19441, but the available evidence indicates that abscesses in platyrrhines are located mainly in the anterior teeth (Schultz, 1935, 1960; Smith et al., 1977), except among marmosets and tamarins, in which abscesses were located three times a s often posteriorly (Hershkovitz, 1970). Periodontal disease Periodontal disease in humans generally involves a n inflammatory response to a n irritant such as plaque and calculus (mineralized plaque) on tooth surfaces in the region of the gum attachment. It is evaluated on the basis of crestal alveolar bone loss, and its expression is quite variable, although high, in the great apes. Kilgore (1989) observed that a shelf-like appearance of the alveolar crest is present in all Gombe chimpanzees in whom teeth are present, and severe alveolar bone loss was noted in eight of those ten animals. Periodontitis was expressed in 76% of a large sample of lowland gorillas according to Kakehashi and colleagues (1963), but included a s evidence were fenestrations as well as horizontal bone loss, furcation, and interproximal craters. Fenestrations are no longer considered to be a consequence of periodontitis (Page and Schroeder, 1982), and the possibility exists that some or all of the interproximal craters may result from progression of a n apical infection and should be classes as abscesses. Fenestrations make up the largest proportion of the recorded lesions, and if those and interproximal craters were discounted the proportion of affected animals may more closely approximate frequencies reported elsewhere. The interdontal abscesses in mountain gorillas, which were associated with extensive calculus deposits, are of uncertain etiology without benefit of radiographs but were originally attributed to periodontal disease (Lovell, 1990a). Antemortem tooth loss Antemortem tooth loss (AMTL) is usually caused by infectious destruction of the bone that anchors the tooth in place. The infection is most commonly caused by exposure of the pulp cavity, through caries, tooth breakage, or severe enamel wear. The lowest frequencies of AMTL, usually <lo%, are found in orangutans (Lovell, 1990b; Schultz, 1935), gibbons (Schultz, 19441, and many Old World and New World monkeys (Schultz, 1935, 1956, 1960; Smith et al., 1977). The highest frequencies of AMTL appear in chimpanzees and gorillas, although the figures vary by study. An explanation for some of this variability may be found in methodological differences: Schultz’s data are based on completely closed alveoli while other authors also include partially resorbed tooth sockets, thus, higher frequencies can be expected from other investigators. This does not explain all of the variation, however, nor do differences in sample size or frequencies of potential precursors to tooth loss, caries and abscesses. The age distribution of these samples may be a factor, however. Multiple tooth loss is common in animals of advanced age: three of the Gombe chimps lost nine or more teeth (Kilgore, 1989). Among 12 adult Lovell] ILLNESS AND INJURY IN NONHUMAN PRIMATES 125 chimpanzees from Sierra Leone, two aged animals lost six teeth each (Jones and Cave, 1960). One older male chimpanzee had lost a total of 18 teeth (Fig. 3), while the maximum number of teeth lost in a gorilla was 11 (Lovell, 1990b). An aged Japanese monkey of the Takasakiyama group lost six teeth (Tasumi, 1969). Enamel wear When chimpanzees exhibit extreme tooth wear it appears mainly on the anterior teeth (Kilgore, 1989; LaVelle, 1975; Lovell, 1990b) and may result from food preparation activities, such as leaf stripping. Wear appears to be the most important factor contributing to abscess formation and tooth loss in the Gombe chimpanzees, and is most severe with advanced age (Kilgore, 1989). Similarly, tooth wear was the primary cause of tooth destruction and loss among yellow baboons (Bramblett, 1967) and a common disorder among some New World monkeys involves heavy occlusal wear on the canines, eventually exposing pulp canals and leading to infection and possibly tooth loss (Smith e t al., 1977). Otherwise, extreme wear of teeth was not observed in platyrrhines except in spider monkeys (Schultz, 19351, and was observed with less frequency among catarrhines as compared to apes. In contrast to severe wear on anterior teeth in chimpanzees and New World monkeys, gorillas exhibit more extreme wear on the posterior teeth, possibly due to the heavy grinding stresses associated with their folivorous diet (Lovell, 1990b). Enamel hypoplasia The available data on enamel defects are extremely variable. Enamel hypoplasia was found to be fairly common and much more severe in the great apes compared to cercopithecoids, with >95% of African apes exhibiting some incisal enamel defect and with orangutans displaying a similar pattern of frequency and severity (Vitzthum and Wikander, 1988). Colyer (1936) found grooves and depressions to be limited mainly to anterior teeth, especially the canines, and enamel defects were most common in orangutans, but only 17% of the sample was affected. A comparison of hypoplasia frequencies in gorillas and chimpanzees reported considerably higher frequencies of 76% and 58% respectively, with this intrastudy difference being statistically significant (Skinner, 1986). In another study, six of 12 adult chimpanzees exhibit linear enamel hypoplasia (Jones and Cave, 1960). Microscopic examination of the teeth of the three great apes indicated that many incisors and canines, particularly in the upper jaw, exhibit transverse labial grooves, but no gross hypoplastic lesions were observed in orangutans or gorillas (Schuman and Sognnaes, 1956). Summary of findings in oral pathology Gorillas and gibbons consistently show the lowest frequencies of carious lesions among the apes, while lesions are generally more common in platyrrhines than in catarrhines. Abscesses are more prevalent in the African apes and New World monkeys than in Old World monkeys, and mountain gorillas display considerable alveolar destruction in the form of interdontal abscesses. There are some inconsistencies in the data, however. Severe wear and multiple antemortem tooth loss are prevalent in aged chimpanzees from Gombe (Kilgore, 1989) but are not so in those mountain gorillas for whom age data also exist and who can be said to be comparably advanced in years (Lovell, 1990a). In addition, howler monkeys have low caries frequencies but high abscess frequencies, although a positive correlation between the two types of lesions is expected. The inconsistency may rest with the data collection: a n abscess is usually identifiable in the jaw even if the tooth is not present, while a carious tooth would not be scored if i t was lost antemortem. Since AMTL was not recorded for these animals this cannot be verified. Among both Old and New World monkeys, AMTL affects mainly the anterior teeth (Schultz 1935, Smith et al., 1977), but no significant difference in the frequency of AMTL in posterior versus anterior teeth was observed in a sample of Love111 ILLNESS AND INJURY IN NONHUMAN PRIMATES 127 marmosets and tamarins (Hershkovitz, 1970). Patterns of AMTL do not correspond directly to the relative frequencies of caries and abscess nor to the progress of tooth wear. As is apparent, given the variability in sample characteristics and methodology, a n attempt to determine the statistical significance of differences in pathological frequencies among genera would be quite impractical. The following sections, however, attempt to interpret broad distinctions in pathological experience in terms of environmental and social factors. Dental disease and diet Table 2 summarizes the principal dietary adaptations and dental pathological profiles of the primates for which data are not available. In the human paleopathological literature a n increased caries prevalence is associated with a diet high in sugar and highly processed carbohydrate foods, which stick to the tooth surface and provide a food source for cariogenic bacteria in the mouth. While it may be predicted that greater frequencies of carious lesions will be found in those primates who are relatively more frugivorous compared to the folivorous animals, the results do not support this prediction. Although folivorous animals do consistently have low frequencies of caries, the reverse is not true. This is not completely unexpected, since the sugar contents of fruits will vary widely according to factors such a s local environmental conditions and ripeness, and the pulp will not adhere to tooth surfaces in the same manner as do the highly processed carbohydrates usually indicted in human dental disease. In general, variable caries frequencies are associated with varied omnivorous and vegetarian diets. It has been suggested that diet cannot be entirely responsible for differences in caries frequencies among platyrrhines since they subsist on the same diet in the same jungle (Schultz, 19561, but this is simplistic. The geographic distribution and habitats of these animals vary considerably, and sympatric species occupy different econiches and exploit different food resources (Napier and Napier, 1967; Wolfheim, 1983). The predominant diet of primate groups within a genus or species varies according to the geographic range of the animals in their natural habitats a s well as the seasonality of available foodstuffs (Jones, 1972). In addition, idiosyncratic characteristics of a n environment may produce aberrant dental lesions, such as the accelerated enamel wear in howler monkeys living on a volcanic island, where foliage was frequently covered in abrasive volcanic dust (Smith et al., 1977). Thus, any attempt to correlate dental lesions with diet requires that these variables be examined for local populations, rather than genera or species, since intrageneric or -species variability in dietary adaptations tends to obscure categorizations of dietary specializations. More specific dietary data for local populations and improved data collection may permit these associations to be more rigorously examined, but since more primates eat a wide variety of food it is likely that only the most divergent diets can be confidently compared in terms of their associated dental pathology. Certainly the data presented in Table 2 indicate that no clear picture can be discerned regarding the relationship of dental lesions to diet at this level of analysis. A confounding factor in the relationship of dental disease to diet is that assumptions of a natural diet may be inappropriate. Careful assessment of the study sample is necessary before this assumption can be made, since a number of local populations have been provisioned or have had access to human trash heaps, which they raid for food (Jones and Cave, 1960; Merfield, cited in Colyer, 1936:674). Fig. 3. Extensive antemortem loss of the anterior teeth in a male chimpanzee. Fig. 4. Healed oblique fractures of the right ulna and radius in a female gorilla, with myositis ossificans. low - low low low medium - medium low low low low low low low low low low low low low medium low medium low high low low medium - - - - - - low low low medium - high - low medium low low high high - - - - - - - medium3 low low - - - - - - - - - low - low -2 - high high medium Enamel hypoplasia severe severe medium low low low medium - - low - low - medium high high low AMTL low low low - low medium low high high high high high medium Abscesses medium low medium Caries Enamel wear vegetarian vegetarian omnivorous omnivorous omnivorous frugivorous omnivorous omnivorous omnivorous folivorous folivorous vegetarian vegetarian vegetarian omnivorous omnivorous omnivorous omnivorous graminivorous frugivorous vegetarian frugivorous Principal dietary adaptation vegetarian '- 'Relative levels of expression for each pathological condition are taken from data presented In Table 1. Principal dietary adaptations are derived from Jones (1972) and Napier and Napier (1967); vegetarian refers to diets composed primarily of leaves, stems, shoots, bark, and fruits; frugivorous refers to diets in which fruits predominate; omnivorous refers to diets that include vegetation as well as insects and some meat; graminivorous refers to diets that emphasize grasses; folivorous refers to diets based on leaves. indicates that data are not reported for this pathological condition 'This frequency is for caries, abscesses, periodontal disease, and AMTL combined in the study by Hershkovitz (1970). Pongidae Pan Gorilla Pongo Hylobatidae Hylobates Cercopithecidae Cercocebus Cercopithecus Erythroce bus Macaca Mandrillus Papio Theropithecus Colobidae Colobus Nasalis Presbytis Callitrichidae Callithrix Saguinus Cebidae Alouatta Ateles Callicebus Cebus Lagothrix Pithecia Saimiri Periodontal disease TABLE 2. Dental disease and diet' Love111 ILLNESS A N D INJURY IN NONHUMAN PRIMATES 129 Recent evaluations of periodontal disease in free-ranging baboon populations in Ethiopia and Kenya indicate that animals that feed largely on garbage may have higher periodontal disease scores than do animals that are primarily wild-feeding (Phillips-Conroy et al., 1991). A baboon troop that fed regularly on trash from an army camp displayed no carious lesions but did exhibit abscesses and other gum infection as well as many broken teeth (Strum, 1987). Finally, variation in tooth macro- and microstructures may be responsible for variation, or lack thereof, in patterns of dental lesions. For example, although orangutans have thicker molar enamel than do chimpanzees and gorillas, and capuchins have comparatively thick enamel relative to other New World monkeys, these differences in enamel thickness are not associated with differences in caries frequencies or degree of enamel wear in the data reviewed here. Future studies must consider explicitly the morphology of teeth and enamel characteristics when comparing the nature, frequency, and location of lesions. Primates whose dietary specialization includes hard nuts or seeds have extremely thick enamel for withstanding high chewing forces, while folivores have thinner enamel but sharp shearing crests, and frugivores tend to have rounded molar cusps for crushing, rather than cutting, food. Thus, in addition to dietary components, these characteristics may influence the susceptibility of a tooth to carious destruction. Dental microwear studies are providing useful information on the interpretation of diet and are a valuable complement to macroscopic evaluation of dental lesions (for a review of primate microwear studies, see Teaford, 1988). Dental disease and systemic stress Although enamel hypoplasia is thought to reflect physiological insult during the time of tooth formation and is widely discussed in the human paleopathological literature (for a recent review, see Goodman and Rose, 1990), there has been limited research on enamel hypoplasia in free-ranging primates. Only two studies have systematically evaluated stress as a factor in the expression of enamel defects. Molnar and Ward (1975) noted that free-ranging apes have fewer enamel hypoplastic defects than do captive animals, which may reflect inadequate diet and/or psychosocial stress in the latter group. Among free-ranging animals, regularity of hypoplastic grooving in chimpanzees and gorillas may be linked to stress associated with their habitat’s twice-yearly rainy season (Skinner, 1986). Comprehensive studies of the relationship of enamel defects t o health and wellbeing during the developmental years are now possible, however, given that longitudinal data are now available for many animals that have been followed in long-term field studies. Macro- and microscopic examination of the teeth upon the death of the animals or a program of dental casting would provide the necessary data. Although patterns of dental maturation are not yet well understood (see, e.g., Mann et al., 1990))the identification of the frequency and timing of physiological perturbations, such as seasonal environmental stress and birth trauma, in the teeth of ancestral and modern primates and early hominids may provide clues to growth rates and hence to the processes of primate evolution (e.g., Skinner, 1986). Dental disease and aggression Trauma as a predisposing factor to oral pathology must be considered specifically in future studies, since carious infection and subsequent abscess and eventual tooth loss may be due to tooth breakage rather than diet. A senile male Japanese monkey broke upper canines, exposing the pulp cavities to infection and subsequent abscess (Tasumi, 19691,and although upper central incisors were found to be the most frequently abscessed teeth in New World monkeys (Schultz, 1935, 1960; Smith et al., 1977), the canines of males were more commonly affected when sex differences were considered, usually secondary to tooth breakage (Schultz, 1960). Thus the frequencies of caries, abscesses, and AMTL may not always correlate with aspects of diet. Data collection should in future include the etiology of lesions in individual animals, so that the ultimate cause of AMTL can be ascertained. This 130 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 34, 1991 may differ for individuals as well as local populations and species, and sex differences in the etiology of AMTL could be recognized. Since AMTL has implications for nutritional health, longevity, and reproductive success (see below), then a distinction between dietary and social behavioral causes is of interest. Trauma to the teeth may also affect their development and impair mastication. A subadult gorilla displayed a malformed left central incisor, possibly resulting from cranial trauma that arrested the tooth's growth (Colyer, 1936). A chimpanzee with a n irregular mass of dental tissue between the left orbit and anterior nares, resembling a n ill-formed canine tooth, was thought to be the victim of a n injury that drove the developing tooth upward (Colyer, 1936). Alternatively, this may be a case of ectopia, a genetic condition where the tooth erupts in a region remote from its normal position. Most cases in humans involve the maxillary canines, which may appear in the nasal cavity or in the orbit and its vicinity (Pindborg, 1970). Dental disease, longevity, and reproductive success Tooth wear and the antemortem loss of teeth have implications for longevity and reproductive success in nonhuman primates. For example, older male baboons and chimpanzees undergo extensive tooth loss and are unable to chew effectively (Bramblett, 1967; Zihlman et al., 19901, thus limiting their nutritional intake. Animals of advanced age may not survive if antemortem tooth loss or wear is severe enough to prevent them from eating adequately. Since female nonhuman primates are capable of reproducing a t advanced ages, this may have a n impact on the number of live births, and the death or ill health of females may influence the survival of their immature offspring. The synergistic relationship of malnutrition and infectious disease also indicates that animals with severe dental disease who are malnourished are also a t risk of further deterioration and death from infection. Alternatively, even while not causing death, malnutrition could be sufficient to affect female fecundity and male spermatogenesis. Important to the interpretation of tooth wear, AMTL, and longevity is a n assessment of the masticatory requirements of free-ranging animals, and assumptions about the dietary habits of animals represented in collections must be critiqued. For example, some chimpanzees have become closely located to human habitation because of encroaching agriculture, and are therefore eating cultivated crops and raiding trash heaps. While this may result in poorer oral health for the animals, it has the advantage of providing abundant and easily masticated food, which may have made possible the increased longevity of animals in which teeth have become lost or inefficient. Animals with impaired dental function may be unable to sustain life on strictly natural diets, and their survival to advanced ages depends, therefore, upon the food provided by native gardens and farmlands (Jones and Cave, 1960). A postmortem examination of a female baboon of the Pumphouse Gang showed that her teeth would not have been adequate for chewing food after a few more years (Strum, 1987). The Gombe chimpanzees and Darajani baboons exhibit extreme tooth wear and antemortem loss and may have been provisioned sufficiently with easily masticated food to ensure their survival to a n age past that obtainable under natural conditions. A comparison of mortality in wild chimpanzees a t Gombe and captive zoo chimpanzees found that survivorship in older (>27 years) animals was better in zoos than in the wild (Courtenay and Santow, 1989). While the difference was attributed to the more sheltered zoo environment and veterinary care, the feeding of easily chewable and digestible foods to older animals may also have been a factor. PATHOLOGICAL CONDITIONS OF THE SKELETON Pathological lesions A variety of pathological conditions of the skeleton have been observed in nonhuman primates, including trauma, infection, and arthritis, and their frequencies are summarized in Table 3. Trauma and infectious disease have implications for mortality as well as for loss of rank and, therefore, reproductive success during a n Lovell] ILLNESS A N D INJURY IN NONHUMAN PRIMATES TABLE 3 . Pathological conditions Sample size Pongidae Pan Gorilla Pongo Hylobatidae Hylo bates Cercopithecidae Macaca Papio Colobidae Nasalis Callitrichidae Saguinus Cebidae Aloutta Aotus Cebus 9 11 24 42 49 56 19 26 31 85 90 99 the skeleton' Trauma Healed fractures Infection Arthritis % % o/u 70 55 10 18 21 0 - - 8 199 11 14 41 46 68 6 9 43 118 233 260 - 15 78 250 15 39 61 100 of - 131 27 0 0 16 19 48 24 17 8 0 21 5 20 34 Source Jurmain, 1989 Jurmain, 1989 Fox, 1939 Rollet, 1891 Lovell, 1990b Schultz, 1956 Schultz, 1956 Rollet, 1891 Lovell, 1990a Lovell, 1990b Fox, 1939 Rothschild and Woods, 1989 Randall, 1944 Rollet, 1891 Duckworth, 1911 Fox, 1939 Lovell, 1990b Schultz, 1956 16 17 33 - Schultz, 1937, 1939a Schultz, 1944 Schultz, 1956 - 80 Kessler et al., 1986 Buikstra, 1975 Schultz, 1956 Schultz, 1956 Fox, 1939 Bramblett, 1967 McConnell et al., 1974 29 - 64 - - 2 13 3 39 1 25 41 22 - Schultz, 1956 Schultz, 1942, 1956 56 12 - Schultz, 1956 4933 10 2513 22 3 20 1 27 <I - 2 - 3 Schultz, 1969 Schultz, 1956 Schultz. 1969 Schultz; 1956 Schultz, 1969 8 <1 - 'Sample sizes, frequencies of pathological conditions, and the sources of those data are given for each taxon. Trauma includes healed fractures as well as other traumatic injury, such as cutting, piercing, and superficial wounds. '- indicates that data are not reported for this sample for this pathological condition. 3These samples include crania only, and therefore can be expected to have lower than average frequencies for traumatic lesions. individual animal's lifetime. Populational patterns may be related to specifics of locomotor or social behavior or environment. As in humans, acute, epidemic infectious diseases may have the greatest selective impact, but usually are not discernable from skeletal remains. Therefore, the significance of these diseases in primate evolution can only be postulated, although there are data on epidemic disease in modern nonhuman primates from which such speculation can be derived. For example, a n epidemic of dysentery is believed to be responsible for the deaths of 26 pregnant macaques in the Cay0 Santiago colony in 1940 (Carpenter, 19401, and a presumed yellow fever epidemic was believed to have halved group 132 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 34, 1991 sizes of howler monkeys on Barro Colorado Island and resulted in unusual movement of animals between groups (Carpenter, 1953, 1962). But while any serious epidemic of infectious disease may have resulted in a n evolutionary “bottleneck” effect, as in the post-Columbian New World (e.g., Dobyns, 1983; Ramenofsky, 1987; Zubrow, 1990), the natural history of infectious disease suggests that small and nomadic groups of nonhuman primates would not have maintained such virulent infection. Therefore, it is traumatic injury and chronic, endemic infection that may be relatively more important in determining both populational and individual reproductive success for many taxa. The interpretation of skeletal lesions that indicate chronic infection is particularly interesting since these conditions imply that a n animal’s immune response is fairly effective. In spite of a healthy immune response, however, chronic infection may impair reproductive success. Arthritis, on the other hand, probably has little impact on health and survival and hence reproductive success, unless it impairs an animal’s foraging mobility, but its relationship to joint biomechanics and locomotor style of different taxa makes it useful for the comparative assessment of the etiology of arthritis in humans. Trauma Evidence of traumatic injury is common in the cranial and postcranial skeletons of apes and monkeys, and may take the form of healed fractures or cutting, piercing, or superficial wounds. I t is the most common of all the pathological conditions evident in the skeleton and healed fractures (Fig. 4) are the most frequent type of traumatic lesions. There is considerable variability in the frequencies of traumatic lesions, however. Among the great apes, gorillas seem to exhibit the fewest traumatic lesions. Although fracture frequencies were not reported, limb abnormalities in pygmy chimpanzees were attributed to trauma: these were observed in the field rather than by skeletal analysis, so the cause of the anomalies was difficult to ascertain in many cases, but congenital defects were ruled out since almost all infants and juveniles had normal limbs (Kano, 1984).New World monkeys exhibit varied frequencies of healed fractures, but in general Old World monkeys are more frequently affected. Injuries were found to be rare, however, among Barbary macaques (Deag, 1980): of approximately 350 animals in the study area, only one broken finger, one injury to a hindlimb with a resulting permanent limp, and several animals with scars were noted, and among 100 free-ranging chacma baboons only one fracture, that of a femur with consequent deformity, was noted (McConnell e t al., 1974). Evidence of survival of severe trauma is common, including cases where secondary infection would be a probable outcome. Holland (1924) described a n adult male gorilla whose skeleton exhibits a healed fracture of the humeral shaft with evidence of recovery from a gunshot wound. In a chacma baboon a portion of a rib was missing, apparently resorbed after being shattered by a bullet, which remained in the resulting fibrous scar (McConnell et al., 1984). Multiple injuries are also common. The oldest male Darajani baboon had eleven broken ribs (Bramblett, 1967), and Hugo, the oldest male Gombe chimpanzee, experienced a t least eight fractures (Jurmain, 1989). Deformity following fracture is not uncommon, as healed fractures among orangutans exhibit marked displacement nearly three times as frequently as slight or no deformity (Lovell, 1990bl. Duckworth (1904) described several examples of healed fractures in orangutans, including a case in which excessive callus formation around a fracture resulted in fixture of the forearm in a supinated position, and Korschelt (1930) described a healed fracture of the tibia and fibula that displayed considerable deformity and callus formation. Healed fractures in both chimpanzees and gorillas, however, are predominantly undistorted or only slightly distorted, although marked deformity of a healed forearm fracture in a mountain gorilla has been described (Schaller, 19631, as has a nonunited ulnar fracture and dislocation of the ulna and radius associated with the healed fracture of the humerus in two gorillas (Ferreira, 1938; Schultz, 1950). Consolidation of fractures in chimpanzees and orangutans has been considered to Love111 ILLNESS AND INJURY IN NONHUMAN PRIMATES 133 Fig. 5. “Telescopic”fracture of the distal end of the left second metacarpal in a female mountain gorilla. The articular surface of this bone and of the correspondingproximal phalanx display evidence of arthritis. Fig. 6. Healed fracture of a clavicle in a male orangutan. be almost perfect, with callus and deformity more pronounced in humans who displayed corresponding fractures (Rollet, 1891). The anatomical distribution of fractures is not always reported, but among the Cay0 Santiago macaques the majority of fractures are found in the hindlimb (Buikstra, 1975) while the Gombe chimpanzees exhibit healed fractures predominantly in the forelimb (Jurmain, 1989). Overall, among the great apes, hand and foot bones are most commonly fractured (Fig. 51, followed by the ribs in chimpanzees and gorillas and the clavicle (Fig. 6) and humerus in orangutans (Lovell, 1990b). Ribs were most frequently affected in proboscis monkeys (Schultz, 1942, 1956). Fractured digits and long bones of the hindlimb of yellow baboons were the most 134 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 34, 1991 common injuries, including a femoral neck fracture that led to a false joint (Bramblett, 1967). Schultz (1937, 1944) and Randall (1944) found that healed fractures are more numerous in males than females among the great apes, but Lovell (1990b) found no statistically significant difference in the frequency of injuries between males and females, and no significant sex differences were observed for fractures among macaques (Buikstra, 1975) or baboons (Bramblett, 1967). Infection Very few data are available concerning skeletal lesions of infectious origin in free-ranging primates, and most early studies document only unusual cases. Although a variety of chronic diseases may result in systemic infection that could leave generalized periostitis lesions on the skeleton, few examples have been reported. Chimpanzees display a higher rate of infectious lesions compared to gorillas and orangutans. The frequency of lesions in baboons is low, as is that in capuchin monkeys, while <1% of howler and spider monkeys are affected. Frequencies of skeletal infection in other primates have not been reported. The cause of infectious lesions is often uncertain. Several authors have postulated the presence of yaws, a treponemal disease that is endemic among humans in many tropical areas of the world, in the great apes. Wallis (1934) described lesions in the mandible of a gorilla that he attributed to yaws, as did Denis for cases for facial destruction in that genus (Schultz, 1956:969). Cousins (1972) suggested that the case of leprosy identified in a gorilla (Geddes, 1955, Fig. 19) was more likely yaws. Since the condition was noted only as a caption to a photograph it should perhaps be considered idiopathic, although yaws is endemic in that region and remains a possibility. Schultz also diagnosed yaws as the cause of destructive lesions he observed in a chimpanzee (Schultz, 1956). Two chimpanzees exhibit skeletal lesions that may represent a treponemal syndrome (Lovell, 1990b). Given the uncertainty of these diagnoses, the presence of treponematosis in wild, freeranging apes should be considered unsubstantiated until a positive identification of the infectious pathogen can be made. An unconfirmed diagnosis of treponematosis has been made in baboons, but the condition may not be pathogenic (Fiennes, 1967). Although lesions on long bones in chimpanzees and gorillas have been said to resemble those of tuberculosis (Rollet, 18911, there is no unequivocal evidence of tuberculosis, a major killer of captive primates, in free-ranging animals that have been free of human contact (Rankin and McDiarmid, 1968). While there is much evidence for respiratory infections such a s pneumonia and bronchitis among primates, such as macaques (Fa, 1984; Turckheim and Merz, 19841, chimpanzees (Goodall, 19861, and gorillas (Fossey, 19831, no skeletal evidence of these conditions has been found in documented autopsy cases (Lovell, 1990a). Similarly, apes and monkeys are frequently affected by coughs and colds, particularly during wet seasons (Deag, 1980; Dunbar, 1980; Fossey, 1983; Galdikas, personal communication; Goodall, 1983, 1986; Lindburg, 19711, but no skeletal lesions have been observed, possibly because these infections are of either insufficient duration or severity to leave skeletal scars. Other respiratory infections may be fungal in nature, and can occur by inhalation of spores from contaminated vegetable matter or may be secondary to other infections, especially intestinal parasitism or dietary deficiency (Al-Doory, 1972). Aspergillosis and Candidiasis are not usually serious, often being restricted to the tongue, but the latter was disseminated to a generalized mycosis and caused death in a capuchin monkey (Fiennes, 1967). Histoplasmosis may also be a threat to terrestrial primates, since it is present in soil and has been observed in wild baboons (Fiennes, 1967). The skeletal manifestations of a natural infection of coccidioidomycosis in chimpanzees have been described, although only four of the six animals known to have been infected a t the time of their deaths displayed skeletal lesions attributable to the infection (Long and Merbs, 1981). The leading cause of known deaths among Barbary macaques was fungal skin disease and its sequels (Fa, 19841, but Love111 ILLNESS AND INJURY IN NONHUMAN PRIMATES 135 few subsequent skeletal lesions of fungal disease have been identified. A likely bacterial or fungal infection affected the ankle of a n adult male chimpanzee from Gombe (Jurmain, 1989), and fungal infection in a n immature female at Gombe resulted in swellings of the nose and supraorbital region (Roy and Cameron, 1972). Although this female’s health was excellent in the short term, the infection did not respond to treatment and may have exacerbated the social and physical difficulties she experienced subsequent to a paralytic poliomyelitis infection (Roy and Cameron, 1972; Zihlman et al., 1990). Other infections are reported in apes, but their presence in the wild cannot be determined with certainty. For example, lesions resembling those of leprosy appeared spontaneously in a chimpanzee that had been captured wild in Sierra Leone but it was believed t h a t the animal contracted the disease from a n infected human prior to shipment from Africa (Donham and Leininger, 1977). Although gastroenteritis and peritonitis have been implicated in the deaths of nonhuman primates (Fa, 1984; Fossey, 1983; Turckheim and Merz, 1984), there is no unequivocal skeletal evidence for these conditions. The human paleopathological literature, however, identifies the cranial lesions of cribra orbitalia and porotic hyperostosis as usually representing a n anemic condition (Stuart-Macadam, 1987), often related to a heavy intestinal parasite load. Cribra orbitalia was observed in 30% of orangutans, 29% of chimpanzees, 10% of gorillas, two of 19 rhesus monkeys, and in the one baboon examined, and a nutritional deficiency was postulated a s the most likely cause (Nathan and Haas, 1966), although most nutritional deficiencies reported in the literature are confined to captive animals. Various vitamin B deficiencies have resulted in anemias in captive primates (Wolf, 1972) but no skeletal lesions were reported. Schultz (1956) also reported that he observed lesions consistent with porotic hyperostosis and cribra orbitalia in wild gorillas and chimpanzees. Neither cribra orbitalia nor porotic hyperostosis were observed in a larger survey of chimpanzees, gorillas, and orangutans, however, but different diagnostic criteria andlor the number of subadults in the sample may account for the inconsistencies (Lovell, 1990b). It is odd, however, that more lesions of cribra orbitalia and porotic hyperostosis have not been reported, since a number of parasite species are considered significant in nonhuman primate disease (Kuntz, 1982). Some of these result in chronic ill health, although i t is often not the parasite itself, but the effect of the parasite in addition to, or reacting with, other microorganisms. Subclinical infections may accelerate in captivity or in association with other stress and cause death. Chimpanzees are especially vulnerable to intestinal and filarial roundworms, which cause tissue destruction and hemorrhaging in lungs and intestines and can be fatal. Infection has also been reported in gibbons, orangutans, baboons, and monkeys, producing moderate to severe morbidity and moderate mortality (Fiennes, 1967). Eighty-seven percent of sampled Gombe chimpanzees and 53% of pygmy chimpanzee fecal samples contained eggs of the roundworm Strongyloides (Goodall, 1983, 1986; Hasegawa et al., 19831, although infection in the Gombe animals was not considered heavy. Strongyloides was the most common parasite among the free-ranging Cay0 Santiago rhesus monkeys, although there were no marked symptoms of infection, and the overall health and fecundity of these animals was good (Kessler et al., 1984). Strongyloidiasis was also reported for chacma baboons (Appleton et al., 1986). Oesophagostomiasis is another parasitic infection that is common in Old World primates, and causes moderate morbidity but is rarely fatal (Kuntz, 1982). Oesophagostomum eggs were identified in fecal samples of common and pygmy chimpanzees (Goodall, 1983, 1986; Hasegawa et al., 1983) and chacma baboons (Appleton e t al., 1986). Infection with the hookworm Necator and the whipworm Trichuris was also reported for chimpanzees (Goodall, 1983, 1986). Contact with humans was considered to be minimal, with human waste deposited in latrines and garbage pits; no domestic animals or pets were in the park. McGrew et al. (19891, however, believed that Gombe’s primates have much contact with humans and food items are often handled in unhygienic conditions. 136 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 34, 1991 Although the Gombe chimpanzees exhibit frequent periodic bouts of diarrhea, these are usually associated with a change in diet, such as when the animals consume large quantities of newly ripened fruit (Goodall, 1983). Filariae and microfilariae, which are roundworms of blood and tissue, are ubiquitous and common parasites of all groups of monkeys, apes, and prosimians. Infection is particularly high in South American species (Clark, 1930); some infections may cause death, but others are associated with anemia (Fiennes, 1967). Tapeworms and flukes also infect nonhuman primates. Baboons are known to be reservoir hosts of Schistosoma (Fenwick, 1969; Miller, 1960), and infection was thought to infect half of a population of yellow baboons (Bramblett, 1967). These are the most likely primates to be exposed to such infection because they are largely terrestrial and like to reside near snail-infected water and drink at waterholes where they are observed to search for snails (Fiennes, 1967). However, pygmy chimpanzees and Old and New World monkeys also suffer from schistosomiasis (Cheever et al., 1970; Fiennes, 1967; Hasegawa et al., 1983). Usually the disease resembles mild infections in humans (Fiennes, 1967) and animals appear to acquire a partial immunity as they age (Bramblett, 19671, but severe cases can have lethal consequences (Ohsawa, 1979). Tapeworms may pose a threat to primates that eat raw fish or meat, and in severe infections may cause intestinal perforation and peritonitis (Schmidt, 1978). Intestinal protozoa also infect nonhuman primates. E. histolytica is harmless to Old World monkeys, but is dangerous to humans and apes(Fiennes, 1967). Balantidium coli, observed to infect chacma baboons (Appleton et al., 1986), may seem harmless but can flare up in stress conditions and can be fatal (Fiennes, 1967), but species of Troglodytella are nonpathogenic and almost invariably present in chimpanzees and gorillas (Goodall, 1983, 1986; Goussard et al., 1983; Hasegawa et al., 1983). In addition to intestinal parasites, a variety of blood and tissue protozoa are known to infect nonhuman primates. Natural infection of trypanosomiasis in squirrel, howler, and capuchin monkeys has been reported and infected female squirrel monkeys were found to have higher neonatal mortality and lower total reproductive efficiency than did noninfected females (Travi et al., 1986). Malaria is a serious health threat to humans, but the disease-causing parasites in nonhuman primates appear to be well tolerated and not serious under natural conditions. The malaria parasites appear to have diverged evolutionarily, with different species for humans, apes, and monkeys: Plasmodium reichenowi, which is related to human falciparum malaria, P. vivax schwetzi, which is related to human vivax malaria, P. malariae, related to human P. malariae, P. pitheci, which affects Bornean orangutans and is different from any human form, and P. hylobati, which affects gibbons (Bray, 1963).P. knowlesi is a parasite infecting macaques (Bray, 1963). Malarial parasites have been identified through blood smears in gorillas and chimpanzees, New World monkeys, and Old World monkeys (Reichenow, 1920; Schultz, 1956). Captive primates suffering from malaria are typically lethargic, suffer from loss of appetite, and may shiver; diarrhea may accompany these symptoms (Voller, 1972). Since these symptoms may be mistaken for those of a cold, gastrointestinal infection, or “old age,” the prevalence of malaria in free-ranging animals may be unrecognized or underestimated if blood samples have not been examined. Localized inflammation may be posttraumatic in origin, and osteomyelitis may result if the infection becomes disseminated haematogenously. Five percent of all inflammatory lesions in chimpanzees, gorillas, and orangutans were secondary to trauma (Lovell, 1990b), including cranial osteomyelitis in a silverback mountain gorilla that probably resulted from a bite wound (Fossey, 1983; Lovell, 1990a). Acute osteomyelitis in the right foot, tibia, and fibula of a n adult male baboon was perhaps due to infection from a trapping injury (Bramblett, 1967). Probable osteomyelitis has been observed in the hand of a Gombe female (Jurmain, 1989). In Love111 ILLNESS AND INJURY IN NONHUMAN PRIMATES 137 addition, periostitis that could not be attributed to trauma was noted on both isolated and grouped manual and pedal phalanges in apes, and may reflect localized infection, such a s skin ulcers (Lovell, 1990b). Ascertaining the cause of some skeletal lesions may be difficult, as in the case of a female gorilla who was observed to have a crippled right foot and a n atrophied left forearm, with the left hand being bent inwards and the elbow rigid; this was attributed to a disease called “chully-chang” by the locals, caused by poison of the liana vine (Merfield and Miller, 1956). Arthritis The frequency of arthritis involvement, primarily lipping a t diarthrodial joint margins and a t the amphiarthrodial joints of the vertebral column, varies across genera with the highest frequency in gorillas, followed by chimpanzees and orangutans (Fox, 1939; Jurmain, 1989; Lovell, 1990a,b; Rollet, 1891; Rothschild and Woods, 1989; Schultz, 1956). The mountain gorillas show a higher frequency than do other apes, with the majority of cases involving the vertebrae and including ankylosis of lumbar and sacral elements (Lovell, 1990a). Ottow (1952) reported arthritis in seven of eight aged mountain gorillas, with severe involvement appearing in the lumbar spine. Arthritis in gorillas is anatomically widespread, affecting the knees, elbows, hands, and feet in addition to the spine, and also at the occipital condyles (Randall, 1944; Stecher, 1958a). Taylor and colleagues (1955) described osteoarthritis affecting the left acetabula and femoral heads in two adult males, with one of these cases likely attributable to a slipped femoral capital epiphysis. Another case concerned a n adult female that displayed relatively severe osteoarthritis of the right hip, a condition believed to result from congenital dysplasia (Stecher, 1958b). The relatively high percentage of gorillas affected by arthritis has been attributed by several investigators to the animals’ greater body mass compared to the other genera (Fox, 1939; Lovell, 1990b), but a n analysis of biomechanics and arthritis in gorillas and chimpanzees found a very weak correlation between body size and degenerative joint disease (Woods, 1986). A very strong positive correlation exists, however, between age and pathological involvement (Woods, 1986), as is well documented in humans. Arthritis is also skeletally widespread in orangutans, but for the most part appears to occur secondarily to trauma (Lovell, 1990b), except in the spine. Posttraumatic arthritis has also been reported for gibbons (Schultz, 19441, gorillas (Ferreira, 19381, and macaques (Tasumi, 1969). Marginal lipping of vertebrae, cervical osteoarthritis including eburnation at the dens atloaxial articulation, and evidence of disc herniation are among the manifestations of arthritis t h a t have been reported for orangutans (Fick, 1933; Fox, 1939; Lovell, 1990b). Thoracic disc degeneration is relatively more frequent than cervical arthritis in orangutans, and is a s frequent a s apophyseal changes in the lumbar region (Cook e t al., 1983). Arthritis a t the temporomandibular joint has been observed in gorillas, chimpanzees, orangutans, gibbons, and capuchin, howler, spider, and rhesus monkeys, and almost all of these lesions are either traumatic in origin or subsequent to excessive tooth wear in aged animals (Ferreira, 1938; Fox, 1939; Jurmain, 1989; Lovell, 1990b; Randall, 1944; Schultz, 1939,1940,1941,1950; Tasumi, 1969; Wallis, 1934). Vertebral osteophytosis appears to affect most frequently the lower cervical region in baboons, although elbows, hips, knees, and wrist were also affected (Bramblett, 1967; Fox, 1939; McConnell et al., 1974; Schultz, 1956). Among 25 proboscis monkeys, one adult male exhibited vertebral osteophytosis with ankylosis from T11 through S1, including the ankylosis of one rib (Schultz, 1956). According to one study, both gibbons and macaques show relatively high frequencies of lesions throughout the vertebral column (DeRousseau et al., 1980, cited in Cook et al., 19831, but no arthritis was observed in the spine of a senile male Japanese macaque, nor at the sacroiliac joint, although ossification of the 138 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 34, 1991 pubic symphysis was observed and the animal also exhibited arthritis at the hip, shoulder, and elbow joints (Tasumi, 1969). Arthritis was observed in only four of 250 macaques (Schultz, 19561, but in 80% of a small sample of rhesus monkeys from Cay0 Santiago (Kessler et al., 1986). While the above lesions are mainly those of degenerative joint disease, a similarity between rheumatoid arthritis in humans and an arthritic condition found in the hands of two gorillas has been postulated (Fox, 1939). Spondyloarthropathy has subsequently been described in wild-shot lowland gorillas and chimpanzees (Rothschild and Woods, 1989, 19911, and a psoriatic-like syndrome has been posited in some cases. Other conditions Sumner and colleagues (1989) have described age-related bone loss in freeranging chimpanzees. A skeletal sample of female animals from the Gombe population was examined and was found to display endosteal bone loss similar to humans, except that more bone was lost from cortical, rather than cancellous, sites. An examination of the two female chimpanzees from Gombe that experienced limb paralysis due to polio revealed that bone growth and mineralization of the affected limb was compromised when the paralysis occurred in a subadult, and that left-right assymmetry of shoulder, arm, and forearm bones is pronounced in both animals (Morbeck et al., 1991). A senile male Japanese macaque displayed osteoporosis of the vertebral bodies of the C5 to T1 and T11 to L4 vertebrae, with associated compression fracture and ventral kyphosis (Tasumi, 1969). Several unusual skeletal conditions have been observed in the apes. A femur from an aged female orangutan was considered by Schultz (1956) to exhibit lesions typical of Paget’s disease, and Wegner (1925) offered a tentative diagnosis of Paget’s disease for cranial abnormalities he observed in a female gorilla. A bony growth on the face of a gorilla was ascribed by Schultz (1956) to neoplasia or to goundou (gundu), a disease endemic among humans in West Africa that is usually thought to be a hypertrophic osteitis somehow connected to yaws (Barker and Herbert, 1972). The literature contains a good deal of controversy over the differential diagnosis of hyperostotic conditions in the facial regions of apes and monkeys. Often thought to represent goundou, von Recklinghausen’s disease (Primary hyperparathyroidism), or Paget’s disease, most researchers now consider these diagnoses to be incorrect. Some localized lesions are probably osteomas (Schultz and Starck, 1977). Two gorilla skulls display extreme rarefaction, especially in the alveolar and sinus areas, of unknown origin, although mycotic infection and neoplasia are among the conditions possibly involved (Lovell, 1990b). Although spontaneous soft tissue tumors have been reported for both wild and captive animals, skeletal examples of neoplasia are relatively rare, and no malignant disease has been identified. Lovell (1990b) found benign button osteomas on the face and mandible of both gorilla subspecies, but these were not observed in either chimpanzees or orangutans. Jurmain (1989) reported one case of a benign tumor, perhaps an osteochondroma, in the Gombe chimpanzee, Old Female. The majority of cancers are considered to be degenerative diseases in humans and have their greatest mortality in those over age 60, therefore having little evolutionary impact. The manifestations of cancer in nonhuman primates are, therefore, of comparative interest, given their relative longevity and reproductive life span and the proposed relationship of many human cancers to diet and environmental agents. Various conditions resulting in observable bone deformity (e.g., rickets) in captive Old and New World monkeys have been reported in the literature (Fiennes, 1964; Graham-Jones, 1964; Wright and Bell, 1964); although their etiology remains unknown, probably they are related to inadequate sunlight and poor diet. No unequivocal cases of a condition of this description have been reported for free-ranging animals. Love111 ILLNESS AND INJURY IN NONHUMAN PRIMATES 139 Summary of findings in skeletal pathology Marked patterns exist in the expression of pathological conditions. Traumatic injury is the most common pathological condition, with interesting differences apparent in the nature and location of lesions, which seem to vary functionally. Frequencies of trauma vary among studies as well as among animals, but the available evidence suggests that one in five animals displays at least one healed fracture, and injuries to the digits, cranium, and long bones of the fore and hindlimbs are most common. These patterns may be related variably to aspects of locomotion, aggression, and encounters with human trapping or other collecting activities. For example, the pattern of traumatic injury differs significantly between orangutans and chimpanzees: The latter display primarily piercing or superficial wounds to the cranium while healed fractures of the forelimb and pectoral girdle predominate among orangutans. These differences in anatomical distribution of fractures have been attributed to the animals’ different locomotor patterns and social behaviors (Lovell, 1990b). In general, gorillas display relatively low frequencies of traumatic injury, which may be due to their relatively terrestrial habits and subdued social nature when compared, for example, to chimpanzees. Arthritis is also a common affliction, but its manifestations differ between genera. It is not uncommon in animals of advanced age, and is often a sequel to trauma. Although gorillas exhibit considerable arthritic involvement in the spine, such lesions are apparently less common in chimpanzees. Perhaps most interesting are the findings that vertebral marginal osteophytosis, a condition very common in human and mountain gorilla skeletal remains, is an extremely rare phenomenon in chimpanzees (Jurmain, 1989; Lovell, 1990b), and that arthritic involvement at the temporomandibular joint is widespread. Skeletal evidence of infectious disease is comparatively rare. Most lesions represent localized inflammation, frequently subsequent to trauma, and there is no reliable skeletal evidence for the respiratory and intestinal infections that are so common in nonhuman primates. Compared to human paleopathology, there are no reported cases of nutritional deficiencies among nonhuman primates in the wild. The relative ubiquity of these in certain extinct and extant human populations may therefore be best explained by social and technological factors. Finally, while benign osseous neoplasms are reported, there are as yet no identified cases of malignant neoplasia in the skeletal remains of free-ranging primates. As noted for dental lesions, the variability in samples and methodology preclude any attempt to derive statistical significance from the data in Table 3. The following sections, however, are designed to evaluate patterns of pathological conditions as they relate to aspects of behavior. Table 4 summarizes the skeletal pathological profiles of the primates for which data are available and the locomotor, environmental, and social characteristics for each taxon. The locomotor, habitat, and group categories in Table 4 are presented only as heuristic devices, since the definitions and descriptions of all of these remain controversial in the primate literature. More detailed considerations of these characteristics, such as Ghiglieri’s (1987) summary of social structures of great apes, will be essential if future analyses of their relationships to illness and injury are to be productive. Skeletal pathology and locomotion It has been suggested that trauma in orangutans results mainly from falls, given the animals’ relatively arboreal nature (Lovell, 1990b), a conclusion based on the higher frequency and different anatomical distribution of fractures compared to other apes. Similarly, the high frequency of long bone fractures among gibbons was attributed to falls that occurred during rapid brachiation (Schultz, 1939, 1944). Schultz’s data for gibbons, however, are not significantly higher than those for macaques and baboons (Buikstra, 1975), although the crucial data may relate to anatomical distribution, with gibbon fractures predominantly in the forelimb and - - - Colobidae Nasalis Callitrichidae Saguinus Cebidae Alouatta Aotus Cehus low medium medium low medium medium high medium low medium medium Healed fractures low low low - - low - -2 high low high Infection low low low - low high medium medium medium low low Arthritis arboreal arboreal arbor ea1 arboreal arboreal arboreal terrestrial arboreal arboreal/ terrestrial terrestrial arboreal Habitat quadrupedal quadrupedal quadrupedal quadrupedal quadrupedal quadrupedal quadrupedal brachiation modified brachiation quadrupedal modified brachiation Locomotion multimale monogamous multimale monogamous multimale multimale variable monogamous one male semisolitary multimale Group type marked slight marked slight pronounced pronounced variable slight pronounced pronounced slight Sexual dimorphism 'Relative levels of expression for each pathological condition of the skeleton are taken from data In Table 3. Information on habitat, locomotion, group type and degree of sexual dimorphism are taken from Fedigan (1982) and Napier and Napier (1967). 'A dash indicates that data are not reported for this category of pathological condition. low - Cercopithecidae Macaca Papio medium low high Gorilla Pongo Hylobatidae Hylohates high Pongidae Pan Trauma TABLE 4 . Pathological profiles and lifeways' Love111 ILLNESS AND INJURY IN NONHUMAN PRIMATES 141 baboon and macaque fractures found mainly in the hindlimb (Buikstra, 1975). Like gibbons, orangutans incur more forelimb fractures, while other monkeys reviewed in this paper display most fractures in the hindlimb. Falls during chases and displays, especially among males, may be important causes of injury, and active play of juveniles also results in fractures from falls (Bramblett, 1967; Goodall, 1983). The predicted pattern if locomotor style is correlated with fracture frequency is that the brachiators (gibbons) and modified brachiators (chimpanzees and orangutans) will have the highest frequencies of healed fractures. It is baboons, however, that exhibit the highest frequency of fractures of all primates reviewed here. The explanation may be that baboons are relatively terrestrial and hence they are not well adapted to an arboreal habitat and fall frequently when fleeing through trees (Bramblett, 1967). Gorillas are also terrestrial quadrupeds, however, yet their fracture frequency is relatively low, giving rise to the question of the relative arboreality of these two taxa. The brachiators and modified brachiators have the next highest frequencies, but so too do two Old World and two New World monkey genera, all of which are arboreal quadrupeds. Again in contrast, two other monkey genera that are also arboreal quadrupeds have the lowest frequencies of trauma. These inconsistencies indicate that the broad distinctions of locomotor style and habitat may be insufficiently precise to be useful, and a life history approach to the evaluation of the relationship of locomotion to injury may be more informative. For example, partitioning of frequencies of fractures and arboreal activity between subadults and adults may serve to pinpoint the relationship, if any. Bulstrode and colleagues have determined that falls are 11times more common in young animals than in adults, and concluded that these may be the source of many healed fractures that are recognized in the adult animals (Bulstrode et al., 1986). Thus, terrestrial adult primates may exhibit the results of injury that occurred earlier in the life cycle, i.e., in subadulthood, when locomotor and play activities may have been very different. Individual variation or sex differences in locomotor propensities within any given species, as well as species differences within genera, must also be more closely examined. The significance of the assessment of the association between locomotor style and fracture frequency has to do with the costs of skeletal failure. Brandwood and colleagues (1986) have argued that differences in the frequencies of healed fractures among taxa reflect different costs of skeletal failure and differences in loading regimes. In mammals and birds, for examples, skeletal fracture is deemed t o be more costly than in molluscs, and therefore mammals and birds have lower fracture frequencies. The apparent inconsistency whereby mammals have higher fractures frequencies than do birds, when it would be predicted that wing fractures, for example, would be very costly, was attributed to more unpredictable loads being imposed on mammal skeletons (Brandwood et al., 1986). Thus, an assessment of the relative costs of different locomotor styles might serve to improve our understanding of the various selective pressures a t work in the determination of locomotion and of changes in locomotion and habitat over time. Research into the anatomical adaptations to arboreal and terrestrial environments and the structural characteristics of long bones in different locomotor styles should prove helpful in determining these costs (e.g., Burr et al., 1989; Swartz, 1990). Arthritis manifestations have also been examined in relation to locomotion, but again there are no clear patterns evident in the data in Table 4. The biomechanics of bipedal and quadrupedal locomotor systems were compared in an analysis of the manifestations of osteoarthritis in the hind limb of humans, gorillas, and chimpanzees, and the relationship was found to be a complex one (Woods, 1986). An analysis of the patterns of osteoarthritis in rhesus monkeys and gibbons also revealed a complex relationship between locomotor biomechanics and arthritis (DeRousseau, 1988). The disease is polyarticular and bilateral in both species, but age-progressive in the main joints of the appendicular skeleton in rhesus monkeys and only at the hip and shoulder in gibbons. Sexual dimorphism may play a role in sex differences in manifestation of osteoarthritis. The sexually dimorphic rhesus 142 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 34, 1991 display sex differences while the monomorphic gibbons do not. In addition to these differences in patterning of osteoarthritis, the frequency of osteoarthritis also differs between the two animals, with the macaques consistently exhibiting significantly greater frequencies of osteoarthritis a t their joints. Compressive forces associated with body weight in quadrupedalism may encourage joint degeneration in macaques, although joint shape may also be a factor (DeRousseau, 1988). A comparison of free-ranging and captive macaques indicated that free-ranging animals had a significantly higher prevalence and severity of degenerative joint diseases than did caged animals of the same age, a finding that was attributed to the physical and social environments and accelerated growth and maturation in freeranging monkeys (Kessler e t al., 1986). Skeletal pathology and aggression Much trauma in the apes occurs to the hands and feet, and may be due variously to trap injuries, falls, or fights (Lovell, 1990b). Hands and feet appear to be most vulnerable during intracommunity conflicts at Gombe (Goodall, 1983), although most injuries are not serious. The only fractures observed in a group of Japanese macaques were to the digits (Itani et al., 1963). Howler, capuchin, and spider monkeys display low frequencies of traumatic injury to the cranium (Schultz, 1960; Smith et al., 19771, which may reflect relatively low intergroup conflicts in those animals; however, bite wounds have been observed among several species of macaques (Dittus, 1977; Drickamer, 1975; Hausfater, 1972; Simonds, 1965; Wilson and Boelkins, 1970; Whitten and Smith, 19841, as well as among howler monkeys (Chivers, 1969; Crockett and Pope, 1988), baboons (Dunbar, 1984; Hall and DeVore, 19651, and langurs (Hrdy, 1977). Interpersonal violence, whether inter- or intragroup, appears to be the cause of many cranial injuries (Jurmain, 1989; Lovell, 1990a,b). Violent fights between male geladas often resulted in facial wounds (Ohsawa, 1979). Penetrating wounds to the cranium are common in both chimpanzees and gorillas (Fig. 7) and are strongly suggestive of bite wounds (Jurmain, 1989; Lovell, 1990a,b). Aside from obvious bite wounds and superficial cranial lesions, however, it may be difficult to distinguish cranial injuries that result from fights from those incurred in falls. For example, although mandibular and facial fractures have been reported mainly for gorillas (Lovell, 1990b; Randall, 1944; Wallis, 1934), these injuries in a n orangutan have been identified a s similar to those seen in humans injured in elevator falls (Colyer, 1936). Among the Japanese macaques a t Takasakiyama, injuries were usually caused by fights, with aggression between males, between females, and between males and females (Itani et al., 1963). Similarly, most injuries among rhesus monkeys in north India were assumed to be due to interpersonal conflicts, particularly during mating season (Lindburg, 1971), a s was the case with howler monkeys (Crockett and Pope, 1988). Adult male macaques are apparently most commonly and most seriously injured during male-male conflicts during the mating season (Whitten and Smith, 1984; Wilson and Boelkins, 1970). Young male primates are often objects of more aggression when they reach sexual maturity (Koford, 1966; Otis et al., 1981; Watts, 1990). Both adult and juvenile toque macaques in Sri Lanka were observed with punctures and lacerations on the limbs and head, although males incurred more injuries and more serious injuries than did females and the majority of these resulted from interactions during the mating season (Dittus, 1977; Dittus and Ratnayeke, 1989). Among orangutans, aggression seemed to occur in two contexts: male competitive disputes and sexual assault on females (Mackinnon, 1974). Conflicts between males over females were also observed in mangabeys (Chalmers, 19681, Barbary macaques (Fa, 19841, and mountain gorillas (Watts, 1990). However, aggression between female geladas was observed in addition to the herding behavior of males toward females (Dunbar and Dunbar, 19751, and dispersing females are often subjected to assault from females when they join a new group (Crockett and Pope, 1988). Observable wounds in Love111 ILLNESS AND INJURY IN NONHUMAN PRIMATES 143 Fig. 7. Penetrating wound to the cranial vault in a female mountain gorilla. Fig. 8. Extreme maxillary anterior tooth wear in a male chimpanzee. (Reprinted by permission of the Smithsonian Institution Press from Patterns of Injury and Illness in Great Apes: A Skeletal Analysis, by Nancy C . Lovell. 0 Smithsonian Institution 1990. Fig. 8, p. 205.) baboons often resulted from fights between adult males, the causes of which were food or intolerance of young (Bramblett, 1967). Food was also identified as a factor in one group of mangabeys (Chalmers, 1968b), and reduced access to available food was the most important factor contributing to a n increase in attack frequency 144 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 34, 1991 among chimpanzees, and provisioning may have increased attack frequency by eliciting more attacks with a given aggregation size and promoting large aggregations (Wrangham, 1974). Intragroup aggression among macaques was often precipitated by feeding by humans (Fa, 1984; Lindburg, 1971). A rapid decrease in food availability to free-ranging rhesus monkeys resulted in a decrease in fights, however, since there was no food to fight over and animals were foraging independently (Loy, 1970). As has been noted, (e.g., Bernstein and Ehardt, 19851, intragroup agonistic behavior in some species rarely includes actual fighting, with avoidance the most common response and submission very important. It is essential, therefore, that an assessment of social behaviors such as submission be undertaken in light of the patterning and frequency of aggression-related injury, since such behaviors may result from the selective pressure imparted by injury. Skeletal pathology, mortality, and reproductive success The high mortality of older male macaques on Cay0 Santiago was thought t o result from fighting and the stresses of constant social tension (Koford, 1966). Intercommunity conflicts resulted in injuries believed responsible for 22% of chimpanzee deaths at Gombe from 1965 to 1980 (Goodall, 19831, and 4% of deaths among the Arashiyama West Japanese macaques were attributed to wounding or trauma (Fedigan et al., 1983). Mortality from aggression in prereproductive years is relatively well documented, with infanticide a mortality factor during intra- and intergroup encounters among redtail monkeys (Struhsaker, 19771, capuchin monkeys (Valderrama et al., 19901, howler monkeys (Rumiz, 19901, and Presbytis, Pygathrix, Theropithecus, Papio, Macaca, Cercopithecus, Pan, and Gorilla (Angst and Thommen, 1977; Goodall, 1986; Watts, 1989). These injuries are difficult to associate with the manner of an animal’s death unless there are observational data to support such an interpretation. Infant mortality may also be affected by poor maternal nutrition (Altmann et al., 1977). Therefore, nutrition in the wild, especially seasonally, may have a significant reproductive impact. Other mortality factors also do not have skeletal manifestations. Many primate species may be at risk of predation, for example (Anderson, 1986), but recognition of predation in skeletal remains is rarely possible. In addition, skeletal evidence for infection such as pneumonia and gastroenteritis is relatively unsubstantiated, and thus cannot be used to identify major causes of death although these are the significant factors in mortality of Barbary macaques (Fa, 1984; Turckheim and Merz, 1984), geladas (Dunbar, 1980; Ohsawa, 19791, chimpanzees (Goodall, 1983), and rhesus monkeys (Teas et al., 1981). Deaths among langurs were attributed to intraspecific killings, predation, accidents, starvation, disease, and unknown causes (Rajpurohit and Sommer, 1991). It has also been observed that injured males may lose rank, and this may result in reduced success in competition for food as well as mates (Dittus and Ratnayeke, 1989; Ohsawa, 1979). Although an adult male gorilla was observed to have his right arm torn off from above the elbow, the wound healed perfectly and the male was still head of his family (Merfield and Miller, 1956).Thus there are differences in the effect of injury or illness on rank depending upon whether the social group is in fact a highly ranked one; gorilla groups are typically one male groups. METHODOLOGICAL CONSIDERATIONS Essentials Although an assessment of the evolutionary significance of illness and injury rests on a comparative perspective, the published data are not often comparable due to a variety of methodological problems and inconsistencies. Standardized collection and reporting of pathological data, detailed descriptions of the samples under consideration, and assessments of the validity of samples as representative of either local populations or species are essential if meaningful associations between subsistence, locomotion, social behaviors, and health are to be identified. If future research is to be effective in providing data that can be used to test hypoth- Love111 ILLNESS AND INJURY IN NONHUMAN PRIMATES 145 eses and answer questions about the relationships between dental pathology and way of life, then adherence to standards of data collection and reporting of sample characteristics is essential. Data collection There is a need for a more specific identification of caries frequencies by using the tooth count method as well a s the individual count method, provided that frequencies a r e recorded for each tooth class, the numbers of which vary: New World monkeys have three premolars while Old World Monkeys, apes, and humans have two. Humans, gibbons, and many New World monkeys frequently do not possess a third molar, while in some species supernumerary fourth molars appear not infrequently. As well, the number of affected teeth must be reported as a function of the number of observable teeth, and the possibility of the underestimation of caries frequency because of the antemortem loss of badly decayed teeth must be examined. Application of a “caries correction factor” (Lukacs, 1992), which assumes that antemortem tooth loss results from caries, may be appropriate for human skeletal remains but is not necessarily valid for nonhuman primates. Caries may be the proximate cause, but the ultimate cause may be enamel wear or tooth breakage that exposed the pulp cavity to bacteria, subsequent abscess, and eventual loss. Difficulties also exist in comparing frequencies of abscesses in different studies since authors rarely offer a precise description of what constitutes a scoreable abscess. While periapical abscesses are usually identifiable and typically result from infection of the pulp cavity subsequent to severe wear, caries, or tooth breakage, the etiology of interdontal craters or abscesses may be more difficult to ascertain. These are traditionally thought to be of periodontal disease origin; however, it is also argued that they result from spread of apical infection along the periodontal ligament to the alveolar crest (Clarke et al., 1986). Some researchers categorize only discrete apical discontinuities i n bone as abscesses, with interdontal craters classed cs evidence of periodontal disease, thus leading to confusion. For a n excellent review of the etiology and diagnostic features of periodontal and pulpal pathology the reader is referred to Clarke and Hirsch (1991). All of the reported frequencies of periodontal disease may be too high, since older animals with severe enamel wear may be exhibiting continued tooth eruption rather than bone loss (Fig. 8), and periodontal “pockets” may more properly represent dental abscesses originating apically (cf. Clarke et al., 1986). A reevaluation of the expression of periodontitis in nonhuman primates appears to be in order, since the condition is often thought to be responsible for antemortem tooth loss but may be less important in this regard than is localized alveolar destruction. Precise descriptions of observed arthritic lesions would also assist in the comparison of results between studies. In this review, the term “arthritis” has been used without any attempt to diagnose the specific syndromes involved, although in almost all cases it refers to degenerative joint disease, either osteoarthritis of the apophyseal facet joints or osteophytosis of the vertebral central margins. The differential diagnosis of arthritic syndromes is complex, however, and it is not always clear from available data which condition is actually represented, particularly in earlier papers. Sample characteristics In addition to the need for standardized collection and reporting of pathological data, detailed descriptions of the samples under consideration must also be provided. The sizes of the examined samples are also not always reported, which may not only result in misleading frequencies but prevent a n assessment of the significance of differences in frequencies that may be observed. A strong positive correlation of oral pathology with age is found consistently, which clearly indicates that comparative studies are meaningless without age distributions. Since caries and abscesses were found very rarely on deciduous teeth, and only in captive speci- 146 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 34, 1991 mens, for example (Schultz, 19351, their inclusion in some samples and not others may result in artificial differences in frequencies of these conditions, no matter how statistically significant. Alternatively, caries frequencies may drop with age because those teeth are lost. In addition to the problems of comparing samples with different age distributions, several studies fail to report the species sampled, referring only to genus, or in some cases family. Inconsistencies may therefore appear in the data that are the result of different diets, relative body size, or habitat variations. There are, for example, several recognized species of baboons, which have diverse geographic ranges, different body sizes, and dissimilar social structures (Napier and Napier, 1967; Wolfheim, 1983). Our unqualified acceptance of the close evolutionary relationships among primates may serve to obscure the extent of differences that may be of primary importance in the evaluation of health status. As well, the different life spans of various primates may confound interpretations of lesion frequencies: i t would not be unreasonable, for example, to expect that the number of lesions accumulated during the five-year life span of marmosets in the wild (Hershkovitz, 1970) would be significantly fewer than the number of lesions accumulated by gorillas in their 25- to 30-year life span (Napier and Napier, 1967). Thus, a n evaluation of risks of illness and injury specific to different life stages should be undertaken in addition to a n assessment of accumulated lifetime risk. An issue that is usually only superficially addressed by investigators is whether museum collections can be considered representative of naturally occurring social groups. Opinions on this vary widely. Museum figures may underrepresent reality because some curators apparently discarded badly pathological specimens (Schultz, 1935), although some researchers were confident that their sample was a randomly selected one from a natural population, with none of the specimens preserved or discarded on the basis of pathological conditions (e.g., Smith et al., 1977). Males may be overrepresented since collectors may have preferred males, especially larger males, and males may have been the easiest targets since in many primate species they will aggressively approach intruders. However the memoirs and field records of several collectors make i t clear that among apes at least the collection of a family group was more likely, and that collection was more opportunistic than selective (Lovell, 1990b; Merfield and Miller, 1956). A rigorous attempt at evaluating representativeness was made by Buikstra (1975), but the natural social group to which she compared her museum group was not entirely naturalistic: it was one of four groups whose social composition was previously altered, for example, through partial cropping or experimental manipulation (Sade et al., 1976). Thus, there remains a need to work out new methods to deal with the inadequacies of museum-based samples when attempting taxonomic comparisons. The integrity of “natural” populations evaluated in the field for illness and injury is also problematic, however, and has implications for life history study. Since there are pronounced differences in frequencies of pathological conditions between wild and captive animals (Colyer, 1936, 1947; Schultz, 19351, data on captive animals cannot be used to infer the situation in the wild. In addition, the issue of the provisioning of animals becomes relevant for the interpretation of the etiology of lesions as well a s the assessment of the impact of human intervention on these animals (for a review of the latter, see Asquith, 19891, and the potential for introduction of disease to free-ranging primates who feed on trash must also be considered. Although baboons are parasitized by Schistosoma, animals from regions without human populations were not infected (Fiennes, 1967), and i t has been argued that the infection was acquired from human sources (Nelson, 1960).A “natural” infection of schistosomiasis was reported in a male chimpanzee that had been received from a n animal compound from Sierra Leone (De Paoli, 1965). Although the infection was not experimentally induced, the animal may have contracted the disease while in temporary captivity through direct or indirect human contact. Similarly, schistosomiasis infection in monkeys was thought to have been Love111 ILLNESS AND INJURY IN NONHUMAN PRIMATES 147 contracted before their capture, but the possibility that they were exposed to human infection in Africa while awaiting shipment could not be ruled out (Cheever et al., 1970). Both schistosomes and tapeworms were identified in free-ranging chacma baboons in Kruger National Park, but the natural appearance of these in wild animals remains uncertain. Animals in the park often are in fairly direct contact with humans, when begging for food, or in indirect but potentially dangerous contact, when frequenting trash heaps near tourist camps (McConnell et al., 1974). Similarly, pygmy chimpanzees infected with Stongyloides lived near human residences and may have been infected with human parasites (Hasegawa et al., 1983). Other infectious diseases that affect nonhuman primates appear to originate in human populations. Salmonella gastroenteritis was a mortality factor among Barbary macaques, but is not common in nonhuman primates and was likely contracted from humans (Fa, 1984). Polio and respiratory infection among the Gombe chimpanzees were also thought to be introduced from neighbouring human settlements (Goodall, 1986; Wrangham, 1974). While effectively resulting from human contact, tetanus infection among macaques on Cay0 Santiago was due to their close proximity to a horse, which excreted high concentrations of a form of the tetanus pathogen (Rawlins and Kessler, 1982). Some of the traumatic injury observed in nonhuman primates can also be attributed to encounters with humans (Bramblett, 1967; Fossey, 1983). Rahm (1967) observed the sequels to snare injuries in wild-captured chimpanzees: six of 44 animals exhibited scars and atrophy of distal elements, including two animals that were destroyed because of ingrown snares and subsequent infection. Other than associated with trap injuries, infectious complications to trauma are relatively rare (Duckworth, 1911; Lovell, 1990b). Another potential problem with field study data is that cause of death cannot always be determined with confidence, and the inclusion of “disappearances” as deaths is somewhat controversial. For most primate groups, males are believed to have emigrated if they disappear, while females are assumed to have died, while the reverse is assumed for other species. Caution has been urged in inferring mortality from injuries in primate field observations, especially when social mobility and emigration are common (Crockett and Pope, 1988). In addition, observation of mortality through aggression or accident is thought by some to be easier than observation of death from disease and senescence, which are not as dramatic. In many cases, too, a dying animal becomes separated from the group and its corpse may not be recovered, or the corpse is decayed such that diagnosis of cause of death is not possible. Prospects The data reviewed in this paper are primarily derived from macroscopic examination of the external aspects of the primate skeleton. Technological advances, however, show great promise for providing information on the internal aspects of bones and teeth, as demonstrated by the successful applications of computed tomographic and photon absorptiometric scans to chimpanzee skeletons for assessing bone loss (Sumner et al., 1989) and by scanning electron microscopic examination of tooth surfaces for dietary reconstruction (Teaford, 1985; Teaford and Oyen, 1989; Teaford and Robinson, 1989; Teaford and Walker, 1984). Not only may these methods be used to address specific research questions, but the data they provide may also be important for defining characteristics such as diet and locomotion, which can then be examined for their relationships to pathological profiles. A final issue pertains to the nature of the life history approach. As has been mentioned earlier in this paper, aging and parturition are both important processes in the life cycle. It would be useful to be able to determine the age of a n adult and the number of births by a female in their skeletal remains when such information is not available from field observations, such as is the case with museum specimens. This information would provide direct evidence of longevity and fecun- 148 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 34, 1991 dity for individual animals. There have been numerous attempts to develop reliable methods of obtaining this information from human skeletons (Todd, 1920; McKern and Stewart, 1957; Gilbert and McKern, 1973; Meindl et al., 1985; Suchey and Katz, 1986, Suchey et al., 1986, for age estimates; Kelley, 1979; Suchey et al., 1979, for parturition), but considerable variability in the osseous changes associated with older ages and inconsistencies in the parturition markers indicate that these methods can be applied only with caution. One criticism that has been leveled a t these studies is that the reference collections upon which they are based may have incomplete or incorrect records of age at death and number of births. Research on primate material from longitudinal studies for which these data are well controlled may circumvent that problem. Several studies have attempted to identify skeletal characteristics of aging and parturition through changes in the primate bony pelvis, and these have important implications for both human and alloprimate skeletal biology. An early study indicated that only limited estimations of age could be made on the basis of changes in the pubic symphysis of macaques (Rawlins, 19751, but more recently the degree of pubic resorption in female macaques has been found to be significantly related to both parity and age a t death, and resorption was infrequent in males (Tague, 1990). In contrast, however, obvious differences between males and females, and degrees of resorption relative to number of births, could not be demonstrated for the Gombe chimpanzees (Morbeck and Galloway, 1991). Aside from the utility in identifying life history variables for individual animals, this work is of interest for determining phylogenetic differences in the etiology of skeletal changes associated with parturition, that is, as consequences of hormonal action, shape of the birth canal, and brain size a t birth. Although resorption of the pubic region was associated with age and parity, resorption of the preauricular area was not evident in macaques, in contrast with humans in which these lesions commonly appear (Tague, 1990). As well, differences in bone resorption are apparent between chimpanzees and gorillas (Tague, 1988). Thus, further work in this area may not only develop useful techniques for reconstructing life history, but may also elucidate the physiological and mechanical processes involved in aging and parturition in humans and other primates. CONCLUSIONS The pathological consequences of various primate behaviors and social organizations can be addressed through the study of nonhuman primate skeletal materials a t the individual, local populational, and phylogenetic levels. Individual variation in nutritional, injury, and disease experience is seen to affect reproductive success through subadult mortality, mortality during reproductive years, restriction of a female’s ability to care for her offspring, and impairment of male and female competition for mates. An understanding of the causes of this variation is essential for the interpretation of evolutionary processes, and thus the identification of selective pressures in the environments, behaviors, or events t h a t affect local populations and the recognition of the timing of their impact in different individuals’ life histories is crucial. At the phylogenetic level, a comparative approach is used to examine patterns or central tendencies in pathological profiles, in order to explain these in terms of evolutionary processes and identify the direction of genetic change. Broad distinctions in dietary strategies, locomotion, and social behaviors among primates, however, are currently of limited use in interpreting evolutionary effects, a problem that is a t least partially due to methodological problems. Methodological inconsistencies can be addressed by the adoption of a standard protocol for data collection, such as that prepared by the Paleopathology Association, which may provide the needed uniformity of descriptive and diagnostic criteria in skeletal samples. In addition, more rigorous evaluation of the usefulness of samples themselves will permit assessment of pathological profiles and their associations and impacts on survival and reproductive success more confidently. Lovelll ILLNESS AND INJURY IN NONHUMAN PRIMATES 149 Methodological problems can also be turned to advantage. For example, although contemporary nonhuman primate populations and their settings may no longer be “naturalistic,” it may be that the evaluation of their adaptation to changing environments will provide us with the most useful data for understanding the processes of primate evolution. Paleopathologists examine the adaptation of the human organism to its physical and social-cultural environment, and the relationship of different subsistence economies to human health, such as the transition from a nomadic hunting and gathering lifestyle to a sedentary agricultural one, is a n example of a recent focus of paleopathological research (e.g., Cohen and Armelagos, 1984). And yet, it may be premature to evaluate the health effects of cultural and technological changes throughout prehistory without reference t o baseline data obtained from nonhuman primates that do not possess such culture and technology. Given the evidence for trauma in these animals and their ability to heal and to survive serious injury, the argument commonly found in the paleopathological literature (e.g. Lovejoy and Heiple, 1981) that relatively complete healing of fractures in human populations, albeit with little angulation, implies both medical knowledge and social support for injured or ill group members is a case in point (for a critique of the interpretation of attitudes and social behaviors from skeletal lesions in humans, see Dettwyler, 1991). Nonhuman primates display often remarkable evidence of healing, including cases where potential disability was marked, such as in humeral and clavicular fractures in the arboreal apes. Yet there appear to be no documented cases of the provisioning of injured or ill animals by conspecifics except for cases where mothers have assisted their injured or disabled infants (Berkson, 1973; Chapman and Chapman 1987; Fedigan and Fedigan, 1977; Furuya, 1966; Nakamichi et al., 1983), and the tending of injuries seems to be restricted to cleaning and licking of wounds. Since grooming has been associated with wound-tending among macaques (Dittus and Ratnayeke, 1989; Simonds, 1965), it is possible that some grooming events among other primates have also been related to wound cleaning but have not be recognized or reported as such. While some animals may provide moral support to injured group members, it is important to note th a t this tolerance and altruism is not extended toward injury victims during the competitive activities such as foraging (Dittus and Ratnayeke, 1989). It is vital that these behaviors be examined explicitly, since the behaviors of injured or ill animals and of other group members may influence recovery and survival and hence the reproductive success of the animal. If these behaviors can be shown to be consistent within a local population or within a species, then the evolution of these behaviors may be related to the success of a group or groups. The nature and degree of medical knowledge among nonhuman primates requires further study, as the limited available evidence for these is tantalizing. There is, for example, evidence that nonhuman primates select certain plants for their medicinal value, such as baboons’ utilization of a plant toxic to Schistosoma (Phillips-Conroy, 1986) and chimpanzees’ possible selection of Aspilia leaves and other plants for their pharmacological effects (Huffman and Seifu, 1989; Kawabata and Nishida, 1991; Koshimizu et al., 1991; Wrangham and Goodall, 1989). A continuing dialogue between ethologists and osteologists will ensure that the analyses of skeletal lesions and primate behavior produce more than just discrete and disconnected bodies of data, and integrated research that tests hypotheses derived from skeletal evidence against field observations, or vice versa, will enhance our understanding of the relationships of subsistence, locomotion, social behaviors, and health in both contemporary and ancestral primates. While field studies have in the past tended to provide samples too small for meaningful interpretations of cross-sectional morbidity data, many, such a s at Amboseli, Cay0 Santiago, Gibraltar, Gilgil, Gombe, Karisoke, and the Mahale mountains are now of sufficiently long duration that the longitudinal data essential for life history approaches are becoming available. The anesthetization of baboons for translocation provided an opportunity for the animals to be examined for dental health, 150 YEARBOOK OF PHYSICAL ANTHROPOLOGY [Vol. 34, 1991 injuries, and parasite loads (Strum, 1987).In addition, research focusing on aspects of health and diet is becoming more prevalent (e.g., Hildebolt et al., 1991; PhillipsConroy et al., 1991) and will serve to furnish vital data provided that workers heed the cautions pertaining to methodological comparability. Thus, in the future we should be able to go beyond the theoretical framework presented here and demonstrate empirically the evolutionary significance of illness and injury. Benefits from an improved understanding of the interrelationships of injury, illness, and the social and physical environment of animals, as made possible from this research, also accrue to those concerned with the welfare of animals in zoo and colony settings, leading to reduced health and mortality risks and improved care and conditions for captive animals. ACKNOWLEDGMENTS I thank the Interlibrary Loans staff at the University of Alberta, David Link, and Carolyn Prins for assistance with library research, Linda Fedigan and Lisa Gould for providing me with a number of useful references, and Bob Jurmain and Lynn Kilgore for sharing their thoughts on issues relevant to this paper. Emllke Szathmary and three anonymous reviewers provided helpful comments for the improvement of the manuscript. 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