Mammal Rev. 1992, Volume 22, No. 2,57-77.

Printed in Great Britain

The biology of cementum increments (with an

archaeologicalapplication)
DANIEL E. LIEBERMAN and RICHARD H. MEADOW
Department of Anthropology, Peabody Museum, Harvard University, Cambridge,
M A 02138, U . S . A .

ABSTRACT
Cementum, a bone-like tissue that surrounds the roots of teeth, anchoring them to the
periodontal ligament, is useful for determining the age at and season of death of
mammals, an issue of concern for both archaeologists and biologists. When a tooth is
sectioned and examined microscopically, cementum appears in bands that differ in
their optical properties and are well correlated with seasonal growth. Because it is a
continually deposited tissue that is rarely modified or resorbed, cementum records the
history of a variety of seasonal factors that affect its growth. An understanding of the
biological nature of cementum is crucial to the identification of these factors and
interpretation of the resulting incremental structure. This paper outlines current
knowledge of the development, histology and function of cementum in the context of
the mammalian masticatory apparatus. Of the various types of cementum, acellular
cementum is often more appropriate for seasonal correlations. Differences between
acellular cementum increments are probably related to specific dietary factors that often
vary between seasons. Cellular cementum increments probably result from phasic
cementogenesis triggered by tooth eruption. This paper outlines a study of cementum
bands in Gazella gazella for which there is an excellent correlation between the season
of death and incremental structures in their cementum. This correlation can be used
to estimate the season of death of gazelles from archaeological sites in the Levant.
Problems for future research are outlined.

INTRODUCTION
The phenomenon of annual or seasonal growth zones in the hard tissues of vertebrates
varies widely from species to species but has been documented in teeth, dermal bones of
the cranium, vertebral centra, and the periosteal surface of limb bones as well as in the
scales, fin spines, otoliths and hypurals of fishes (Peabody, 1961). Incremental growth
structures are found in all three types of mineralized dental tissue: enamel, dentine, and
cementum (for a review, see Hillson, 1986). This paper presents information about the
use of cementum increments for estimating the age at death and season of death of
mammals-issues of concern for both archaeologists and biologists. For archaeologists
such information is important to estimate the season of occupation of sites and to
document animal exploitation patterns. For biologists, who often know the date of death
of an animal, age at death must be ascertained in order to monitor wildlife demography.
Yet carrying out these determinations is not always straightforward, especially when
dealing with zooarchaeological remains. In this regard, analysis of cementum bands can
be of great assistance in testing hypotheses concerning seasonality that have been based
on other sources of information.
58 D . E. Lieberman and R . H . Meadow
Researchers have known for several decades that incremental structures in the
bony tissues of mammals are useful sources of information on aspects of an indi-
vidual’s life history (e.g. Klevezal & Kleinenberg, 1967). Cementum, a bone-like
tissue that is deposited around mammalian teeth below (apical to) the gum line, is
particularly useful in this regard. Unlike other dental tissues, cementum is de-
posited throughout the life of the tooth and, once calcified, is rarely remodelled or
destroyed in siwo. In contrast, dentine ceases to be deposited once the pulp cavity
of the tooth is filled; enamel is no longer deposited once a tooth is fully formed; and
bone is resorbed and remodelled throughout the life of the animal. For this reason,
incremental structures in cementum have been widely used by wildlife biologists to
monitor animal demography (Gordon, 1984, in press). For ancient remains, the
approach has great potential because the data obtained are independent of the
context in which the faunal remains are found. In addition, because teeth preserve
well and are often recovered in large quantities, they are a plentiful source of
information.
Cementum increment analysis has been used extensively since the late 1960s,
particularly in North America, to monitor the age structure of various species for game
management. Although cementum increment analysis is most commonly used to age
ungulates and marine mammals, the method has also been applied to humans (Stott, Sis
& Levy, 1982; Naylor et aI., 1985; Charles et al., 1986; Condon et al., 1986) and other
primates (e.g. Wada, Ohtaishi & Haciya, 1978; Yoneda, 1982; Kay, Rasmussen &
Beard, 1984; Kay & Cant, 1988). Over the last 20 years, several archaeologists have
applied cementum-increment analysis primarily to determine the seasonal use of sites
(e.g. Saxon &Higham, 1968; Kay, 1974; Bourque, Morris & Spiess, 1978; Spiess, 1976,
1979; Gordon, 1988; Lieberman, Deacon & Meadow, 1990).
Tooth sectioning is now widely recognized as a potentially valuable and informa-
tive technique (e.g. Monks, 1981), but has not been widely employed by archaeol-
ogists since its first introduction to the discipline by Saxon & Higham in 1969 (see
Klevezal & Kleinenberg, 1967; Morris, 1972; Stallibrass, 1982). Reasons for this are
many. The techniques used are time consuming, require some special equipment
and expertise, and are generally destructive of specimens. Because the proximate
causes of banding are not entirely understood, it is necessary to prepare and examine
tooth sections from modern animals of the same species and from the same general
area as the archaeological samples in order to provide a model for interpretation of
the ancient material. Interpretation of bands requires experience and too often has
been highly subjective. Post-depositional processes can affect the preservation of
structure in archaeological teeth and may therefore bias results, with particular con-
cern having been expressed about the possibility of loss of the outermost cementum
increment which records information about season of death. Finally, considerable
terminological confusion exists in the literature, largely because of misunderstand-
ings concerning the histology, functional morphology, and development of dental
tissues.
This paper attempts to address some of these issues with reference to incremental
structures in cementum. In recognition of the fact that an understanding of the biology
of the tissue is a prerequisite to interpretation, the nature of cementum is discussed first.
This is followed by presentation of techniques of analysis that the authors have found
most useful. Next an application to Mountain Gazelles Gazellu gazellu in Israel is
described and its archaeological significance described. Finally, directions for future
research are presented.
 The biology of cementum increments 59
CEMENTUM
Cementum is a complex and varied tissue. There are a number of types of cementum
that differ in terms of their histology, development and function. A proper understand-
ing of these differences is crucial because misunderstandings about the nature and
causes of variation in cementum can lead to serious misinterpretations of data. There-
fore, before discussing how cementum increments can be used to estimate age at death
or season of death of mammals, essential aspects of the histology, development and
function of cementum types are reviewed.

Histology
Cementum is a two-phase, bone-like substance, consisting mostly of collagen and
calcium phosphate (hydroxyapatite) that is laid down around the roots of teeth by
cementoblasts. Cementoblasts, which are similar to osteoblasts in structure and histo-
logy (Roberts et al., 1987), differentiate from mesenchymal cells in the periodontal
ligament and deposit cementum on the surface of root dentine and within and around
the Sharpey’s fibres that protrude from the periodontal ligament. T h e collagen
component of cementum has two sources: intrinsic and extrinsic. Intrinsic collagen is
synthesized by cementoblasts and is a critical component of almost all cementum.
Much of the collagen in certain types of cementum, however, is extrinsic. Extrinsic
collagen is synthesized by fibroblasts in the periodontal ligament in long bundles known
as Sharpey’s fibres around which the cementum is deposited (Butler, Birdedal-Hansen
& Taylor, 1975; Johnson, 1987). These extrinsic fibre bundles become mineralized in
the cementum matrix, serving to anchor the tooth root to the periodontal ligament.
Sharpey’s fibres are generally orientated roughly perpendicular to the root surface
(Nalbadian & Frank, 1980;Jones, 1987).The organic phase of cementum also contains a
number of non-collagenous proteins including glycosaminoglycans and proteoglycans
(Knox & Aukhil, 1988; Glimcher & Lefteriou, 1989; McAllister et al., 1990). Most of
the non-collagenous proteins in cementum are poorly known and poorly documented.
There are a number of ways to classify variation in cementum. For the purposes of
this review, cementum is most usefully classified on the basis of both its structure
and development. In terms of its histology, cementum can be divided into two major
categories: acellular and cellular. Cellular and acellular cementum can be further sub-
divided on the basis of whether the collagen in the tissue is extrinsic, intrinsic or mixed. In
addition to acellular and cellular cementum, two other histologically distinguishable
types of cementum can be recognized on the basis of their role in the development of
the tooth: intermediate (hyaline) cementum, and cementoid (or precementum). These
various types of cementum have differences in terms of their function, location, and
development that have significant implications for their use as reliable indicators of
age at and season of death. In general, acellular cementum is the most useful kind of
cementum for these purposes. Figure 1 shows the disposition of acellular and cellular
cementum in relation to other tissues in a Rattus rattus molar and mandible.

Intermediate cementum
Intermediate (or primary) cementum is a narrow band (roughly 10-20pm in most
species) of calcified tissue situated between the granular layer of Tomes of the dentine
and the other types of cementum. Sometimes confused with or mistakenly identified as
the Hyaline layer of dentine, this innermost layer of cementum is generally deposited
before the tooth is fully erupted and has come into occlusion. Intermediate cementum,
which is acellular, differs from the fibrillar cellular or acellular cementum that is
60 D. E. Lieberman and R . H . Meadow
laid down on top of it because it is generally devoid of collagen fibres (Selvig, 1964;
Lindskog, 1982a,b). Lester (1969) and Grevstad & Selvig (1985) have demonstrated,
however, that the histology and development of intermediate cementum varies between
species. For example, the initial layer of cementum in the developing rabbit incisor
contains intrinsic collagen fibres unlike intermediate cementum in mammals such as
rodents and primates. Non-collagenous proteins in intermediate cementum may be
important for regulating or triggering the subsequent production of cementum by
cementoblasts.

Acellular cementum
Acellular cementum is generally distributed towards the coronal (crown) end of the
tooth root (see Fig. 1). It is deposited in increments throughout the life of the tooth
by cementoblasts that form along the margin of the periodontal ligament on the
surface of the cementum in between the bundles of Sharpey’s fibres (Selvig, 1963,1964;
Formicola, Krampf & Thompson Witte, 1971; Jones, 1987) (see Fig. 2). Acellular
cementum is characterized by several features.
1. Because it is laid down at a relatively slow rate, the cementoblasts remain on
the surface of the cementum and do not become embedded in the tissue. Thus
acellular cementum does not incorporate cementocytes or lacunae as is the
case with cellular cementum. This feature makes acellular cementum easily
distinguishable from cellular cementum.
2. Acellular cementum generally has a high proportion of extrinsic (Sharpey’s)
collagen fibres that are extruded from the periodontal ligament. Accordingly,
acellular cementum also has relatively fewer intrinsic collagen fibres. Sharpey’s
fibres, which generally constitute roughly 40% of the matrix by weight, are typi-
cally orientated perpendicular to the root surface or slightly towards the apical
end of the tooth root (Selvig, 1964; Boyde & Jones, 1972; Davis, 1986).

Fig. 1. Histological section of Rattus rattus mandible, showing disposition of cellular and acellular
cementum, dentine, enamel, the periodontal ligament, and the alveolar bone of the mandible.
 The biology of cementum increments 61

Fig. 2. Rurtus ratfus molar, showing the dispositionof accellular cementum, the periodontal ligament (with
mature cementoblasts), and the alveolar bone of the mandible.

3. Acellular cementum in certain regions, particularly towards the cervical end of

the tooth root, is often composed of seasonally deposited bands that in polarized
light appear either opaque or translucent (Klevezal & Kleinenberg, 1967). These
are the bands, illustrated in Fig. 3, that are of special interest to archaeologists and
biologists for estimating the age at and season of death of mammals.
The principal function of acellular cementum is to attach the roots of teeth to the
periodontal ligament. This is accomplished by means of the mineralization of Sharpey’s
fibres that originate in the periodontal ligament within the matrix of the cementum.
Sharpey’s fibres also serve to attach the periodontal ligament to the alveolar bone

Fig. 3. Acellular cementum increments in a modem Gazelluguzellu from Israel (specimen M3769).
62 D. E. Lieberman and R. H . Meadow
(Johnson, 1987). The functional unit comprised of acellular cementum and Sharpey’s
fibres probably reduces movements of the tooth primarily in the mesiodistal and
buccolingual planes. Differences between bands of acellular cementum both within
and between teeth are therefore likely to result from variations in the stresses in the
periodontal ligament surrounding the tooth.

Cellular cementum
Cellular cementum differs from acellular cementum in a number of important features.
1. Cellular cementum is deposited much more rapidly than acellular cementum
and is hence characterized by the presence of cementoblasts that have become
trapped within the cementum matrix (Lindskog, Blomlof & Hammarstrom,
1987). These cells can remain alive for some time in a resting state as cementocytes
(Jones, 1981; Davis, 1986), but because cementum is not nourished by blood
vessels or capillaries, these cells eventually die and leave behind voids (lacunae)
that make this type of cementum easily recognizable (see Fig. 4).
2. Cellular cementum, because of its different means of deposition, has more
intrinsic collagen fibres than acellular cementum, but calcifies around fewer or
sometimes no extrinsic Sharpey’s fibres (Boyde & Jones, 1972).
3. Cellular cementum is most often deposited at the apical end of tooth roots (see
Figs 1 and 4) and near the furcation of roots (e.g. under the molar pad). Cellular
cementum can be considerably wider in section (‘thicker’) than acellular
cementum in some regions, particularly at the apical end of the tooth roots
(Shellis, 1982).
The function of cellular cementum is not entirely understood, but it is likely that, by
filling space, it serves to fill voids between the root and the periodontal ligament as a
tooth erupts. Teeth must erupt as they wear down to maintain a consistent inter-

Fig. 4. Apical end of a thin section of a non-decalcified modem GazelZa gazelZa molar root (specimen
M3769)’showing cellular cementum with lacunae and increments.
 The biology of cementum increments 63
occlusal surface between maxillary and mandibular teeth (Brown & Chapman, 1990).
Deposition of cellular cementum thereby minimizes the movement of the tooth in the
periodontal ligament during occlusion (Graf & Cimasoni, 1988). The rate and amount
of cellular cementum deposition is probably related to the degree of eruption, the
amount of wear in a given tooth, and the overall size of the tooth. It is crucial to recognize
that while the growth of cellular cementum is generally phasic because of long periods of
cementoblast inactivity, there is currently limited evidence that these growth periods
are strongly seasonal. Rest bands in cellular cementum could therefore result from
very different lengths of time. This means that while cellular cementum increments
(discussed below) may have potential for yielding information about an individual’s age
of death, they are not always useful for estimating season of death.

Precementum/cementoid
Recent experiments studying the regeneration of cementum on root surfaces that were
surgically damaged have identified an electron dense, granular zone along the border of
the periodontal ligament and the cementum (Nalbadian & Frank, 1980; Garrett et al.,
1981; Lindskog et al., 1987; Knox & Aukhil, 1988). The precementum or cementoid
(see Fig. 2) is essentially premineralized cementum that is rich in fibres, ground matrix,
and non-collagenous proteins. Precementum is not necessarily present on all parts of
the tooth root where cementum is found. Precementum is probably important in the
development of cementum because it may regulate variations in the nature of the
cementum that is deposited. Research on this layer of incompletely calcified tissue will
be critical in determining which factors regulate cementogenesis (Rose et al., 1987;
McAllister et al., 1990), particularly those factors that result in banding.

Development
An understanding of the differences in the development of the various types of
cementum is important for their use in estimating life-history variables that have
affected their growth. The onset of cementogenesis has been clearly linked to the
disintegration of the epithelial sheath of Hertwig which surrounds the tooth germ.
Intermediate cementum often contains isolated epithelial cells that are remnants of the
root sheath. Initial deposition of the first layer of cementum occurs with the deterio-
ration of the epithelial sheath of Hertwig into isolated regions (the epithelial rests of
Malassez) which exposes the root dentine to the dental follicle. At this point, certain
ectomesenchymal cells differentiate into cementoblasts and lay down intermediate
(primary) cementum around the periphery of the root dentine (Lindskog, 1982a,b;
Lindskog & Hammarstrom, 1982). Formation of intermediate cementum occurs slowly
and gradually, and ceases when the tooth comes into occlusion (Lester, 1969; Formicola
e t al., 1971; Owens, 1980; Jones, 1981).
Cementum continues to be deposited throughout the life of the tooth. Yet, despite
the large amount of research on the histological origins and nature of early cemento-
genesis, little is known about the proximate factors that regulate cellular and acellular
cementogenesis. The rate of cementogenesis appears to be a critical factor in differen-
tiating between these two types of cementum. Cellular cementum is laid down around
cementoblasts in areas where there is rapid cementogenesis, and acellular cementum is
laid down much more slowly along the margin of the periodontal ligament and the tooth
root (Selvig, 1963). Presumably, stresses associated with occlusion trigger cemento-
genesis. Cementum contains a variety of growth factors that regulate the growth,
synthesis, migration and attachment of fibroblasts-factors that are not present in
64 D . E. Lieberman and R . H . Meadow
the periodontal ligament or the dentine (McAllister et al., 1990). These and other
non-collagenous proteins, which are probably produced in precementum, are likely to
be critical in regulating the calcification of the cementum collagen substrate (Knox 81
Aukhil, 1988) as well as in mediating fibroblast activity in the periodontal ligament
(Nalbadian & Frank, 1980; Miki, Narayanan & Page, 1987). A more complete under-
standing of cementogenesiswill require more information on the complex relationships
between cementum and the periodontal ligament.

Incremental structures
A number of researchers have noted the presence of incremental structures in
cementum and have used these increments to estimate the age at and season of death in
both modern and archaeological fauna. Incremental structures in cementum are usually
studied under a microscope from either thin sections or polished thick sections of teeth
that are embedded in a matrix such as resin or epoxy. The number of bands can give
information about the age of death of an individual, provided they are deposited regu-
larly and it is known when the first band forms; and the season of death can be estimated
from the outermost band if there is a consistent relationship between the nature of
different bands and the seasons in which they are deposited. As mentioned above, a
major problem with much of the previous research on incremental bands in cementum
is that researchers have often not distinguished between the different types of
cementum. From the point of view of estimating age at and season of death of mammals,
not all cementum is of equal use. Seasonal variation in tissue growth is different between
cellular and acellular cementum because of the differences in their function and
histology. Incremental growth bands occur in both cellular and acellular cementum that
can be used for estimating age at death, but incremental bands in acellular cementum are
more useful for determining both the age at and the season of death of an individual
because they often can be distinguished more clearly, they are more seasonal in nature,
and they grow more regularly throughout the life of an animal.

Cellular cementum
Incremental growth does occur in cellular cementum, but is poorly studied and of a
different nature than the banding in acellular cementum. Bands in cellular cementum
tend to be concentrated around the apical portion of roots (see Fig. 4). Increments
of cellular cementum are uneven in size and distribution, and vary in their width.
Increments that are closer to the dentine, however, are usually much wider than outer
increments. This probably reflects the slowing rate of tooth eruption as smaller amounts
of cellular cementum are deposited when the tooth erupts less as an animal ages. Unlike
acellular cementum bands, cellular cementum increments are optically similar and are
separated by ‘rest lines’ that probably represent cessation or extreme retardation in the
rate of cementum deposition (Davis, 1986). Jones (1987) has reported differences in the
degree of mineralization across cellular cementum.
Incremental growth bands in cellular cementum are a potentially excellent indicator
of age at death. Their presence in different taxa is most comprehensively summarized
by Grue & Jensen (1979). However, cellular cementum bands do not seem to be as
generally useful for determining season of death. If a tooth erupts rapidly in one
season, then the absence of cellular cementum growth during the rest of the year affords
little scope for precise seasonal determinations. An equally important consideration is
that, because most researchers have not differentiated between cellular and acellular
cementum, it is difficult to evaluate the specific potential of cellular cementum for
 The biology of cementum increments 65
estimating the age at death in many mammalian species. Thus, while Grue & Jensen
(1979) reported considerable variation in apical cementum in terms of the correlation
between the age of mammals and their number of increments, they did not explicitly
distinguish between cellular and acellular cementum. Apical cementum is almost
always cellular. It is interesting to note that in certain species with high-crowned
(hypsodont) teeth, as well as in a number of species with low-crowned (brachydont)
teeth including dogs and humans, there is an extremely poor correlation between age at
death and cellular cementum increments. One must also note, however, that Grue &
Jensen (1979) report relatively good correlations for other species.
As noted by Shellis (1982), there is much variation in the distribution of cellular
cementum both between species and between teeth. In some extremely high-crowned
herbivores (such as equids) as well as in many marine mammals (Boyde, 1980), layers of
cellular cementum containing numerous extrinsic Sharpey’s fibres are deposited
towards the coronal end of the root on either dentine or enamel. In the horse, for
example, cellular coronal cementum with Sharpey’s fibres that connect to the perio-
dontal ligament is deposited on enamel (Jones & Boyde, 1974). Thus, coronally
orientated, extrinsic-fibre cellular cementum may have considerable potential for
estimations of season of death in certain species.

Acellular cementum
Acellular cementum towards the coronal end of tooth roots is generally recognized as
the most useful region in which to study incremental growth structures in cementum.
When sectioned and examined using transmitted light under a polarizing microscope,
acellular cementum appears to be composed of alternating translucent (light) and
opaque (dark) bands (illustrated in Fig. 3). In spite of the fact that the biological
mechanisms that result in these bands are not entirely understood, a large number of
studies on modern fauna have demonstrated that different acellular cementum in-
crements are well correlated with season and age of death for most species. Researchers
have correlated acellular cementum bands with seasonality and age for a large variety of
mammalian species in various environments (for reviews, see Klevezal & Kleinenberg,
1967; Morris, 1972; Casteel, 1975; Stallibrass, 1982; Gordon, 1984, in press).
Generally, if one knows in which season different bands of acellular cementum are
formed, then the season of death of an individual can be estimated by determining the
nature of the outermost band of cementum. Bands that under polarized transmitted
light appear opaque tend to be deposited in most animals during the non-growth season;
they are sometimes mistakenly called rest lines (based on rest lines in cellular
cementum) even though they can be quite wide. In contrast, bands that appear
translucent are usually deposited during the growth season.
Differences in the composition of opaque and translucent acellular cementum bands
that result in their distinguishing optical properties are incompletely understood
at present. Klevezal & Kleinenberg (1967) suggested that opaque bands may be hyper-
calcified, while Kubota et al. (1963) and Ohsumi, Kasuya & Nishiwaki (1963) have
argued that the same bands may be hypocalcified. Unfortunately, as the few ultra-
structural studies of cementum have concentrated on the surface of the root and on
differences between cementum at the apical end and coronal end of the root, little
research has been devoted to the differencesbetween acellular cementum bands (Selvig,
1965; Boyde & Jones, 1972; Jones, 1987). However, recent microprobe analyses by
Lieberman (in press) of caprine mandibular molars indicates that the ratio of calcium to
phosphorus across acellular cementum increments remains constant.
66 D . E. Lieberman and R . H . Meadow
Some researchers have proposed that the different optical properties of opaque and
translucent cementum bands are due to different densities resulting from different rates
of mineralization (Jones, 1981; Davis, 1986). A recent study by Lieberman (to be
published in detail elsewhere), however, suggests that these differences are caused by
changes in the orientation of the Sharpey’s fibres in acellular cementum. Hydroxy-
apatite crystallites in cementum (as in any mineralized tissue) are precipitated along a
pre-existing collagen matrix (Lowenstam & Weiner, 1989). Thus, changes in the orien-
tation of the collagen fibre bundles, around which cementum mineralizes, will affect the
optical behaviour of different bands (for a review, see Gilbert, 1989). As demonstrated
in Fig. 5 , the angle of the collagen bundles in acellular cementum changes between
bands. Sharpey’s fibres probably respond to extrinsic forces exerted on the tooth during
occlusion, resulting in a more-acute angle relative to the orientation of the mineralizing
front under greater occlusal forces (schematized in Fig. 6) Seasonal changes in the
biomechanical stresses placed on teeth therefore may result in acellular cementum
bands. This hypothesis is currently being tested.

Fig.5. Scanningelectronmicroscope view of partially demineralizedsection of modem 0thmolar with two

bands of acellular cementum. Note the change in angle of the Sharpey’sfibre bundles between Band
1 and Band 2.

Because cementogenesis is incompletely understood, it is essential that estimates of

season of death of animals from cementum increment analysis be based on controlled
studies of modern fauna from analogous environments. This requirement may become
less absolute once the causes of banding have been determined.

CEMENTUM INCREMENT ANALYSIS

The technique of cementum increment analysis has been used widely since the 1960s,
particularly by biologists in North America to monitor the age structure of various
species for wildlife management. Because biologists interested in wildlife management
are primarily concerned with estimating the age at death of fauna, a large body of
literature exists on methods of determining the age of death of modem fauna principally
from cellular cementum increments (see Laws, 1952; Klevezal & Kleinenberg, 1967;
Morris, 1972; Spinage, 1973, 1976; Thomas, 1977; Fancy, 1980; Gordon, 1984, in
press). Archaeologists have used cementum increment analysis both to estimate the age
 The biology of cementum increments 67
Increased occlusal force

Sharpeys Fibers

Fig. 6. Schematized cross-section showing the relationship of dentine, acellular cementum, periodontal
ligament, and alveolar bone. Increased occlusal force during certain seasons can result in changes in
Sharpey’s fibre orientation.

at and season of death of animals in order to determine animal exploitation patterns and
to estimate the season of occupation of archaeological sites (e.g. Saxon 8z Higham, 1969;
Kay, 1974; Bourque et al., 1978; Spiess, 1976, 1979; Gordon, 1988; Lieberman et al.,
1990). Archaeologists have therefore concentrated more on seasonal banding in
acellular cementum.
One problem with evaluating the use of cementum increment analysis is that there
is considerable variation in preparation technique and in how increments are analysed.
The discussion below summarizes many of the basic techniques and offers a few
suggestions based on our own experiences.

Preparation of thin sections

Cementum increments range in width between roughly 10 and 100pm, making it
necessary to prepare samples as either polished thick sections for reflected-light
microscopy or as thin sections for transmitted-light microscopy. Because light scatters
when reflected off relatively translucent materials such as dental tissues, transmitted-
light analysis is often preferable to reflected light for the analysis of cementum
increments. Under transmitted light more histological detail can be seen in thin
sections.
The technique of preparation of thin sections can have significant effects on the
interpretation of samples. The optimal thickness of sections depends on a variety of
factors such as the state of preservation of the tooth and the type of equipment being
used. In general, it is best to prepare the samples so that they are thin enough to allow
68 D . E. Lieberman and R. H . Meadow
one to discern major histological features in the tooth such as the dentine tubules, the
granular layer of Tomes, and osteons in the alveolar bone surrounding the tooth. Thin
sections can be prepared using either histological or ground-section (petrographic)
techniques. Histological sections are typically made using a microtome that cuts
sections thinner than 10 pm from decalcified samples that are embedded in paraffin
or Epon@. For most archaeological samples, ground sections are preferable to histo-
logically prepared sections because they do not require decalcification of the tooth
(discussed below), beacuse they are easier to prepare (particularly in the case of large
specimens such as teeth still encased in alveolar bone), and because the state of
preservation of archaeological samples is often insufficient to allow discrimination of
increments in sections less than 15 pm thick. We have found that sections 30 pm thick
are generally optimal.
Even though all teeth have cementum, only teeth that are still encased in alveolar
bone should be analysed because cementum is less hard than dentine (Brear et al., 1990)
and can easily be stripped from the tooth root as a result of various post-mortem
processes. As a result, analysis of loose teeth can often lead to a false determination of the
age and season of death of specimens. If it is necessary to remove teeth from the bone
before embedding the sample, they should be carefully cut out of the alveolar bone with
a high-speed rotary saw (such as a Dremela). Many embedding media, such as resin,
are readily available and easy to use; however, a relatively hard, optically translucent,
non-viscous, and non-exothermic epoxy such as Epo-Tech@ or Buehler Epoxidea
produces optimal quality thin sections. It is particularly important that the epoxy does
not generate heat while it is curing in order to prevent the sample from expanding while
setting. It is also necessary to impregnate specimens under a vacuum to remove air
bubbles.
Thin sections are produced by sectioning embedded teeth either longitudinally or
transversely and affixing them to slides with epoxy. In general, longitudinal sections are
preferable to transverse (cross) sections because they expose more of the perimeter of
the root enabling one to analyse selectively regions that preserve the most cementum
(Stallibrass, 1982). There are many ways to grind down the section to appropriate
thickness (approximately 30 pm). Automated thin-sectioning machines (such as a
Buehler Petrothinm) can produce nearly perfect thin sections in a matter of minutes and
yield the best results. These machines ensure that the sections are ground evenly and
accurately and that very little of the sample is wasted, enabling many sections to
be produced from the same specimen. However, if such equipment is not available,
sections can be cut to between 100 and 200 pm on a low-speed saw (such as a Buehler
Isornet@) and subsequently ground down to their final thickness on a 15-pm diamond
grinding wheel. Polishing both sides of the section is necessary to remove scratches that
result from sectioning and grinding. T o enhance their optical resolution, sections can be
polished using a 6 pm diamond grinding wheel or by other means such as using diamond
paste on a low-nap cloth.
Although some researchers decalcify sections by dissolving the mineral component
of the tissue with acidic solutions such as formic or nitric acid (see Fancy, 1980), we
recommend the use of non-decalcified sections because decalcification can remove some
of the optical qualities (the orientation of hydroxyapatite crystals) that distinguish
between opaque and translucent acellular bands. Moreover, decalcification is particu-
larly inadvisable for archaeological samples as it can result in the disintegration of teeth
that have lost much of their organic (collagen) component (Spiess, 1976). Staining with
dyes such as haematoxylin is principally of use for decalcified histological thin sections.
 The biology of cementum increments 69
Interpretation of thin sections
One source of confusion in the literature results from the fact that researchers often fail
to distinguish the histological nature of the cementum (e.g. cellular or acellular) upon
which they are basing their conclusions. Also, researchers have had the tendency to use
a variety of terms for incremental structures. In addition to urging that researchers
distinguish between cellular and acellular cementum bands, we agree with Gordon’s
(1989) suggesting that bands also be described on the basis of their optical properties as
either opaque or translucent. Terms such as ‘rest lines’ or ‘winter lines’ are imprecise,
can imply different conditions in different environments, and vary depending on the
type of equipment used to analyse samples.
Researchers such as Gordon (1988,1989) have stressed that it is important to exam-
ine the entire perimeter of the tooth under the microscope to ensure that assessments of
age at death and season of death are made in regions where all the cementum is retained.
For acellular cementum, the best regions tend to be near the cervical portion of root
where there is still alveolar bone around the tooth; however, it is critical to remember
that the cervical end of the root may have more increments because it takes more than
one season for the root to form. In contrast, root cementum will cease to have increments
deposited once it has emerged into the oral cavity above the gingival margin. In most
mammals, cellular cementum is generally widest around the apical end of the root.
A polarizing light microscope with a rotatable stage is crucial for distinguishing
between bands of acellular cementum using transmitted light. Electron microscopes can
also be used, but they are less convenient and more expensive for analysing large
numbers of samples. While cementum bands are visible on etched root sections (see
Hillson, 1986), low-voltage backscattered electron microscopy can clearly distinguish
acellular increments.
Post-mortem alteration of the sample can have profound effects on the nature and
clarity of cementum bands. The depositional context of samples sometimes results in
decalcification of cementum bands or in various types of mineralization. Often calcite or
silicon will fill voids in the cementum and other dental tissues. For such samples,
computer image enhancement techniques described by Lieberman et al. (1990) can
greatly improve the resolution of increments without losing information about the
number of bands and the nature of the outermost band. Computer image enhancement
requires the digitization of a microscopic image. The images in this paper were captured
from a microscope on a Macintosh 110computer using a Mass Micro Color Space 110
digitizer in a 640 x 480-pixel PICT format, providing a range of 256 grey levels per
pixel. Once digitized, images can be filtered by a variety of functions that can increase
the contrast between regions with similar pixel values (see Lieberman et al., 1990). The
public-domain software IMAGE (version 1.23) created by Wayne Rasband of the
National Institutes of Health was used to enhance some of the images in this paper (not
all images, however, need to be enhanced).
Computer image analysis is also useful for quantifying the results and reducing the
subjectivity that has often plagued the interpretation of cementum increments. Once a
microscopic image is digitized, image analysis programs (such as IMAGE) can graph the
relative luminance (brightness) of pixels across the cementum increments to quantify
the number of bands and to determine whether the outermost band is opaque or translu-
cent (see Fig. 7). Opaque bands appear as peaks and translucent increments as troughs,
allowing one to calculate precisely the number and nature of increments at selected
regions along the tooth root. Multiple transects (see Fig. 8) provide rapid syntheses of
information on large regions of the tooth, and are particularly useful for discriminating
70 D . E. Lieberman and R . H . Meadow
split lines or false increments. Details of the use of optical image enhancement and
analysis techniques, including information on the cost and necessary equipment, are
discussed in detail in Lieberman et al. (1990).

Fig. 7. Acellular cementum increments of modem Gazella gazella (specimen M3769)from Israel along
with luminance profile of the relative value of pixels along a transect across the increments.

Fig. 8. Section of tooth root of Owis molar from the archaeological site of Tepe Yahya, Iran, showing
acellular cementum increments, void left behind by disintegration of the periodontal ligament, and
the alveolar bone of the mandible. Multiple luminance profiles, at right of rectangular area can
syn,thesize information about the nature and number of cementum bands for a relatively large
region.
 The biology of cementum increments 71
APPLICATION-DETERMINATION OF SEASON OF DEATH OF
GAZELLA GAZELLA FROM ISRAEL
Cementum increment analysis can easily be applied to a wide range of problems
given a basic understanding of the biological bases of cementum growth. One par-
ticular example is the application of the technique to gazelle teeth from the Middle
East to provide useful and needed information on the season of occupation of
archaeological sites. Up to now, the seasons during which most Levantine sites were
occupied have been unknown. However, site seasonality data are crucial for testing
hypotheses concerning the evolution of hunter-gatherer mobility strategies and the
origins of agriculture. There is general agreement among most archaeologists that
agriculture in the Middle East evolved during the Pre-Pottery Neolithic period in
the southern levant around 10,300 years ago, after the Natufian period (Bar-Yosef &
Belfer-Cohen, 1989). People of the Natufian period were complex hunter-gatherers
who differed from previous hunter-gatherers in the region in a number of significant
ways. They gathered and processed large amounts of cereals, built relatively sub-
stantial houses, and made large quantities of new tool forms such as sickles that are
associated with cereal processing. However, there is considerable debate over
whether the Natufians lived in sites throughout the year (i.e. were sedentary) or
whether they were mobile like most hunter-gatherers. Some researchers argue that
sedentism, or some form of reduced mobility, is a necessary precondition to agricul-
ture and that sedentism probably resulted in the origins of food production (e.g. Bar-
Yosef & Belfer-Cohen, 1989; Henry, 1989). Others have argued that sedentism may
have been a result of food production (Moore, 1985). Clearly data on site seasonality,
such as those that can be provided by cementum increment analysis, are needed to
resolve these issues.
Gazelles were chosen for analysis in this study because they are the most common
animals found in Levantine archaeological sites until the domestication of Sheep and
Goats (Bar-Yosef, 1981). Guzella gazellu are also especially useful for seasonality
studies because they are territorial, non-migratory, breed rapidly, and until recently
were plentiful throughout the Levant (Baharav, 1974,1981,1983; Mendelssohn, 1974).
The absence of gazelles at a site from a particular season implies that the site was not
then occupied. It is important to keep in mind, however, that other explanations such as
seasonal avoidance of lean meat need to be examined (e.g. Speth & Spielmann, 1983),
and that evidence of seasonalityderived from fauna always needs to be evaluated in light
of other archaeological data.
Knowledge of the histology and development of cementum increments in modern
gazelles is important for applying cementum increment analysis to archaeological
specimens. Gazelles generally have only acellular cementum surrounding the root;
cellular cementum is almost always limited to root apices and molar pads. The cor-
relation between acellular cementum bands and seasonal deposition in modern gazelles
was first tested on a sample of 20 teeth from 15 modern Gazella gazellu from Israel
whose dates of death are known. Details of the study are reported in Lieberman et al.
(1990) and Lieberman (in press) following the protocol summarized above. As in most
mammals, translucent acellular cementum bands in gazelles are deposited in the
growth season (April-October), and opaque bands are deposited during the ‘non-
growth’ season (November-March). These correlations were verified with two blind
tests. Of the 20 teeth, the season of death of 18 out of 20 were correctly predicted by a
first blind test and 17 out of 20 by a second blind test. Estimation of only the general
season of death was attempted.
72 D. E. Lieberman and R. H . Meadow
Gazelle teeth from a large number of prehistoric sites in the Levant are being
analysed by Lieberman as part of an investigation on the seasonal use of resources by
hunter-gatherers in the region prior to the origins of agriculture. So far, only a few sites
have been studied, one of which is Hayonim Cave in Israel. Hayonim Cave is situated in
the hills of the Mediterranean vegetationalzone, 13 k inland from Haifa (see Fig. 9). The
cave was excavated between 1965 and 1979 by 0. Bar-Yosef, E. Tchernov and B.
Arensburg (Bar-Yosef & Tchernov, 1966; Bar-Yosef & Goren, 1973; Belfer-Cohen,
1988) and the terrace in front was excavated by D. Henry (Henry, Leroi-Gourhan &
Davis, 1981) and F. Valla (Valla, Plisson & Buxo I Capdevila, 1989).Hayonim Cave was
selected as a preliminary study because it contains a well-preserved archaeological
sequence from the Mousterian through the Epipalaeolithic. Tchernov (1984), Davis
(1983) and Pichon (1984) have estimated the season of occupation at Hayonim using
various different kinds of faunal data. Davis (1983) reconstructed the kill-off patterns
of hunted gazelles using crown heights and suggested that the cave was occupied in
the winter during the upper Paleolithic and that the terrace was occupied year-round
during the Natufian. Tchernov (1984) argued that during the Natufian the site as a
whole was occupied throughout the year on the basis of the presence of human

30

100km ,
Fig. 9. Map of southern Levant, showing location of Hayonim Cave as well as other important Natufian
sites.
 The biology of cementum increments 73

Fig. 10. Images of acellular cementum increments alongwith luminance profilesof two archaeological samples
of Gazella gazella from Hayonim Cave. Hay- 1 1, at top, is from the Natufian Period and has an outer
translucent increment, suggesting death between April and October; Hay-19, at bottom, is from the
Kebaran period and has an outer opaque increment,suggestingdeath betweenNovember and March.

commensals including Black Rats Rattus rattus, House Mice Mus musculus and House
Sparrows Passer domesticus. Pichon (1984) has suggested that the presence of both winter
and summer migratory birds implies that the site was occupied throughout the year
during the Natufian.
In this study, a total of 15 gazelle individuals were sampled from the Natufian dated to
between 12,500 and 11,000 BP, and eight individuals from the Kebaran dated to between
17,000 and 14,000 BP (Bar-Yosef 81Belfer-Cohen, 1989). The eight Kebaran samples
represented the only eight preserved mandibles from the 4-5 m2excavated in Layer C; the
Natufian-level mandibles were randomly sampled from different squares within Layer B,
which was roughly 80 m2in size. All eight of the teeth from the Kebaran period had outer
opaque acellular increments, suggesting that the animals were hunted between
November and March. In contrast, of the 13 interpretable teeth from the Natufian, five
had outer opaque acellular increments which clearly suggest that the animals were killed
between November and March, but eight had outer translucent acellular increments that
indicate culling between April and October. Sample images of two tooth roots from
Hayonim (one from the Natufian and one from the Kebaran) and their luminance profiles
are illustrated in Fig. 10. The results are summarized in Fig. 11. On the basis of these data,
one can conclude that the Natufians were either permanently settled at Hayonim or that
they were using the site at least twice a year. In the context of the other archaeological
remains and the analyses of Tchernov (1984) and Davis (1983), the former hypothesis
seems most likely (Lieberman, in press). It should be mentioned that additional teeth
from other layers of the site, as well as teeth from a variety of other Levantine sites are
currently being analysed.
74 D. E. Lieberman and R . H . Meadow

April-October
(OuterT d u c m t I-mt)
' -
November March
(Outer Opaque Increment)
Kebann (Hayonim Level C) 17poO-14,OaO bp

nr5

-
April October ' -
November March
(OuterOpaque Increment)
( O u t a T d u c e n t Increment)
Natufian (HayonimLevel B) lZ,5OO-ll,OOO BP
Fig. 11. Results of Cementum increment analyses of Guzelluguzella teeth from Hayonim Cave.

CONCLUSION
Cementum increment analysis is a technique with great potential for researchers inter-
ested in aspects of the life histories of mammals, in particular in determining age and
season of death. Researchers using cementum for such purposes, however, need to pay
more attention to the histological and functional contests of the tissue. One cannot study
cementum without keeping in mind the variation within the tissue. In particular, it is
crucial that researchers distinguish between the different kinds of cementum that are
being analysed, as acellular and cellular cementum have different functions, histology,
and optical properties.
Considerable research is still needed on cementum, particularly on the bio-
chemistry and functional morphology of the tissue. We still know very little about the
relationships between cementum and the periodontal ligament. Although numerous cor-
relational studies have demonstrated that seasonal differences in diet cause changes in
acellular cementum and that there is phasic growth in cellular cementum, the proximate
biological mechanisms that result in these changes need to be understood if we are
eventually to use cementum accurately and confidently to estimate aspects of the life
history of mammals from environments and contexts that are not completely known.
(Lieberman is currently conducting a controlled experiment on a sample of Goats to
determine which seasonal factors affect acellular and cellular incremental structures
in cementum.) Eventually, such studies on cementum that examine the tissue in the
context of the functional morphological unit comprised of the cementum and the
periodontal ligament will provide useful information not only on techniques for
studying the life histories of mammals from different environments and time periods, but
also on how the growth and structure of bone-like substances such as cementum are
influenced by biomechanical and nutritional stresses.
 The biology of cementum increments 75

ACKNOWLEDGMENTS
We would like to thank the following individuals for their advice and assistance: Dr 0.
Bar-Yosef, Dr A. W. Crompton, C. Harrington, Dr D. Killick, Dr D. Stern, and Dr E.
Tchernov. This research was also supported by funding from the CARE Archaeological
Foundation, the L.S.B. Leakey Foundation, the National Science Foundation, the
Wenner-Gren Foundation, and an NSF Doctoral Dissertation Grant. For commenting
on drafts of this paper, we particularly wish to acknowledge W. A. Barry Brown as well
as an anonymous referee. Finally, we wish to thank Simon Davis as well as the officers
and members of the Mammal Society for providing the stimulus and opportunity to
present aspects of our research, first orally and subsequently in this published form.

REFERENCES
Baharav, D. (1974) Notes on the population structure and biomass of the mountain gazelle, Gazellagazella
gazella. IsraelJournal of Zoology, 23,3944.
Baharav, D. (1981) Food habits of the mountain gazelle in semi-arid habitats of eastern Lower Galilee, Israel.
Journal of Arid Environments, 4,6349.
Baharav, D. (1983) Reproductive strategies in female mountain and dorcas gazelles. Journal of Zoology,
London, 200,445-453.
Bar-Yosef, 0 . (1981) The epi-palaeolithic complexes in the southern Levant. In: Prihistoire du Leoant,
pp. 389-408. Colloques Internationaux du C N R S , 598, Paris.
Bar-Yosef, 0. & Belfer-Cohen, A. (1989) The origins of sedentism and farming communities in the Levant.
Journal of World Prehistory, 3,447-498.
Bar-Yosef, 0 .& Goren, N. (1973) Natufian Remains at Hayonim Cave. Paliorient, 1,49-68.
Bar-Yosef, 0 .& Tchernov, E. (1966) Archaeological finds and fossil faunas of the Natufian and microlithic
industries at Hayonim Cave, Western Galilee (Israel). Israel ExplorafionJournal, 15, 105-140.
Belfer-Cohen, A. (1988) The Natufian Settlement at Hayonim Cave. PhD dissertation, Hebrew University of
Jerusalem.
Bourque, B. J., Morris, K. & Spiess, A. (1978) Determining the season of death of mammal teeth from
archaeological sites: a new sectioning technique. Science, 199,530-531.
Boyde, A. (1980) Histological studies of dental tissues of Odontocetes. In: Age Determination of Toothed
Whales and Sirenians (ed. by W.E. Perrin & A. C. Myrick Jr), pp. 65-87. Reports of the International
Whaling Commission, Cambridge.
Boyde, A. &Jones, S. J. (1972) Scanning electron microscopic studies of the formation of mineralized tissues.
In: Developmental Aspects of Oral Biology (ed. by H. C. Slavkin & L. A. Bavetta), pp. 243-274. Academic
Press, New York.
Brear, K., Currey, J. D., Pond, C. M. & Ramsay, M. A. (1990) The mechanical properties of the dentine and
cement of the tusk of the Narwhal Monodon monoceros compared with those of other mineralized tissues.
Archives of Oral Biology, 35,6154121.
Brown, W. A. B. & Chapman, N. G. (1990) The dentition of fallow deer (Duma dama): a scoring scheme to
assess age from wear of the permanent molariform teeth. Journal of Zoology, London, 221,659-682.
Butler, W. T., Birkedal-Hansen, H. &Taylor, R. E. (1975) Proteins of the periodontium: the chain structure
of the collagens in bovine cementum and periodontal ligament. In: Extracellular Injuence of Gene
Expression (ed. by H. C. Slavkin & R. C. Gerulick), pp. 371-377. Academic Press, New York.
Casteel, R. W. (1975) Incremental growth zones in mammals and their archaeological value. Kroeber
Anthropological Association Papers, 47148,l-27.
Charles, D. K., Condon, K., Cheverud, J. M. & Buikstra, J. E. (1986) Cementum annulation and age
determination in Homo sapiens I: tooth variability and observer error. American Journal of Physical
Anthropology, 71,311-320.
Condon, K., Charles, D. K., Cheverud, J. M. & Buikstra, J. E. (1986) Cementum annulation and age
determination in Homo sapiens 11, estimates and accuracy. AmericanJournal of Physical Anthropology, 71,
321-330.
Davies, S. J. (1983) The age profiles of gazelles predated by ancient man in Israel: possible evidence for a shift
from seasonality to sedentism in the Natufian. Paliorient, 9,5542.
Davis, W. L. (1986) Oral Histology. W.B. Saunders, Philadelphia, PA.
Fancy, S. G. (1980) Preparation of mammalian teeth for age determination by cementum layers: a review.
Wildrife Society Bulletin, 8,242-248.
Formicola, A. J., Krampf, J. I. & Thompson Witte, E. (1971) Cementogenesis on developing rat molars.
Journal of Periodontics, 42,766-773.
Garrett, S . , Bogle, G., Adams, D. & Egelberg, J. (1981) The effect of notching into dentine on new cementum
formation during periodontal wound healing. Journal of Periodontal Research, 16,358-361.
Gilbert, A. S. (1989) Microscopic bone structure in wild and domestic animals: a reappraisal. In: Early
Animal Domestication and its Cultural Context (ed. by P. J. Crabtree, D. Campana & K. Ryan), pp. 46-86.
MASCA Research Papers in Science and Archaeology, Philadelphia.
Glimcher, M. J. & Lefteriou, B. (1989) Soluble glycosylated phosphoproteins of cementum. Calcified Tissue
International, 45, 165-1 72.
Gordon, B. C. (1984) Selected bibliography of dental annular studies on various mammals. Zooarchaeological
Research News Supplement 2 .
76 D . E. Lieberman and R . H . Meadow
Gordon, B. C. (1988) Of Men and Reindeer Herds in French Magdalenian Prehistory. BAR S390, Oxford.
Gordon, B. C. (1989). Archaeological tooth and bone seasonal increments: the need for standardized terms and
techniques. Paper presented at 54th Annual Meeting, Society for American Archaeology, Atlanta, 5-9
April 1989.
Gordon, B. C. (in press) Archaeological seasonality using incremental structures in teeth: an annotated
bibliography. ZooarchaeologicalResearch News Supplement.
Graf, J. M. & Cimasoni, G. (1988) Le cement, cet oublie. Revue Mens Suisse Odontologie et Stomatologie, 98,
847-854.
Grevstad, H. J . & Selvig, K. A. (1985) Location and ultrastructure of the first cementum formed in rabbit
incisors.Journal of Dental Research, 93,289-303.
Grue, H. & Jensen, B. (1979) Review of the formation of incremental lines in tooth cementum of terrestrial
mammals. Danish Review of Game Biology, 11,143.
Henry, D. 0. (1989) From Foraging to Agriculture: the Levant at the End of the Ice Age. University of
Pennsylvania Press, Philadelphia.
Henry, D. O., Leroi-Gourhan, A. &Davis, S. (1981)Hayonim Terrace: Late Pleistocene changes in environ-
ment and economy.Journal of Archaeological Science, 8,33-58.
Hillson, S . (1986) Teeth. Cambridge University Press, Cambridge.
Johnson, R. (1987) A classification of Sharpey's fibers within the alveolar bone of the mouse: a high voltage
electron microscope study. The Anatomical Record, 217,339-347.
Jones, S. J. (1981) Dental Tissues. In: Dental Anatomy and Embryology (ed. by J. W. Osborne), pp. 66-209.
Blackwell ScientificPublications, Oxford.
Jones, S. J. (1987) The root surface: an illustrated review of some scanning electron microscope studies.
Scanning Microscopy, 1,2003-2018.
Jones, S. J. & Boyde, A. (1974) Coronal cementogenesisin the horse. Archives of Oral Biology, 19,605-614.
Kay, M. (1974) Dental annuli age determination on white-tailed deer from archaeological sites. Plains
Anthropologist, 19,224227.
Kay, R. F. & Cant, J. G. H. (1988) Age assessment using cementum annulus counts and tooth wear in a free-
ranging population of Macaca mulatta. AmericanJournal of Primatology, 15,1-15.
Kay, R. F., Rasmussen, D. T. & Beard, K. C. (1984) Cementum annulus counts provide a means for age
determination in Macaca mulatta. Folia Primatologica, 42,85-95.
Klevezal, G. A. & Kleinenberg, S. E. (1967) Age Determination of Mammals by Layered Structure in Teeth
and Bone. (Original title: Opredelenie Vozrusta mlekopitayushchikh po sloistym strukturam zubov i kostz].
Institut Morfologii Zhivotnykh im. A.N. Severtsova, Akademiya Nauk S.S.S.R., Moscow. (Translations
Series No. 1024, Foreign Languages Division, Department of the Secretary of State of Canada. Fisheries
Research Board of Canada, Ste. Anne de Bellevue, Quebec).
Knox, B. & Aukhil, I. (1988) Ultrastructural study of experimental cementum regeneration in rats.Journa1 of
Periodontal Research, 23,6047.
Kubota, K., Matsumoto, K., Nagasaki, F. & Tsuboi, M. (1963) An age determination of the highly aged fur
seal by means ofphotography of the maxillary canine. Bulletin of the Tokyo Medicaland Dental University,
10,61-73.
Laws, R. M. (1952) A new method of age determination for mammals. Nature, 169,972.
Lester, K. S. (1969) The unusual nature of root formation in molar teeth of the laboratory rat. Journal of
Ultrastructural Research, 28,481-506.
Lieberman, D. E. (in press) Seasonality and gazelle hunting at Hayonim Cave: new evidence for sedentism
during the Natufian. Paldorient.
Lieberman, D. E.,Deacon, T. W. & Meadow, R. H. (1990) Computer image enhancement and analysis of
cementum increments as applied to teeth of Gazella gazella. Journal of Archaeological Science, 17,
519-533.
Lindskog, S. (1982a) Formation of intermediate cementum I: early mineralization of aprismatic enamel and
intermediate cementum in monkey.Journalof CraniofacialGenetics and Developmental Biology, 2,147-1 60.
Lindskog, S. (1982b) Formation of intermediate cementum 11: a scanning electron microscope study of the
epithelialroot sheath of Hertwig in monkey .Journalof Craniofacial Genetics and Developmental Biology, 2,
161-169.
Lindskog, S. & Hammarstrom, L. (1982) Formation of intermediate cementum 111: 'H-Tryptophan and
'H-Proline uptake into the epithelial root sheath of Hertwig in vitro. Journal of Craniofacial Genetics and
Developmental Biology, 2,171-177.
Lindskog, S . , Blomlof, L. & Hammarstrom, L. (1987) Cellular colonization of denuded root surfaces in
vivo: cell morphology in dentin resorption and cementum repair. Journal of Clinical Periodontology, 14,
390-395.
Lowenstam, H. A. & Weiner, S. (1989) On Biomineralization. Oxford University Press, Oxford.
McAllister, B., Narayanan, A. S., Miki, Y. & Page, R. C. (1990) Isolation of a fibroblast attachment protein
from cementum.Journal of Periodontal Research, 25,99-105.
Mendelssohn, H. (1974) The development of the populations of gazelles in Israel and their behavioural
adaptations. In: The Behaviour of Ungulates and Its Relationship to Management (ed. by V. Geist & F. R.
Walther), pp. 722-742. IUCN Publications (New Series, No. 24) Morges, Switzerland.
Miki, Y., Narayanan, A. S.& Page, R. C. (1987) Mitogenic activity of cementum components to gingival
fibroblasts.Journal of Dental Research, 66, 1399-1403.
Monks, G. G. (1981) Seasonality studies. In: Advances in Archaeological Method and Theory, Vol. 4 (ed. by M.
B. Schiffer), pp. 177-240. Academic Press, New York.
Moore, A. M. T. (1985) The development of Neolithic societies in the Near East. In: Advances in World
Archaeology, Vol. 4 (ed. by F. Wendorf& A. Close), pp. 1-69. Academic Press, New York.
Morris, P. A. (1972) A review of mammalian age determination methods. Mammal Review, 2,69-104.
 The biology of cementum increments 77
Nalbadian, J. & Frank, R. M. (1980) Electron microscopic study of the regeneration of cementum and
periodontal connective tissue in the cat. Journal of Periodontal Research, 15,7 1-89.
Naylor, J. W., Miller, W. G., Stokes, G. N. & Stott, G. C. (1985) Cementum annulation enhancement: a
technique for age determination in man. AmericanJournal of Physical Anthropology, 68,197-200.
Ohsumi, S . , Kasuya, T. & Nishiwaki, M. (1963) Accumulation rate of dental growth layers in the maxillary
tooth of the sperm whale. Whales Research Institute, Scientific Reports, 17,1535.
Owens, P. D. A. (1980) A light and electron microscope study of the early stages of root surface formation in
molar teeth in the rat. Archives of Oral Biology, 24,901-907.
Peabody, F. E. (1961) Annual growth zones in living and fossil vertebrates. Journal of Morphology, 108,
11-62.
Pichon, J. (1984) L’avifaune natoufien du Levant. Doctoral dissertation, Universite Pierre et Marie Curie
(Paris VI), Paris.
Roberts, W. E., Wood, H. B., Chambers, D. W. & Burk, D. T. (1987) Vascularly orientated differentiation
gradient of osteoblast precursor cells in rat periodontal ligament: implications for osteoblast histogenesis
and periodontal bone loss. Journal of Periodontal Research, 22,461467.
Rose, G. G., Yamasaki, A., Pinero, G. J. & Mahan, C. J. (1987) Human periodontal ligament cells in vitro.
Journal of Periodontal Research, 22,20-28.
Saxon, A. & Higham, C. (1969) A new research method for economic prehistorians. American Antiquity, 34,
303-311.
Selvig, K. A. (1963) Electron microscopy of Hertwig’s epithelial sheath and of early dentin and cementum
formation in the mouse incisor. Acta Odontologica Scandanavica, 21, 175-186.
Selvig, K. A. (1964) An ultrastructural study of cementum formation. Acta Odontologica Scandanavica, 22,
105-120.
Selvig, K. A. (1965) The fine structure of human cementum. Acta Odontologica Scandanawica, 23,423441.
Shellis, R. P. (1982) Comparative anatomy of tooth attachment. In: The Periodontal Ligament in Health and
Disease (ed. by B. K. B. Berkovitz, B. J. Moxham & H. J. Newman), pp. 3-24. Oxford University Press,
Oxford.
Speth, J. D. & K. Spielmann (1983) Energy source, protein metabolism and hunter-gatherer subsistence
strategies. Journal of Anthropological Archaeology, 2, 1-3 1.
Spiess, A. E. (1976) Determining the season of death of archaeological fauna by analysis of teeth. Artic, 29,
5555.
Spiess, A. E. (1979) Reindeer and Caribou Hunters: an Archaeological Study. Academic Press, New York.
Spinage, C. A. (1973) A review of the age determination of mammals by means of teeth, with especial
reference to Africa. East African WildlifeJournal, 11,165-187.
Spinage, C. A. (1976) Incremental cementum lines in the teeth of tropical African mammals. Journal of
Zoology, London, 178,117-131.
Stallibrass, S. (1982) The use of cement layers for absolute ageing of mammalian teeth: a selective review of
the literature, with suggestions for future research and alternative applications. In: Ageing and Sexing
Animal Bones from Archaeological Sites(ed. by B. Wilson, C. Grigson & S. Payne), pp. 109-126. BAR (BS)
109, Oxford.
Stott, G. G., Sis, R. F. & Levy, B. M. (1982) Cementum annulation as an age criterion in forensic dentistry.
Journalof Dental Research,61,814-817.
Tchernov, E. (1984) Commensal animals and human sedentism in the Middle East. In: Animals and
Archaeology: 3. Early Herders and their Flocks (ed. J. Clutton-Brock & C. Grigson), pp. 91-115. BAR
S202. Oxford.
Thomas, D. C. (1977) Metachromatic staining of dental cementum for mammalian age determination.
Journal of Wildlife Management, 41,207-21 1.
Valla, F. R., Plisson, H. & Buxo I Capdevila, R. (1989) Notes preliminaires sur les fouilles en cours sur la
terrasse d’Hayonim. Paldorient, 15; 245-257.
Wada, K., Ohtaishi, N. & Haciya, N. (1978) Determination of age in the Japanese monkey from growth layers
in dental cementum. Primates, 19,775-784.
Yoneda, M. (1982) Growth layers in dental cementum of Saguinus monkeys in South America. Primates, 23,
460-464.