AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 134:520528 (2007)

Dental Indicators of Health and Stress in Early Egyptian

and Nubian Agriculturalists: A Difficult Transition and
Gradual Recovery
Anne P. Starling* and Jay T. Stock
Leverhulme Centre for Human Evolutionary Studies, Department of Biological Anthropology,
University of Cambridge, Cambridge, UK CB2 1QH
KEY WORDS

linear enamel hypoplasia; subsistence transition; Nile valley; Badari

ABSTRACT
Although agriculture is now the globally
predominant mode of food production, studies of the
skeletal remains of early agriculturalists have indicated
high levels of physiological stress and poor health relative to hunter-gatherers in similar environments. Previous studies identifying this trend in different regions
prompt further research of the causes and effects of subsistence transitions in human societies. Here, 242 dentitions from five ancient Egyptian and Nubian populations
are examined: 38 individuals from Jebel Sahaba (Upper
Paleolithic), 56 from Badari (Predynastic), 54 from
Naqada (Predynastic), 47 from Tarkhan (Dynastic), and
47 from Kerma (Dynastic). These populations span the
early period of agricultural intensification along the Nile
valley. Skeletal remains were scored for the presence of
linear enamel hypoplasia (LEH) of the dentition, an
established indicator of physiological stress and growth

interruption. The prevalence of LEH was highest in the

proto-agricultural (pastoralist) Badari population, with
a gradual decline throughout the late Predynastic and
early Dynastic periods of state formation. This suggests
that the period surrounding the emergence of early agriculture in the Nile valley was associated with high stress
and poor health, but that the health of agriculturalists
improved substantially with the increasing urbanization
and trade that accompanied the formation of the Egyptian state. This evidence for poor health among protoand early agriculturalists in the Nile valley supports
theories that agricultural intensification occurred as a
response to ecological or demographic pressure rather
than simply as an innovation over an existing stable
subsistence strategy. Am J Phys Anthropol 134:520528,
2007. V 2007 Wiley-Liss, Inc.

The ancient history of the Nile valley is well-studied

and has fascinated historians and archaeologists for centuries. The Predynastic period has received a great deal
of recent attention as the time when the foundations of
the Pharaonic state were established (Wilkinson, 1999).
Over a relatively short period of time, ancient Egyptian
and Nubian populations transformed from primarily nomadic pastoralist communities to settled agricultural
proto-city-states (Kemp, 1989). Immediately following
this subsistence transition was the emergence of the
worlds first nation-state, a highly hierarchical and centralized bureaucratic polity.
This subsistence transition has been well-documented,
and therefore provides a unique opportunity to study the
health consequences of increasing sedentism and dependence on agriculture. This study examines the conditions of this transition in Egypt and Nubia through a
bioculturally-integrated paleopathological approach. The
prevalence of linear enamel hypoplasia (LEH) of the dentition, an indicator of physiological stress, is examined in
five populations spanning the temporal range of 13000
1500 B.C., including the Neolithic transition.

hierarchical civilization and social complexity (Childe,

1936; Cohen, 1989). However, the paradox that continues
to attract researchers of human biology and history to
questions surrounding the origins of agriculture is how
little this progress seemed to benefit the earliest food
producers (Larsen, 2006).
Despite the intuitive sense that increased social complexity has produced increased quality of life, most studies have shown a decline in health in the earliest agriculturalists (e.g. Cohen and Armelagos, 1984; Cohen,
1989; Steckel and Rose, 2002; Steckel et al., 2002;
Larsen, 2006). While cultivating rather than gathering
plant resources is frequently cited as a means of increasing food security (Smith, 1995; Larsen, 2006), it is also a
risky investment if the crops fail. In addition, the concentration of food resources can be viewed as a liability
rather than an advantage to early hunter-gatherers
adopting domestication, as these food stores may become

AGRICULTURE AND THE NEOLITHIC

REVOLUTION
It is undeniable that the transition from a nomadic
foraging lifestyle to a sedentary agricultural one has had
significant consequences for the human adaptive niche.
This transition has been viewed, historically and
recently, as the crucial shift leading to modern human
C 2007
V

WILEY-LISS, INC.

Grant sponsor: Leverhulme Trust

*Correspondence to: Anne Starling, Department of Biological
Anthropology and Anatomy, Duke University, 08 Biological Sciences
Bldg., Box 90383, Durham, NC 27708-0383.
E-mail: aps4@duke.edu
Received 18 October 2006; accepted 20 July 2007
DOI 10.1002/ajpa.20700
Published online 4 September 2007 in Wiley InterScience
(www.interscience.wiley.com).

DENTAL STRESS MARKERS IN EARLY AGRICULTURALISTS

a target for aggressive neighbors (Cohen, 1989). These
interactions with other human populations, as well as
interactions with the external environment and the internal dynamics of human societies, must be considered
in evaluating the effects of plant and animal domestication on the earliest agriculturalists.
It is clear that the advent of agriculture is associated
with population growth among most Neolithic societies
(Dumond, 1975). However, it is not clear if this population growth has been a cause or effect of agricultural
intensification. One proposed causal link between agriculture and population growth is that sedentism reduces
the interbirth interval, presumably due to reduced physical activity or greater reliability of food resources (Roth,
1985), but this association has been questioned by subsequent researchers and empirical evidence for the link
between sedentism and interbirth interval is weak (Pennington, 1992). An influential work by Boserup (1965)
attempted to reverse this view of causality and to posit
population growth as the independent variable driving
technological and subsistence change. From this perspective, endogenous population pressure would eventually
make a foraging lifestyle less viable and cause the need
for a shift in subsistence (Cohen, 1977). By extension of
this theory, all of the subsequent steps of urbanization
and state formation can also be seen as inevitable consequences of pressures to support a burgeoning population.
The archaeological record can be used to assess
whether the transition to agriculture emerged gradually
as an adaptation over a previously successful strategy, or
as a result of environmental or demographic stress. In
this context, the analysis of skeletal remains can tell us
whether agriculture improved the quality of life of the
earliest farmers, and whether this relationship is consistent through time and space. Previous analyses of
these questions have largely focused on stress and disease though paleopathological markers, as these provide
general indicators of poor quality of life (Cohen and
Armelagos, 1984; Beckett and Lovell, 1994; Larsen,
1995, 2006; Keita and Boyce, 2001; Pechenkina et al.,
2002; Steckel and Rose, 2002; Keita, 2003). Stressful
stimuli recorded in human skeletal remains include disease and parasite load, dietary deficiencies, and synergistic effects between the two (Scrimshaw et al., 1968;
Stephenson and Holland, 1987; Keita, 2003).
In this study, we investigate the patterns of disease
and dietary health over the course of the Neolithic in the
Nile valley, via a commonly studied indicator of general
physiological stress, LEH of the dentition (Kreshover,
1940, 1944; Sarnat and Schour, 1941). This analysis is
used to test whether the patterns of LEH are consistent
across the agricultural transition, and through a time
scale that includes not only the early Neolithic, but also
the growth and expansion of the Egyptian and Nubian
states. The patterns of health and disease that emerge
are interpreted within the context of the causes and
consequences of agricultural intensification in the Nile
valley.

521

1981; Hummert, 1983; Hummert and Van Gerven, 1983;

Martin et al., 1984). However, this sample is notably
lacking material from the Neolithic period in the Nile
valley.
The Nile valley is not considered to be an independent
point of origin of agriculture. The traditional view, still
commonly cited (Smith, 1995), is that domesticated crops
and animals arrived gradually in the area from the fertile crescent. Evidence is accumulating, however, for
early African domestication of cattle and grains in the
Eastern Sahara and Western Desert regions, and these
areas may also have served as sources of domesticated
crops for the Nile valley Neolithic (Warfe, 2003).
Archaeological evidence of cattle domestication in the
Eastern Sahara (Wendorf et al., 1984) has been supported by genetic comparisons of 50 African cattle breeds
(Hanotte et al., 2002), which suggest that cattle were independently domesticated in North Africa prior to interbreeding with domesticated cattle from the Near East.
In addition, some researchers have emphasized the influence of Lower Egypt and the Delta region on the Upper
Egyptian Neolithic (Holmes, 1992; Warfe, 2003). Studies
comparing modern and ancient DNA of domesticates,
support a combination model involving multiple origins
of agriculture with subsequent localized diffusions (Jones
and Brown, 2000).
The first definitive food-producing sites in the Nile valley are from the Badari civilization, at 4500 B.C. Agricultural products at these sites consisted of barley, cattle, and sheep or goats (Arkell and Ucko, 1965). The lack
of evidence of permanent dwellings and the relatively
thin layer of animal droppings at this site are interpreted to mean that the settlement was not inhabited for
very long; the Badarians were likely still seminomadic
pastoralists rather than full-time farmers (Hassan,
1988). Regardless of its first origins, it is undisputed
that agricultural intensification in Egypt proceeded in
earnest through the early Predynastic period, and by the
beginning of the 1st Dynasty the Nile valley region was
comprised of several sedentary communities, loosely
united under the first pharaohs (Kemp, 1989).
This study examines the prevalence of LEH in five
Nile valley populations which surround the temporal
span of the Neolithic, from late Paleolithic hunter-gatherers to the inhabitants of the hierarchical Nubian
Kerma civilization. Based on past studies of other geographical regions, which show increases in skeletal
stress and disease indicators in early agriculturalists as
compared with contemporaneous foragers (Cohen and
Armelagos, 1984; Pechenkina et al., 2002) it is hypothesized that the earliest proto-agricultural population, the
Badari, will show the highest levels of nonspecific stress,
as evidenced by the percentage of individuals with LEH
of the dentition. Later populations are predicted to show
some evidence of recovery and improved health, as
urbanization and social complexity increased and food
shortages were buffered by trade relationships (Hassan,
1988; Keita and Boyce, 2001; Zakrzewski, 2006).

The Northeast African context of agriculture

There has been relatively little study of the human
biology of the agricultural transition in Africa. One
prominent exception is a series of populations from Wadi
Halfa in Sudanese Nubia which have been studied
extensively for over 30 years (Armelagos, 1969; Vagn
Nielsen, 1970; Armelagos et al., 1972; Van Gerven et al.,

MATERIALS AND METHODS

The skeletal remains used in this study were from five
chronologically distinct populations along the Nile in
Egypt and Nubia between 13000 and 1500 B.C. (Table 1).
The five populations existed during three separate
epochs: one in the Upper Paleolithic period, two in the

American Journal of Physical AnthropologyDOI 10.1002/ajpa

522

A.P. STARLING AND J.T. STOCK

TABLE 1. Origins and sample sizes of the study subjectsa

Population

Time period

N dentition

Jebel Sahaba
(Upper Paleolithic)
Badari (Predynastic)
Naqada (Predynastic)
Tarkhan (Early Dynastic)
Kerma (Late Dynastic)
Total

130009000 B.C.

38

50004000
40003100
31002686
21001500

B.C.
B.C.
B.C.
B.C.

56
54
47
47
242

a
All dates are approximate, based primarily on Kemp (1989)
and Zakrzewski (2003).

Predynastic, and two in the Dynastic (or Pharaonic)

period.
The presence or absence and eruption status of all permanent and deciduous teeth was recorded according to
criteria adapted from an earlier system (Moorrees et al.,
1963). Each of the 32 permanent teeth (and 20 deciduous
teeth, if present) was scored as unerupted, emerging, in
occlusion, missing (for unknown reason), postmortem
tooth loss, or antemortem tooth loss. If the tooth crown
was greater than 50% complete, included a complete section from tip to cemento-enamel junction, and was not
obscured by calculus, sediment, or other materials, it
was considered scorable. The number of scorable teeth
was noted for each individual. Loose teeth associated
with an individual were not scored unless they fit completely into a crypt in the mandible or maxilla.

Linear enamel hypoplasia, a nonspecific

stress indicator
LEH is a well-established indicator of individual past
episodes of poor health and growth disturbance (Sarnat
and Schour, 1941; Kreshover, 1940, 1944; Goodman and
Rose, 1990; King et al., 2005). The enamel of permanent
teeth forms during childhood and does not subsequently
remodel (Skinner and Goodman, 1992). Intense periods
of disease and nutritional stress can cause interruptions
in the enamel formation, producing a band of reduced
enamel thickness, or hypoplasia (Harris and Ponitz,
1980). This indicator has been examined in skeletal samples in order to test archaeological theories; for example,
to examine the health effects of increasing urbanization
(Keita and Boyce, 2001) or socioeconomic disparities
(Cucina and Iscan, 1997), or to search for evidence of
historical events such as famine (Lovell and Whyte,
1999). The most common current use of LEH data is to
compare the levels of physiological stress in past populations, including modern humans (Cucina, 2002; King
et al., 2005; Pechenkina and Delgado, 2006; Boldsen,
2007), Neandertals (Guatelli-Steinberg et al., 2004), nonhuman primates (Guatelli-Steinberg and Lukacs, 1999;
Lukacs, 1999; Lukacs, 2001), and human ancestors
(Skinner, 1996).
The primary causes of enamel hypoplasia are heredity,
localized trauma, and systemic metabolic stress
(Goodman and Rose, 1990). Linear hypoplasias result
from disturbances that last between several weeks to a
few months (Rose et al., 1985). Among archaeological
populations, systemic stress appears to be the most common cause of this disorder (Goodman et al., 1980; Goodman and Rose, 1990; Skinner and Goodman, 1992).
While LEH has been accepted as a general indicator of
systemic disturbances in development (Hillson, 1996),

the sensitivity and specificity is largely unknown

(Goodman and Rose, 1990). Formation of LEH bands has
been associated with severe childhood diseases (Hillson,
1996) and childhood nutritional inadequacy (Rose et al.,
1985), but no effort to relate enamel hypoplasia formation to a specific medical cause has yet been successful
(Goodman and Rose, 1990). Studies of living populations
have examined the association of LEH with other dental
diseases and dental caries, as well as with childhood and
congenital diseases (Enwonwu, 1973; Goodman et al.,
1988; Lunardelli and Peres, 2005). The presence of LEH
has been associated with rickets, congenital syphilis, and
tuberculosis (Ortner and Putschar, 1981; Knick, 1982).
Infectious or parasitic disease and malnutrition often
have synergistic effects that may create a more serious
disruption of health, which is then recorded in the bone
and dental enamel (Stephenson and Holland, 1987;
Keita, 2003). In summary, the presence of LEH is a useful non-specific indicator of physiological stress experienced in childhood. Therefore the frequency of this indicator in a population will here be considered to be inversely related to the overall health of the population.

Data collection
Scorable teeth were evaluated for the presence or absence and position of LEH by visual examination of the
buccal surface of each crown, where the defect is most
frequently observable (Goodman and Rose, 1990; Facchini et al., 2004). Enamel hypoplasia was operationally
defined here according to the developmental defects of
enamel (DDE) Index as a quantitative defect of enamel
visually and morphologically identified as involving
the surface of the enamel (an external defect) and associated with a reduced thickness of enamel (FDI, 1982).
The type of defect examined here (and those most frequently referred to in the literature as LEH) falls under
the FDIs Type 4 defects, horizontal grooves (see
Goodman and Rose 1990, for a critical assessment of this
definition).
The presence or absence of LEH bands was recorded
for each tooth in the dentition for each individual, due to
previous reports of differential susceptibility of different
tooth types to enamel defects (Goodman and Armelagos,
1985). It has been noted in several studies that the anterior teeth, particularly the maxillary incisors and mandibular canines, are more susceptible to LEH than are
the more posterior molars and premolars (Goodman and
Armelagos, 1985; Goodman and Rose, 1990; Berti and
Mahaney, 1995). This has led some authors to select particular teeth for controlled observation. For example,
Keita and Boyce (2001) intentionally used posterior (premolar) teeth in their study as they reasoned that these
defects would indicate only the most severe disruptions
of growth. However, due to the fragmentary nature of
many of the ancient specimens in this study, all teeth
positively attributed to a skull were scored for the presence or absence of LEH. Statistical measures were
employed to compensate for the differential preservation
of the different samples. The frequency of LEH in each
population was then examined separately for each tooth
type to address the potential for bias in susceptibility.

Data analysis
2

v tests were used to analyze the differences in prevalence of LEH between populations. Complications

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DENTAL STRESS MARKERS IN EARLY AGRICULTURALISTS

523

Fig. 1. Percentage of individuals with one or more linear

enamel hypoplasia bands anywhere in the dentition, by
population.

encountered in the analysis included the marked differences in tooth preservation between populations, and the
association between the number of teeth observed and
the likelihood of observing LEH (Corruccini et al., 1985;
Ogilvie et al., 1989). As the number of scorable teeth
was not normally distributed, nonparametric tests were
used. Biases in the data were examined using a KruskallWallis test to compare the number of teeth preserved between populations, and a MannWhitney Utest to compare the number of teeth preserved in individuals with and without LEH present. To address the
preservation bias, the prevalence of LEH was also analyzed as a percentage of teeth rather than as a percentage of individuals. In addition, different tooth types were
analyzed separately to examine their differential susceptibility, a factor discussed in previous studies (Goodman
and Rose, 1990).
Of particular interest to this study is the presence or
absence of chronological trends in the frequency of skeletal
stress indicators. The five populations were ranked from
earliest to latest and Kendalls tau correlation was used to
examine the association between the presence of the indicators and chronological order. This was considered to be
more appropriate to this particular association than a
Spearman R test because the Kendalls tau tests the probability that the data are in the same order for the two variables. Therefore it makes no assumptions about the proportional distances between the ranked items.

RESULTS
The overall frequency for the presence of LEH in one
or more teeth was 42.1% of 242 individuals. There were
significant differences between the populations in the
percentage of individuals with one or more LEH bands
anywhere in the dentition (v2 5 27.594; df 5 4; P \
0.001; Fig. 1). The highest frequency of LEH was found
in the early agriculturalists at Badari (69.6%), although
this population also had the highest level of tooth preservation; a correlation discussed in more detail below. A
Kendalls tau test showed significant correlations
between population number (chronologically ranked) and
presence of LEH (P \ 0.001). There was a negative correlation between these variables (T 5 20.202), meaning
that as population rank increased through time, the
prevalence of LEH decreased.
Although the samples were collected in such a way
that the number of scorable dentitions were roughly sim-

Fig. 2. Mean number of scorable teeth per individual in

each population.

Fig. 3. Mean number of scorable teeth present in individuals with and without one or more LEH bands anywhere in the
dentition (Z 5 25.331; P < 0.001; Mann-Whitney U-test).

ilar among the populations (see Methods, Table 1), tooth

preservation had considerable influence on the prevalence of LEH. The number of teeth preserved per individual was not normally distributed. The mean number
of teeth preserved per individual also varied significantly
between populations (v2 5 114.295; df 5 4; P \ 0.001;
KruskallWallis test; Fig. 2). Individuals in the earlier
(Jebel Sahaba and Badari) populations had higher
mean numbers of teeth per individual than did the later
populations.
Previous studies have noted that LEH and other dental defects are frequently underestimated in skeletal
populations because the likelihood of observing defects is
related to the number of teeth preserved (Corruccini et
al., 1985; Ogilvie et al., 1989). This observation was confirmed in the present study: samples with higher mean
number of teeth preserved and scorable showed greater
frequencies of LEH (Z 5 25.331; P \ 0.001; Mann-Whitney U-test; Fig. 3). While this relationship was significant for the entire sample, the association between the

American Journal of Physical AnthropologyDOI 10.1002/ajpa

524

A.P. STARLING AND J.T. STOCK

Fig. 5. Percentage of total teeth with one or more LEH

bands, by population.

Fig. 4. Mean number of scorable teeth preserved in individuals with and without one or more LEH bands anywhere in the
dentition, by population.
TABLE 2. Percentage of teeth in each population with one or
more LEH band
Population
Jebel Sahaba

Badari

Naqada

Tarkhan

Kerma

All Populations

Type of
tooth

N of teeth
with LEH

Total N
of teeth

% of Teeth
with LEH

All teeth
Molars
Premolars
Canines
Incisors
All teeth
Molars
Premolars
Canines
Incisors
All teeth
Molars
Premolars
Canines
Inciscors
All teeth
Molars
Premolars
Canines
Incisors
All teeth
Molars
Premolars
Canines
Incisors
All teeth
Molars
Premolars
Canines
Incisors

44
7
12
9
16
146
39
45
38
24
36
26
6
3
1
43
11
8
8
16
17
14
2
1
0
286
97
73
59
57

676
272
168
94
142
851
382
240
95
134
237
186
42
7
2
463
221
121
27
52
279
219
46
6
8
2,506
1,280
625
247
354

6.5
2.6
7.1
9.6
11.3
17.2
10.2
18.8
40.0
17.9
15.2
14.0
14.3
42.9
50.0
9.3
5.0
6.2
17.8
23.5
6.1
6.4
4.3
16.7
0.0
11.4
7.6
11.7
23.9
16.1

number of teeth in an individuals dentition and the likelihood that one or more of those teeth would show an
LEH band was inconsistent within populations. This
relationship was significant within the Jebel Sahaba,
Badari, and Tarkhan populations, but nonsignificant
within the Naqada and Kerma populations (Fig. 4).
To resolve some of these complexities, results were
separated by population, by tooth, and by tooth type.
Examining the presence of LEH per tooth rather than

Fig. 6. Frequency of LEH by tooth type, entire sample.

per individual reduces preservation bias to some degree,

but this approach has residual influences on results:
LEH defects due to systemic stress are generally found
on more than one tooth (Goodman and Rose, 1990) so
individuals with many teeth preserved may have disproportionate influence on the result. However, this analysis
revealed patterns of differential susceptibility and preservation bias (Table 2).
The patterning of the frequency of LEH per tooth was
very similar to the pattern previously observed per individual, but the trend was even more pronounced (Fig. 5).
The highest per tooth frequency of LEH was in the
Badari population; this was substantially higher than in
the earlier Jebel Sahaba population. There was a gradual decline in prevalence of LEH per tooth over the subsequent populations, with the lowest frequency found
among the Kerma (Dynastic) population.
The sample size of scorable teeth varied greatly for
each tooth type. The largest sample was 164 for permanent left maxillary second molars while the smallest
samples were 37, for both the permanent left and right
mandibular first incisors. The distribution of LEH frequencies by tooth type (Fig. 6) suggests that differential
preservation may have led to underestimation in the
overall frequencies of LEH, as the teeth most likely to
show the defect were the anterior maxillary teeth which
were least frequently preserved. In accordance with previous studies (reviewed in Goodman and Armelagos,
1990) the populations examined here had the highest
rates of LEH in the anterior teeth. The highest frequency of LEH was found in the left mandibular canine
(36.8% of 57 teeth). The lowest frequency of LEH was
found in the left maxillary third molar (1.7% of 115).
This trend was generally consistent within the populations; however, many of these sample sizes were too
small for statistical analysis.

American Journal of Physical AnthropologyDOI 10.1002/ajpa

DENTAL STRESS MARKERS IN EARLY AGRICULTURALISTS

Fig. 7. Frequency of LEH by population for each tooth

type.

When different tooth types were examined separately,

the same general trends were observed: rates of LEH
were generally highest in the Predynastic populations
and lower in the Dynastic ones and the prehistoric foragers (Fig. 7). The differences in LEH frequency between
populations were significant for molars (v2 5 29.956; df
5 4; P \ 0.001), premolars (v2 5 21.409; df 5 4; P \
0.001), and canines (v2 5 26.639; df 5 4; P \ 0.001); and
marginally nonsignificant for incisors (v2 5 8.795; df 5
4; P 5 0.0664), likely due to the very small sample size.
A Kendalls tau correlation showed a significant association between the prevalence of LEH and the chronological population rank (T 5 20.185; P \ 0.002). However,
there appeared to be two separate trends in this data,
an initial increase followed by a decrease in dental stress
indicators. This was addressed by examining the initial
transition to agriculture, from Jebel Sahaba to Badari,
separately from the later progression of agricultural
intensification, from Badari through Kerma. A v2 test
confirmed a significantly higher prevalence of LEH per
individual in Badari than in Jebel Sahaba (v2 5 8.429;
df 5 1; P \ 0.01). Separate Kendalls tau tests showed:
(1) a significant positive correlation between LEH
and population rank for the earliest two populations
(T 5 0.299; P \ 0.005), and (2) a significant negative
correlation for the latter four populations (T 5 20.288;
P \ 0.001). In addition, a binomial logistic regression
predicting the presence or absence of LEH based on population rank for the latter four populations successfully
classified 68.1% of cases.

DISCUSSION
In this study, dental indicators of stress and disease
were analyzed to evaluate the conditions of the transition to agricultural subsistence in the Nile valley. It was
hypothesized that the earliest agricultural populations
would show the highest levels of LEH, indicating the
highest levels of physiological stress. The results supported this hypothesis by demonstrating that the earliest
proto-agricultural population (Badari) had the highest
levels of dental developmental interruptions. It is beyond
the scope of this study to infer whether or not this stress
was due to resource depletion, disease, or dietary insufficiency as suggested by other researchers (Cohen, 1977).
However, this finding does support the idea that the
Neolithic subsistence transition was necessitated by ecological or demographic factors in the Nile valley. As in
many other regions studied, the advent of food production appears to be associated with a decline in health for
the earliest agriculturalists (Cohen and Armelagos,
1984; Steckel and Rose, 2002; Larsen, 2006).

525

The present study differs from previous studies in its

broad time scale and inclusion of the oldest known preagricultural skeletal population in the area (Jebel
Sahaba). This analysis suggests a substantial increase in
stress at the origins of agriculture over late Upper Paleolithic foragers. LEH levels reached a peak in the earliest
agriculturalists, followed by a decline during the period
of intensification and state formation. This pattern persists when the analysis is restricted to like teeth to compensate for differences in susceptibility of different tooth
types (Fig. 7). Of particular interest in Figure 7 is the
LEH prevalence in premolars, which shows pattern very
similar to the overall prevalence of LEH by tooth (Fig.
5). As premolars are less sensitive than incisors or canines to enamel defects, past researchers have argued
for a conservative scoring procedure which includes only
premolars (Keita and Boyce, 2001).
Any comparative study of skeletal populations must
approach the interpretation of differences with caution,
in order to rule out the confounding role of underlying
genetic variation. The populations examined here lived
in roughly the same geographic area, but over a span of
nearly 10,000 years. All populations shared an ecology
that was dominated by the variable floods of the Nile,
which suggests that the broad environmental context of
the samples is relatively consistent. In addition, there is
substantial evidence for contact and trade between populations along the Nile valley as far south as Lower
Nubia, at least as early as the Predynastic period (Arkell
and Ucko, 1965).
The question of the genetic origins of ancient Egyptians, particularly those during the Dynastic period, is
relevant to the current study. Modern interpretations of
Egyptian state formation propose an indigenous origin of
the Dynastic civilization (Hassan, 1988). Early Egyptologists considered Upper and Lower Egyptians to be genetically distinct populations, and viewed the Dynastic period as characterized by a conquest of Upper Egypt by
the Lower Egyptians. More recent interpretations contend that Egyptians from the south actually expanded
into the northern regions during the Dynastic state unification (Hassan, 1988; Savage, 2001), and that the Predynastic populations of Upper and Lower Egypt are morphologically distinct from one another, but not sufficiently distinct to consider either nonindigenous
(Zakrzewski, 2007). The Predynastic populations studied
here, from Naqada and Badari, are both Upper Egyptian
samples, while the Dynastic Egyptian sample (Tarkhan)
is from Lower Egypt. The Dynastic Nubian sample is
from Upper Nubia (Kerma). Previous analyses of cranial
variation found the Badari and Early Predynastic Egyptians to be more similar to other African groups than to
Mediterranean or European populations (Keita, 1990;
Zakrzewski, 2002). In addition, the Badarians have been
described as near the centroid of cranial and dental variation among Predynastic and Dynastic populations studied (Irish, 2006; Zakrzewski, 2007). This suggests that,
at least through the Early Dynastic period, the inhabitants of the Nile valley were a continuous population of
local origin, and no major migration or replacement
events occurred during this time.
Studies of cranial morphology also support the use of
a Nubian (Kerma) population for a comparison of the
Dynastic period, as this group is likely to be more closely
genetically related to the early Nile valley inhabitants
than would be the Late Dynastic Egyptians, who likely
experienced significant mixing with other Mediterranean

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A.P. STARLING AND J.T. STOCK

populations (Zakrzewski, 2002). A craniometric study

found the Naqada and Kerma populations to be morphologically similar (Keita, 1990). Given these and other
prior studies suggesting continuity (Berry et al., 1967;
Berry and Berry, 1972), and the lack of archaeological
evidence of major migration or population replacement
during the Neolithic transition in the Nile valley, we
may cautiously interpret the dental health changes over
time as primarily due to ecological, subsistence, and demographic changes experienced throughout the Nile valley region.
The frequency of LEH in the proto-agriculturalist
Badari population was significantly higher than among
earlier hunter-gatherers, and also higher than among
later populations, during the period of state formation
and increasing social complexity in Nile valley. Why,
then, did the early Badarians become more sedentary
and increase their dependence on agriculture when it
did not immediately increase their health and fitness?
One possibility is that agricultural dependency may
have been forced on a formerly hunting and gathering
population by climatic changes or increased population
density. Archaeological evidence suggests that the shortlived Badari civilization had higher population density
than did other contemporaneous civilizations (Gabriel,
1987; Hassan, 1988). Increases in population may have
been caused by immigration from the Western Desert as
the climate there became more arid and less habitable
around 5000 B.C. (Hassan, 1988, 1993).
It is generally agreed that the techniques of agricultural domestication were adopted much later in the Nile
valley than in the Near East or the Eastern Sahara, despite the likely interactions between the Nile valley
inhabitants and these nearby agriculturalists (Wendorf
et al., 1984, 1992; Holmes, 1993). This delay suggests
that the previous subsistence pattern had to be rendered
unstable before this transition would be desirable or
widespread. This delay in Lower Egypt may be explained
by the fact that soils in the Nile delta region may have
been unsuitable for cultivation prior to increased silt
deposition around 6,000 B.P. (Stanley and Warne, 1993).
However, this does not seem to explain the reluctance of
Upper Egyptians to adopt the grains domesticated by
their Eastern Sahara neighbors as early as 8,000 B.P.
(Wendorf et al., 1992).
When the Neolithic began in the Nile valley, it does
not seem to have been immediately beneficial to human
health. There are numerous costs associated with agricultural intensification, and the proto-agricultural
Badari population likely suffered from many of these. A
significant finding, however, is that the relatively poor
health of the Badarians does not appear to have slowed
the pace of urbanization and increasing social complexity. Urbanism and increasing population density are
almost universally associated with increases in infectious
disease (Cohen, 1989; Stuart-Macadam and Kent, 1992;
Steckel and Rose, 2002) and it is interesting that these
changes, occurring throughout the late Predynastic and
early Dynastic periods, are associated with decreasing
frequencies of LEH disturbances. This may indicate that
the kinds of disturbances recorded by LEH are more frequently those associated with seasonal food shortage
rather than the epidemic diseases of urbanization.
This subtlety of etiology is difficult to separate in modern clinical studies, where poverty inevitably brings both
food insecurity and increased susceptibility to infectious
disease.

Alternatively, lower LEH frequency in later populations studied may indicate that intensification and
urbanization eventually provided greater health and
quality of life for Egyptians. The evidence for improvements in health of these increasingly complex societies
may be attributed to trade relationships and the centralization of food storage and distribution, enabling Predynastic and Dynastic societies to withstand seasonal food
shortages which would have been highly disruptive to an
isolated agricultural community (Hassan, 1988; Savage,
2001). This interpretation is supported by a recent finding that the stature of Nile valley inhabitants increased
throughout the Predynastic period, without evidence of
population discontinuity (Zakrzewski, 2006). Ironically,
this very pooling of resources that may have initially
improved health, enabled concentrations of power in
hierarchical societies characterized by poor quality of life
for those in the lower classes (Hassan, 1988).
Because of the wide geographic and temporal span of
the samples, the differences observed here must be interpreted as preliminary. The different histories of early agricultural intensification in Lower and Upper Egypt may
have influenced LEH manifestation. In addition, there
may still be underlying unidentified differences between
the populations which affect their susceptibilities to defects of dental enamel (Goodman and Rose, 1991). While
the relative similarity between the Upper and Lower
Egyptian morphologies is addressed above, underlying
heterogeneity is most likely to be problematic for the
Jebel Sahaba foragers, because of their temporal distance from the other populations. In addition, there is
some evidence from dental morphology to suggest that
these Paleolithic Nubians are of independent origin to
the later Nubian populations (Irish, 2005).
This study has identified changes in LEH frequency
over time amongst hunter-gatherer, nomadic pastoralist
and agricultural Dynastic populations of the Nile valley.
Future research should investigate whether these trends
are consistent within more finely resolved spatial and
temporal contexts. Conducting more in-depth regional
studies of the interrelationships of sedentism, social complexity, food supply, and social inequality will greatly
enhance our understanding of the relationship between
these factors. In Egypt, as in many other areas of the
world, state formation followed closely on the heels of agricultural intensification, making this initially risky subsistence strategy more reliable and sustainable in the
long run by facilitating the redistribution of resources.
The earliest agriculturalists of this region, as in many
others, bear the mark of a difficult transition between
subsistence strategies.

ACKNOWLEDGMENTS
The authors would like to acknowledge the detailed
and constructive comments of the editor and both
reviewers, which resulted in significant improvements to
the manuscript. We would also like to thank John Taylor
of the Department of Ancient Egypt and Sudan of the
British Museum, London, UK, for access to the Jebel
Sahaba remains. All other specimens were housed in the
Duckworth Collection of the Leverhulme Center for
Human Evolutionary Studies, at the University of Cambridge, UK, and we would like to extend our appreciation to Ms. Maggie Bellatti, for her assistance.

American Journal of Physical AnthropologyDOI 10.1002/ajpa

DENTAL STRESS MARKERS IN EARLY AGRICULTURALISTS

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