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An evolutionary framework for assessing illness and injury in nonhuman primates.

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An Evolutionary Framework for Assessing Illness and
Injury in Nonhuman Primates
Department of Anthropology, University of Alberta, Edmonton,
Alberta, Canada T6G 2H4.
ductive success
Paleopathology, Skeletal biology, Natural selection, Repro-
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.
[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
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 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.
Cercoceb us
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
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.
[Vol. 34, 1991
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
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 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.)
[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
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
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
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.
'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).
Erythroce bus
TABLE 2. Dental disease and diet'
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
[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 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
TABLE 3 . Pathological conditions
Hylo bates
the skeleton'
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
Schultz, 1937, 1939a
Schultz, 1944
Schultz, 1956
Kessler et al., 1986
Buikstra, 1975
Schultz, 1956
Schultz, 1956
Fox, 1939
Bramblett, 1967
McConnell et al., 1974
Schultz, 1956
Schultz, 1942, 1956
Schultz, 1956
Schultz, 1969
Schultz, 1956
Schultz. 1969
Schultz; 1956
Schultz, 1969
'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
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
[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.
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
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
[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).
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
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.
[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.,
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
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
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).
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
[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.
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
arbor ea1
one male
'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.
TABLE 4 . Pathological profiles and lifeways'
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
[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
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
[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.
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-
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-
[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
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
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.
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-
[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.
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
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.
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,
[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.
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. Many of the observations made here are based on
research supported by the Natural Sciences and Engineering Research Council of
Canada, the Social Sciences and Humanities Research Council of Canada, the
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