AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 91:401419 (1993)
Histological Reconstruction of Dental Development and Age at
Death of a Juvenile Paranthropus robustus Specimen, SK 63,
From Swartkrans, South Africa
M.C. DEAN, A.D. BEYNON, J.F. THACKERAY, AND G.A. MACHO
Department of Anatomy and Developmental Biology, University College
London, Gower Street, London WClE 6BT (M.C.D.); Department of Oral
Biology, Dental School, University of Newcastle upon Tyne, Framlington
Place, Newcastle upon Tyne, NE2 4BW fA.D.B.1; Department of
Palaeontology and Palaeoenvironmental studies, Transuaal Museum,
Pretoria, South Africa (J.F.T.); Department of Human Anatomy and Cell
Biology, The University of Liverpool, P.O. Box 147, Liverpool L69 3BX,
United Kingdom (G.A.M.)
KEY WORDS
Hominids, Enamel, Striae of Retzius, Cross
striations, Teeth, Growth
There has been disagreement about whether the earliest
ABSTRACT
hominids grew in a similar manner to great apes or modern humans. This has
important biological implications, since it may have been inappropriate to
apply modern human developmental standards to early hominids. The aim of
the present study was to combine data from replicas of tooth surfaces, computed tomographic (CT) scans, and radiographs with data from a histological
section of the canine crown, in order to provide a complete description of tooth
crown and tooth root development in a single early hominid specimen (SK 63).
Although partially destructive in nature, we have been able to determine the
most reliable data yet for aspects of dental development in an important
juvenile early hominid specimen. Appositional enamel formation time in the
permanent right canine was estimated at between 305 and 418 days, imbricational enamel formation time a t 819 days, and total crown formation time at
between 3.18 and 3.48 years. The most likely age at death was estimated a t
around 4 years with a range of ages calculated between 3.18 and 4.23 years
based on differences in timing of initial mineralization of the canine and
differences in appositional enamel formation times. Crown formation times of
the lower central and lateral incisors were estimated between 2.35-2.68 years
and 2.57-2.91 years, respectively. Crown formation time of the first permanent molar was estimated a t 2.4 years. Wear facets on the first permanent
molars indicate that gingival emergence had occurred sometime prior to
death, between 3 and 4 years of age. Estimates of root extension rates in the
first permanent molars and in the permanent incisors are fast, and either
within or above ranges of rates estimated for modern great apes. While we
recognize that data for one individual may not be representative of data for a
whole population of early hominids, the data for age at death, for age of M,
emergence, and for root extension rates presented here accord with those
known for modern great apes and fall beyond the known ranges for modern
humans. o 1993 Wiley-Liss, Inc.
The well preserved mandible of a juvenile
hominid (SK 63) was found by Robert Broom
and John Robinson at Swartkrans, South
Africa, in 1949 and attributed by them to
0
1993 WILEY-LISS. INC
Paranthropus crassidens. Within the last
1.7 million years the fossilized remains of
hominids, carnivores, and other animals
have accumulated in the dolomitic lime-
402
M.C. DEAN ET AL.
stone cave at Swartkrans. The stratigraphy
at the Swartkrans cave site is complex, since
periods of deposition have been followed by
erosional episodes. At least five depositional
units (Members 1-5) have been recognized
(Brain, 1988; Brain et al., 1988). Abundant
fossils were recovered by Broom and Robinson when lime-mining operations were in
full swing between 1948 and 1953. SK 63 was
recovered from the “Hanging Remnant” of
Member 1. Although dating each of the units
is difficult, it is thought on the basis of faunal
evidence that Member 1 dates to between
1.8 and 1.5 million years B.P. (Brain, 1988).
During the last few years certain juvenile
fossil hominids from East and South Africa
have been assigned an age at death. Direct
comparisons with developing modern human and great ape dentitions led Mann
(1975) to conclude that SK 63 and other juvenile fossil hominids from Swartkrans
(now usually attributed to Australopithecus
robustus or to Paranthropus robustus) were
about 6 years of age at emergence of their
first permanent molars and accordingly
were more similar to modern humans in this
respect. Recent studies relying on internal
and surface incremental markings on the
tooth enamel of early hominids have concluded that SK 63 and other early hominids
were nearer 3.5 years of age a t emergence of
their first permanent molars and are more
similar to modern great apes in this respect
(Bromage and Dean, 1985; Dean, 198713;
Beynon and Dean, 1988). Other studies
(Smith, 1986; Bromage, 1987; Conroy and
Vannier, 1987, 1991a,b) that have considered the pattern of sequences of tooth mineralization and emergence in early hominids
have not found evidence which suggests that
early hominids had prolonged periods of
growth and development. These and other
studies by Smith (1989a,b, 1991a,b, 19921,
which have taken fuller account of brain size
and patterns of life history variables in primates and hominids, have concluded, like
the studies of incremental markings in tooth
enamel, that early hominids had periods of
growth and development similar to those of
modern great apes.
However, previous studies on fossil hominids using tooth enamel structure have not
gone without criticism. The assumption that
perikymata on the surface of teeth represent
near weekly increments of around 8 days
(range 6-10 days) in early hominids has
been challenged (Mann et al., 1990). Mann
et al. (1990) have also challenged the relationship established by Pickerill (1913) for
modern human teeth between perikymata
and striae of Retzius. Furthermore, they
have challenged the evidence that suggests
that alternating varicosities and constrictions seen in scanning electron microscopy
(SEM) studies of fossil hominid enamel, or
cross striations (fine dark lines) across
enamel prisms seen in polarized light microscopy of enamel, are daily increments in
humans and apes. During the past few years
some of these criticisms have been answered
in the literature (Dean, 1987a; Beynon and
Dean, 1988, 1991; Bromage, 1991; Beynon,
1992) and recently, clearer documentation
has been presented in the literature about
histological techniques required to make
correct use of enamel incremental growth
markings in hominoid teeth (Beynon, 1987;
Boyde, 1989, 1990; Bromage, 1991; Dean
and Beynon, 1991a; Beynon et al., 1991;
Beynon, 1992).The present study is the first
that makes use of the partially destructive
procedure of preparing a histological section
of an early fossil hominid tooth. One objective was to test some of the assumptions
made in previous nondestructive studies on
early fossil hominid tooth enamel development. Two important conditions of this kind
of partially destructive investigation are
one, that valuable fossil teeth be removed
from their repository for a minimum period
of time and two, that they are returned completely reconstructed using modern dental
restorative materials and techniques looking (and measuring) just as they did when
they were removed.
SK 63 is a unique specimen in that one
histological section of the isolated canine
tooth is likely to provide information about
each of the contentious questions mentioned
above. This is mostly due to the fact that the
canine tooth, which has just completed its
crown formation, is unquestionably associated with a complete mandible and developing dentition where the first permanent molars have recently come into functional
occlusion.
No other australopithecine fossils retain
teeth that are as well suited to addressing
DENTAL DEVELOPMENT IN PARANTHROPUS ROBUSTUS
these questions. The anterior teeth of some
subadult australopithecine specimens are
useless for our purposes because their developing roots were damaged post mortem (and
therefore have no determinate length). Others cannot be sectioned because they are the
only known specimens of their type. Fortunately, canine teeth are well represented at
Swartkrans and an undamaged contralatera1 canine is preserved in the left mandibular corpus of SK 63. We would have liked t o
compare this Swartkrans specimen with one
from Sterkfontein, Sts 24 and 24a, which is
a seemingly similar representative of a juvenile Australopithecus africanus specimen
and one which closely resembles the Taung
juvenile in its dental development. However, some tooth roots are damaged in this
specimen and despite one opinion to the contrary (Grine, 1981) we suspect that the upper and lower isolated teeth and lower jaw of
the Sts 24 assemblage and the maxilla may
come from different individuals. This follows primarily from the fact that the upper
M1 has fewer occlusal wear facets than the
lower MI. In addition, the maxilla exhibits
signs of a generalized disease, juvenile periodontitis (Ripamonti, 1988), not discernible
in the mandible and the upper lateral incisor fits poorly into the appropriate bony
crypt in the maxilla. Other juvenile australopithecine teeth that might be usefully
compared with those of SK 63 are not available for study because they are unerupted
and thus inaccessible (Taung, SK 61, SK 62).
403
tional enamel formation in this canine
tooth; 4) to estimate the time of imbricational enamel formation and the total crown
formation time in the canine tooth; 5) to estimate the age a t death of the specimen; and
6) to estimate the crown formation time and
root extension rates of the first permanent
molars and permanent incisors and to provide data about the likely age of first permanent molar emergence in Paranthropus robustus.
DESCRIPTION OF SK 63
The developing dentition of specimen SK
63 has been described in the literature previously (Mann, 1975; Smith, 1991b; Conroy
and Vannier, 1991a,b). In this brief account
we make use of new radiographs, new CT
scans, and additional measurements to
highlight what we feel are important points
about dental development in SK 63.
Reasonably good measurements of developing root lengths in the incisors and first
permanent molars can be made in SK 63
either directly or from radiographs. In this
study we chose to measure incisor root
lengths directly, whereas M, root length
measurements were made from routine radiographs (corrected for magnification of the
image) rather than from our CT images. CT
studies have been shown to provide useful
information about the topography of developing teeth within fossil jaws (Conroy, 1988;
Conroy and Vannier, 1987, 1991a,b; Grine,
1991) as well as enamel thickness (Grine,
1991; Macho and Thackeray, 1992; Spoor et
AIMS OF THE STUDY
al., 1993). Recently, CT has also been emAll previous studies in which sections of ployed to estimate root formation stages and
fossil hominid teeth have been prepared, lengths in Plio-Pleistocene hominids (Conwere made on posterior teeth with a view to roy and Vannier, 1991a,b). However, CT is
answering questions about enamel thick- not ideal for resolving problems pertaining
ness. This study was designed to answer a to precise estimates of crown completion and
combination of biological questions relating root height measurements (Eubanks et al.,
to dental development in a single juvenile 1985; Magnusson, 1987; Ulrich et al., 1980).
specimen of Paranthropus robustus (SK 63). Fine measurements at the crown cervix and
The objectives of the present study were 1) root apex made with CT are likely to be inacto determine the number of cross striations curate. This follows because of partial volbetween adjacent striae of Retzius and es- ume averaging and the tapering in cervical
tablish the consistency of this count in a fos- enamel (which is below the critical distance
sil canine; 2) to establish that striae of Ret- of 1.1 mm required for taking CT measurezius close to the surface of the enamel are ments to an accuracy of k O . 1 mm) (Spoor et
associated with an identical number of al., 1993). In addition, problems relating to
perikymata on the enamel surface in fossil the interface of three structures of different
hominids; 3) to estimate the time of apposi- densities (enamel, dentine, and air) arise, so
404
M.C. DEAN ET AL.
Fig. 1. A Right and left halves of SK 63 seen from the buccal aspect; B: occlusal view of the assembled
specimen. Note the immature enamel at the cervix of the developing left second permanent molar and the
worn protoconid of the first permanent molars visible in A.
that “half maximum” measurements cannot
be employed (Spoor et al., 1993). For these
reasons the descriptions of developing teeth
within the jaw of SK 63 that follow, derive
largely from observations made using conventional radiographs.
SK 63 consists of a near complete immature mandible fractured at the symphysis
(Fig. 1). The fracture through the lingual
planum can be reliably joined such that the
two hemimandibles can be correctly aligned.
Bone loss buccally at the symphysis has exposed several developing permanent teeth
(Fig. 2). The left ascending ramus is most
complete and preserves the coronoid and
condylar processes. Only the angle of the
mandible is missing on the left. The right
ascending ramus is less complete but still
preserves the anterior border intact from
the retromolar region to the base of the coronoid process. The posterior border of the ascending ramus and the angle of the mandible are missing on this side as well as the
condyle and tip of the coronoid process. The
proportions of the mandible as a whole are
reminiscent of juvenile human mandibles
DENTAL DEVELOPMENT IN P M T H R O P U S ROBUSTUS
405
Fig. 2. The right central incisor crown and the fracture across the lingual cingulum (arrow) are shown
with the lateral incisor and permanent canine positioned in their cr,ypts.
(Skinner, 1978) although the ascending ramus is proportionally taller and broader and
the specimen as a whole is larger than human mandibles a t emergence of the first
permanent molar.
On the left, the deciduous canine, deciduous first molar, and deciduous second molar
are preserved in occlusion in the alveolar
bone. Each of these teeth shows wear exposing islands of dentine occlusally beneath the
position of former cusp tips. Wear on the
first deciduous molar is most heavy and the
whole of the buccal occlusal surface is worn
through to dentine although on the lingual
occlusal surface two small islands of dentine
exposure beneath former cusp tips have not
coalesced. On the right side of the specimen
only the distal portion of the deciduous canine crown is preserved but the whole tooth
root is present in the alveolar bone. The
right deciduous first and second molars are
also preserved in occlusion and show near
identical patterns of dentine exposure to
their counterparts on the left-hand side.
The permanent central incisor on the
right side of the specimen has a crown
height (measured on the buccal aspect) of
10.4 mm. Careful cleaning with acetone
however, revealed that the tooth crown was
separated from the root and lingual cervix
by a number of disassociated dentine and
enamel fragments positioned between a
fracture. As a result, the crown height lingually measured 13 mm from mamelon to
lingual cervix, greatly exceeding that buccally. While the crown of this tooth is complete buccally it is fractured through the lingual cervix and therefore incomplete here. A
portion of enamel cervix, 3 mm tall, exists on
the root of the right central incisor in the
alveolar bone. When glue and intervening
tooth fragments were cleaned away and the
406
M.C. DEAN ET AL.
superior and inferior portions of crown examined, they were found not to align in a
common long axis and not to fit with each
other at the fractured surfaces (Fig. 2). Reexamination of the crown morphology suggests that the present “mesial”margin of the
incisal edge is in fact more rounded than the
present “distal” margin and that all three
mamelons are set more towards the distal.
We suggest that the crown that has been
associated with the right tooth root and cervix is in fact the left central incisor crown of
SK 63, which for convenience had been attached to the root and cervix of the lower
right central incisor. Nevertheless, since the
lower right central incisor root and complete
cervix are inextricably fossilized to the alveolar bone of the specimen in situ, it is possible to obtain a reliable measurement of root
length, 3.9 mm from the bottom of the lingual cervix to the preserved margin of the
forming root apex distolingually (Fig. 2).
While the upper portion (of what we suggest
is the left central incisor tooth crown) remains fixed in place on the right central incisor root and cervix, it should be realized
that the emergence status of the right central incisor through the alveolar bone and
gingiva is likely to have been about 2 mm
lower than it presently appears, judged by
the position of the lingual cervix. Even so,
this is not enough to alter previous conclusions that the tooth had more than likely
emerged through the gingivae prior to
death.
Nothing of the root of the left central incisor remains in the specimen but both right
and left lateral incisors are partially exposed in their crypts in the alveolar bone.
The crown height of the left lateral incisor
can be measured (10.8 mm) and the root of
this tooth is 2 mm long. Reliable crown
height and root length measurements cannot be made on the right lower lateral incisor. The right permanent canine crown is
complete with minimal fracture of the
enamel margin buccally but more extensive
damage t o the lingual portion of the cervix.
The crown height measures 10.7 mm buccally. This tooth is separate from the specimen but can be placed in the distal portion of
its crypt in a reliable developmental position
low in the mandibular corpus (Fig. 2). The
left permanent canine remains inaccessible
within the mandibular corpus but its base
can be seen and we judge the tooth to be
undamaged buccally. From radiographs and
CT scans of the specimen we estimate that
the left canine may be between 0.5 and 1.0
mm taller than the right canine. The base of
the developing right first premolar can also
be seen in the mandible and we concur with
Conroy and Vannier (1991a) that crown
completion of this tooth was imminent. Both
second premolars can be seen on radiographs (Fig. 3) and CT scans and are tilted
distally in their crypts. The tilted base of the
right second premolar can be seen directly in
the damaged corpus. Crown heights are
given by Conroy and Vannier (1991a) as
10 mm.
Both first permanent molar crowns are, or
were, at the level of the occlusal plane. (A
clear interproximal wear facet on the distal
aspect of the left dm, indicates that the left
first permanent molar has shifted inferiorly
very slightly post mortem). Both lower first
permanent molars have considerable wear
facets on the tip and mesial aspect of the
mesiobuccal cusp and on the tip and distal
aspect of the mesiolingual cusp (Figs. 4,5).
In addition, a clear wear facet on the central
occlusal accessory cusp of the left first permanent molar emphasizes that these teeth
had been in functional occlusion for some
time prior to death. The enamel thickness
occlusally can be estimated at just over 2
mm from radiographs and CT scans using a
fixed window setting (Conroy and Vannier,
1991a). We estimate the root lengths of the
first permanent molars to be between 8.5
and 8.9 mm from lateral radiographs (Fig.
3), slightly more than the 8 mm measured by
Conroy and Vannier (1991a). This discrepancy may be due to problems associated
with CT and small measurements men-
Fig. 3. Lateral radiographs of SK 63. A Radiograph
was taken with the lingual aspect towards the film and
at a high KV. B: Radiograph was taken with the buccal
surface of the specimen against the film and at a lower
KV. There is good detail of the permanent teeth developing within the jaw but the right central incisor is completely “burned out” (A). The outline of the mandible is
clearly visible as is the right central incisor but there is
little detail of teeth within the jaw (B). Scale bar = 1cm.
DENTAL DEVELOPMENT IN PARANTHROPUS ROBUSTUS
407
408
M.C. DEAN ET AL.
Fig. 4.Buccal aspect of the left first permanent molar showing wear on the protoconid. Note also how
the tooth has shifted inferiorly post mortem relative to the dm,.
Fig. 5. SEMs of wear facets on the tip and mesial aspect of the protoconid and on the tip and distal
aspect of metaconid of the right first permanent molar of SK 63.
tioned above. Both second permanent molars are present in their crypts and can be
seen on radiographs and CT scans of the
specimen. Small gubernacular canals open
into the crypts from the retromolar fossae.
The left second permanent molar is visible
in its crypt through the damaged corpus and
this confirms that the crown is incomplete.
Immature enamel surrounds the developing
margin of the crown (Fig. 1) and has the
DENTAL DEVELOPMENT IN PARANTHROPUS ROBUSTUS
409
(W)light curing adhesive dental resin. A
500 Fm section was cut from this half of the
tooth while fixed to the slide and lapped
down to a thickness of 100 pm, lightly
etched with 0.5% phosphoric acid, cleaned,
dried, and mounted with DPX under a cover
slip in preparation for polarized light microscopy. The two cut halves of the canine
tooth were then cleaned and placed back
HISTOLOGICAL METHODS
into the Coltene President mold of the unAND RESULTS
damaged tooth. A series of color matched
Each of the exposed tooth crowns and light curing dental composite resins and
roots of SK 63 was replicated with a high shade tints (used routinely for anterior comresolution putty-wash impression technique posite restorations in clinical dentistry)
(Beynon, 1987) using Coltene President were used to restore the missing tissue from
putty and Coltene light body silicone paste. the canine tooth which was then returned to
The moulds were cast in Spurr Resin (a heat the Transvaal Museum (Fig. 6). Following
curing epoxy resin) and sputter coated with all microscopic investigations the mounted
gold for routine SEM work. Montages of mi- histological section of the tooth was also recrographs made a t 50 times magnification turned to the Transvaal Museum.
The histological section through the appowere prepared of the buccal surfaces of the
central incisor, the isolated right canine, the sitional enamel of the canine was 27%
left lateral incisor, and both first permanent thicker (calculated from linear measuremolars. Between 7 and 10 micrographs were ments) over the dentine horn of the tooth
used to construct each montage. Perikymata than it was when measured on the rightcounts were made from these montages in hand cut face of the tooth that included the
the manner described by Dean and Beynon axial crack (Fig. 7). However, despite this
(1991a). Both montages and perikymata slight obliquity the quality of the section
counts were made independently by two was considerably superior to one that would
authors. Seventy-five perikymata were have incoporated the crack along most of its
counted on the central incisor, 84 on the lat- length.
High-power montages of polarized light
eral incisor, 98 on the isolated canine, and
50, buccally, on the right first permanent micrographs were prepared of the whole of
molar. None could be identified on any other the cuspal and buccal enamel in the section.
aspect of the right or left first permanent Total striae counts were made within the
buccal imbricational enamel. Ninety-one
molars.
The isolated permanent canine was then striae were identified and counted in the imcompletely replicated again using Coltene bricational enamel. To test the assumption
President impression materials. An exact that each stria within the enamel is repreporcelain replica of the tooth was con- sented on the surface of the tooth by a
structed in the laboratory to record fine de- perikyma, counts were made of each betails of shade in each part of the crown and tween horizontal cracks visible in the secto safeguard, as far as possible, against ir- tion cervically and on the SEM montage of
reparable damage or accidental loss of the the buccal cervix. Nineteen striae and 19
tooth (Fig. 6). The original tooth was then perikymata were counted confirming the
partially embedded in Spurr Resin and sec- similarity between early fossil hominids and
tioned with an annular diamond saw as modern humans (Pickerill, 1913) in this reclose to the axial plane as possible. Since a spect (Fig. 8).
Appositional enamel formation times
longitudinal crack runs through part of the
axial plane, the cut face of the tooth with the were calculated from high-power montages
thinnest enamel over the cusp was lapped in three ways independently by two authors
down just lateral to the crack and then fixed (Fig. 9). A) Two individual prism paths were
to a microscope slide with an ultraviolet followed from the enamel dentine junction
characteristic “pavement cracking” appearance of hydrated immature enamel which
has not completed its maturation phase. No
crypts for the third permanent molars are
visible on radiographs, although a shallow
depression high in the retromolar fossa may
indicate incipient early development of a
tooth bud and crypt here.
410
M.C. DEAN ET AL
Fig. 6 . A Right permanent canine before sectioning. Note the axial crack running in the “best plane” of
section. B: Porcelain replica of the original. C, D: Buccal and inferior views, respectively, of the restored
tooth after removal of a 500 wm section.
at the dentine horn to the surface of the
enamel at the tip of the cusp and daily cross
striations marked along each path. A mean
value of two total counts equalled 414 days.
B) Two prominent striae within the cuspal
region were traced down into the lateral
enamel where prisms follow a straighter
path to the enamel surface. A high-power
montage was made between these accentu-
ated striae and a prism path defined from
the enamel dentine junction towards the
enamel surface to an equivalent enamel
thickness to that in the cuspal region. Daily
cross striations were then marked along two
adjacent prism paths where they could be
identified. Mean cross striation repeat intervals were calculated for inner, middle, and
outer enamel. The total length of the prism
DENTAL DEVELOPMENT IN P M T H R O P U S ROBUSTUS
411
RHS
Fig. 7. Line drawings of the two cut faces after removal of the section and of the section itself. The figure
illustrates how small differences in obliquity influence enamel thickness measurements and therefore
estimates of appositional enamel formation time.
paths that lay in the inner, middle, and
outer enamel was divided by the average
repeat interval for their region and the number of days of enamel formation in these
three regions summed. An average count of
two equalled 417 days. C) Following the
method of Risnes (1986), the cumulative
prism length representing the appositional
enamel formation period was divided by the
average prism cross striation repeat interval and multiplied by a factor of 1.3 to compensate for prism decussation. An estimate
of 423 days was calculated using this
method.
The average of these counts of 414, 423,
and 417 days for appositional enamel formation in this section is 418 days. However,
owing t o the slight obliquity of the section,
necessitated in order to avoid the axial
crack, it is likely that the appositional
enamel formation time is slightly overestimated. Linear measurements of enamel
thickness over the dentine horn in the
ground section were 27% greater compared
with that in the left block face. A prism path
reduced by 27% is more likely to represent
the true appositional enamel formation time
of the canine tooth. This is equal to 305 days.
Boyde (1990) and Dean and Beynon (1991a)
each report that counting cross striations in
enamel can be done with 10% accuracy.
In imbricational enamel where striae
could be unambiguously associated with
perikymata at the surface of the enamel,
counts of daily cross striations were repeatedly made between adjacent pairs of striae
(Fig. 10). Ten cross striations inclusive of
each adjacent stria were counted in different
regions of the tooth section which is equivalent t o 9 days enamel formation from stria to
stria. Previous data (Beynon et al., 1991;
Bullion, 1986; Dean, 1987a,b; Dean and
Beynon, 1991a) have indicated that this is
likely to be the same in all teeth from one
individual in both modern humans and
great apes.
The buccal cervix of the canine was fractured close to the cervical margin at a point
where the fractured enamel edge measured
0.3 mm in thickness. The interpolated angle
between the enamel dentine junction and
the enamel surface was 25", giving an estimated enamel loss in the cervical direction
of 0.64 mm. In the cervical enamel, striae
run nearly parallel with the enamel surface
(Fig. 8 ) and we estimate that there were not
*
412
M.C. DEAN ET AL.
Fig. 8. Polarized light micrograph showing striae at
the cervix of the right permanent canine together with a
SEM of the tooth surface made before sectioning. The
number of perikymata at the cervix between horizontal
cracks in the plane of section (black vertical line)
matches with the same number of striae seen in the
histological section a t the same place. Note also the
small amount of enamel fractured from the cervical edge
of the tooth and the oblique orientation of the striae
within the most cervical portion of the section.
more than four striae reaching the surface
in the missing cervical fragment. This is
equal to 36 days (0.1 years) of crown formation lost post mortem.
ness will be thinner than in the canine. Two
estimates of appositional enamel formation
times are presented, one based upon appositional enamel thickness in modern humans
of 0.5 years (182 days) and the other using
the corrected canine enamel thickness of
0.84 years (305 days) as an upper limit. The
central incisor shows 75 perikymata equivalent to 75 x 9 = 675 days of imbricational
enamel formation time, giving total crown
formation times of 2.35 years (857 days) or
2.68 years (980 days). These values reflect
lower and upper limits for crown formation
times, and a mean value of 2.52 years is also
presented (Table 2). Similar calculations in
the lateral incisor with 84 perikymata give
crown formation times of 2.57 years (938
days) or 2.91 years (1061 days), and a mean
value of 2.74 years (Table 3).
The right first permanent molar has 50
perikymata on the buccal aspect, which is
equal to 450 days imbricational enamel for-
Estimated crown formation times
Total canine crown formation time was estimated by summing the measured value of
418 days with the estimate for imbricational
enamel formation of 91 x 9 = 819 days, and
cervical enamel loss of 36 days, giving a total
of 1,273 days or 3.48 years. It is likely however, that this value for appositional enamel
formation is 27% higher than the true value,
owing to the slight section obliquity, giving a
corrected count for crown formation time of
3.18 years. Estimates for age at death and
other parameters are given using both of
these values (Table 1).
In the incisor teeth the thickness of
enamel over the dentine horn is unknown,
but it is anticipated that the enamel thick-
D E N T A L DEVELOPMENT IN PARANTHROPUS ROBUSTUS
413
Fig. 9. Drawings of the three prism paths A, B, and C described in the text and used to calculate
appositional enamel formation times.
mation. This perikymata count is similar to study on tooth development in four chimother counts on first permanent molar teeth panzees however (Chandrasekera et al.,
from Swartkrans (e.g., SK 834). Measure- 1993) initial mineralization of the canines
ments from the CT scans and work in was placed between 3 and 5 months postnaprogress on naturally fractured enamel sur- tally. Radiographic studies give different refaces from Swartkrans (Beynon and Wood, sults and Anemone et al. (1991) first observe
in preparation) indicate that the apposi- permanent canines radiographically at
tional enamel over the dentine horn of SK 63 around 12 months in chimpanzees. The deis close to 2.2 mm thick and that the cross velopmental affinities of Paranthropus rostriation repeat interval is 5 pm in this re- bustus show closer similarities to modern
gion. This is equivalent to 440 days apposi- humans than to great apes. Morphologitional enamel formation. Thus the total esti- cally, the anterior dentition in Paranthromated crown formation time of the first pus is very similar to modern humans and
permanent molar in SK 63 is 440 + 450 the morphology of the mandible in juvenile
specimens resembles humans closely (Skindays which equals 890 days or 2.4 years.
ner, 1978; Bromage, 1990; Dean and Beynon, 1991b). Several authors have also
Estimated age at death
noted the similarity in mineralization and
The estimated age a t death of SK 63 is emergence sequence between Paranthropus
equal to the canine crown formation time and modern humans (Mann, 1975; Dean,
summed with the period of time between 1985; Smith, 1986; Bromage, 1987; Beynon
birth and its initial mineralization. There is and Dean, 1988; Conroy and Vannier,
only one report in the literature of a canine 1991b). The best histological estimates in
already mineralizing at birth in a hominoid. humans place initial canine mineralization
Winkler et al. (1991) observed a permanent at between 0.25 years and 0.5 years (Logan
upper canine mineralizing at birth in an and Kronfeld, 1933). Gustafson and Koch
orangutan. Our own observations from his- (1974) in a study that combines data from 20
tological sections of complete gorilla and other studies, provide a mean age of 0.42
orangutan dentitions (Beynon et al., 1991) years and a range from 0.33-0.55 years. Rasuggest that canine mineralization may be- diographic studies by Moorrees et al. (1963)
gin in great apes between 4 and 10 months suggest mean age of initial mineralization of
postnatally. In a subsequent histological the permanent canine occurs at 0.6 or 0.5
414
M.C. DEAN ET AL.
Fig. 10. Polarized light micrographs of cross striations between adjacent striae coming to the surface in
three different positions on the buccal aspect of the section. Ten cross striations can be counted from stria
to stria inclusive (arrowed in five fields of view) indicating 9 days enamel growth between adjacent striae.
Original magnification 250 times. Cross striation repeat interval is 5 pm on average in these fields of
view.
TABLE 1. Canine crown formation times, estimated times
of death, first molar root formation times, and root
extension rates (to form 8,700 p m of root)
Canine crown formation time (year) 3.18l 3.48 3.48
Delay after birth before onset of
0.25
0.50 0.75
calcification (year)
Calculated age at death (year)
3.43
3.98 4.23
M, root formation time (year)
0.99
1.54 1.79
15.5 13.3
24.1
Root extension rate (Wndday)
'
Canine crown formation time includes corrected appositional enamel
component.
years (1 sd = 0.1 year) and another radiographic study by Fanning and Brown (1971)
documents that 3% of 41 males and 15 females were mineralizing their canines at
0.29-0.37 years, respectively, and that 97%
of the same sample were forming their canines a t 1.21 and 1.02 years, respectively.
Radiographic observations and even some
dissection studies however, cannot document the first days or even weeks of miner-
TABLE 2. Central incisor crown formation times
(maximum, mean, and minimum), three calculated
ages at death, total time available to form 3,900 Wm of
root, and calculated root extension rates (maximum,
median. minimum)
I, crown formation time (year)
Age at death
Available root formation time
(year)'
Root extension rate (&&day)
2.68
3.43
0.25
42.7
2.52
3.98
0.96
11.1
2.35
4.23
1.38
7.7
'Assuming a delay of 0.5 years before onset of root formation
alization and at best the earliest observation
on a radiograph or at dissection ofa mineralizing tooth implies that initial mineralization had begun some time prior to the time of
observation.
The interval between birth and the onset
of mineralization of the canine in fossil hominids is unknown, but based upon the evidence cited above in modern humans and
DENTAL DEVELOPMENT IN PARANTHROPUS ROBUSTUS
TABLE 3. Lateral incisor crown formation times
[maximum, mean, and minimurn], three calculated
ages at death, total time available to form 2,000 Frn of
root, and calculated root extension rates [maximum,
median, minimum)
415
in the central and lateral incisors are presented in Tables 2 and 3, using minimum,
median, and maximum ages at death, and
assume that there was a delay of 0.5 years
I, crown formation time (year)
2.91
2.74
2.57 before the onset of initial mineralization. In
Age at death (year)
3.43
3.98
4.23
the central incisor (Table 2) the values range
Available root formation time
0.02
0.74 1.16
from 42.7 pmlday at the youngest age to
(year)’
Root extension rate lumldavl
274.0
7.4
4.7
11.1 and 7.7 pmlday in the median and maximum estimates. The fastest value is more
‘Assuming a delay of 0.5 years before onset of root formation.
than two times greater than the maximum
coronal dentine extension rate reported in
great apes it appears probable that this oc- insectivores (Shellis, 1984). This suggests
curred in the range of 0.25 and 0.75 years, that the minimum age is too low.
The values of 11.1 and 7.7 p d d a y are
with an estimated mean of 0.5 years. This
range was used with the three estimates of close to the values in modern great apes of
crown formation times to derive a range of 11.7 and 12.2 p d d a y (Beynon et al., 1991)
estimates of age a t death from 3.453.98 to and much higher than those rates reported
4.23 years (Table 1) in specimen SK 63. The for initial root formation in modern humans
lowest value was obtained using the short- of between 2.85 p d d a y and 5 pmlday (Dean
est (corrected) crown formation time and the and Beynon, 1991a; Liversidge, 1993). The
shortest delay in onset time. The “median” lateral incisor shows a broadly similar disvalue is the calculated crown formation time tribution of estimates with a n unrealistic essummed with the delay of 0.5 years in onset timate of 274 p d d a y at the earliest proof mineralization. The highest value for age posed age at death. The estimates for the
at death was calculated using the highest median age at death (3.98 years) gives a
crown formation time and the maximum value of 7.4 p d d a y whilst the maximum
age at death, 4.23 years, gives relatively low
likely delay in onset of mineralization.
values of 4.7 p d d a y . (It is likely that the
Estimated root extension rates
first part of the I, root forms more slowly
The first molar has an estimated root than the rest of the root, but this lateral
length of 8,700 pm (this being the mean incisor value, which is low in comparison to
value of two measurements made from the the central incisor and first permanent molateral radiographs). Assuming a crown for- lar root extension rate values, gives further
mation time of 2.44 years this gives periods support to the conclusion that a median
of 0.99, 1.54, or 1.79 years (Table 1) to form value of around 4.0 years is a valid estimate
this length of root using values for ages a t for age at death in SK 63.)
death based on minimum, median, and maximum values derived from the canine data.
DISCUSSION
These different estimates can be used to calAppositional enamel formation time
culate first molar root extension rates rangThe data presented in this study are the
ing between 13.3 and 24.1 pmlday, with a
median value of 15.5 p d d a y , which is first on appositional enamel formation
slightly higher than values calculated for times in a fossil hominid anterior tooth. The
root extension rates in gorilla molar teeth of corrected value of 305 days or 0.85 years
12.4 and 13.3 pmlday (Beynon et al., 1991). exceeds estimates of 0.5 years made for fosThe root extension rates in the incisor sil hominid incisor teeth (Bromage and
teeth are less secure owing to uncertainties Dean, 1985) and also estimates in a modern
in appositional enamel formation times, in- human lower lateral incisor tooth (245 days
tervals between birth and the onset of initial or 0.67 years, Dean and Beynon, 1991a). It
mineralization, coupled with the ranges in was perhaps to be expected that apposiestimates for crown formation times and age tional enamel formation time in Purunthroa t death. Estimates of root extension rates pus canines would be somewhat greater
416
M.C. DEAN ET AL
than in modern human incisors. However,
the data for appositional enamel formation
time in SK 63 demonstrate that it only exceeds that of the human upper central incisor studied by Boyde (1990) by a few weeks
and that in the human lower lateral incisor
cited above by 8 or 9 weeks. Our own estimate for appositional enamel formation
time in a modern human canine of 375 days
(Dean and Beynon, 1991a) was done in the
same way as method A in this study.
In each of the two histological studies of
human upper central and lower central incisor teeth, mineralization of the incisors began within a month of birth, as judged by
cross striation counts from the neonatal line
in the M1. The estimated age of initial mineralization of the permanent human canine
from Spitalfields, specimen 2179, was between 2 and 3 months after birth. Future
histological studies on human permanent
incisors and canines may demonstrate that
radiographic and dissection studies overestimate the delay postnatally in initial onset
of mineralization of human permanent anterior teeth. In both upper and lower incisors
in these studies 8 or 10 months elapsed between birth and the first imbricational
enamel formation compared to 12 months in
the permanent canine. Data in Figure A3
(Boyde, 1990) for a human upper central incisor tooth shows that relative to the neonatal line in the first permanent molar, imbricational enamel formation began at about
300 days postnatally.
Previous data on a thick enamelled premolar tooth attributed to Paranthropus boisei provided evidence of a 500 day or 1.36
year period for appositional enamel formation in a posterior fossil hominid tooth (Beynon and Dean, 1987).We also cite here work
in progress that suggests a 440 day or 1.2
year appositional enamel formation period
in 2.2 mm thick Paranthropus robustus first
permanent molar enamel (Beynon and
Wood, in preparation). Clearly, more histological data on modern human appositional
enamel formation times and more data from
naturally fractured anterior fossil hominid
teeth are needed to build up a good picture of
variation in appositional enamel formation
times generally. It is possible that data from
CT scans may be able to contribute to calculations of this time period in fossil hominid
anterior teeth where the appositional
enamel is thicker than 1.1 mm, although
they may not be used to accurately assess
developmental stages where thin tissues
taper to dimensions smaller than this (Spoor
et al., 1993).
Age at death
Estimates of age at death for a single individual cannot provide data about average
ages at death in a population. However, they
can be used to test previous claims about age
at death in the same individual. The present
data do not support an age at death of between 6 and 7 years of age for SK 63 (Mann,
1975). Our estimate of 3.45-4.23 (median
3.98) years is considerably less than this.
This estimate around 4 years is, nevertheless, greater than the estimate of 3.2 years
for SK 63 made by Bromage and Dean
(1985) and is more reliable than this first
estimate based only on incisor perikymata
counts. Errors in certain of the histological
techniques we use here are probably less
than 10% (Boyde, 1990; Dean and Beynon,
1991a) but the range of age at death based
on extremes of canine mineralization (0.250.75 years) would almost certainly subsume
all of these errors.
Age of M, emergence
Between 1 and 2 mm of enamel has been
worn from the tips of the mesiobuccal cusps
of both first molars in SK 63, judged by the
height of the other buccal cusps on these
teeth (Fig. 4). It is not possible to make an
accurate estimate of the time this might
have taken but it indicates that these teeth
were in functional occlusion for some time
prior to death. We think this time period is
likely to be months rather than days, weeks,
or years based on data in Dean et al. (1992)
for great ape tooth wear. Therefore, we consider that gingival emergence occurred in
SK 63 some 2-4 months before death. Smith
(1989a,b, 1991a,b, 1992) has demonstrated
that M1 emergence in primates is a very
significant developmental event. In every
way this estimate for the time of M, emergence in SK 63 (approximately between the
DENTAL DEVELOPMENT IN PARANTHROPUS ROBUSTUS
ages of 3 and 4 years) accords with available
data for patterns of development observed in
living great apes and does not fall within the
range of any reliable first permanent molar
emergence data recorded for Homo sapiens.
Crown formation times
417
tension rates were not as fast as later root
extension rates and so exceed an average
value.
More work needs to be done on the relationship between completed root lengths in
primate teeth and the time available to grow
these roots. If the hypothesis that only a certain time is available to grow roots within
the total growth period is correct (Dean and
Wood, 1981) then longer roots will have to
form faster than shorter roots in animals
with similar periods of growth and development. The long roots of Paranthropus may
form very much more quickly than the
shorter roots of, for example, Australopithecus ufarensis, despite a presumably similar
period of growth and development.
Anterior tooth crown formation times in
SK 63 are short. While radiographic studies
of modern humans can be found that include
times for canines of 3.2 years and ranges for
incisors of between 2.3 and 2.9 years we
doubt that direct observations of tooth
germs from individuals of known age at
death (Liversidge et al., 1993) or histological
studies of modern humans (Beynon and
Reid, in preparation) will include many
crown formation times as short as these. It
is highly likely that the average time of
CONCLUSIONS
crown completion for modern human lower
permanent canines is nearer to 5 or 6 years
By using incremental markings in the
and that for incisors greater than 4 years. enamel of the permanent right mandibular
Histological estimates of ape anterior tooth canine of SK 63 (a juvenile fossil hominid
formation times greatly exceed the times es- attributed to Paranthropus robustus), we
timated for SK 63. In chimpanzees these fall have been able to calculate the likely range
between 4.6 and 5.6 years for incisors and of time of crown formation. Using this range
between 4 and 7 years for canines (Beynon of crown formation time for the canine toet al., 1991; Chandrasekera et al., 1993). Ra- gether with estimates of the range for the
diographic data for chimpanzees (Anemone time between birth and initial canine mineret al., 1991) that provide incisor crown for- alization (and an estimate of enamel lost
mation times similar to SK 63, we think are post mortem), we have been able to estimate
incorrect, and result from difficulties defin- an age at death for this specimen of between
ing the stage of crown completion on lateral 3.18 and 4.23 years. We argue that an age of
skull radiographs of living animals.
about 4 years is the most likely age at death.
First permanent molar emergence probably
Root extension rates
occurred close to 3.5 years of age in this indiThe best data for the time it takes to form vidual, judging from wear facets visible on
the first permanent molar root in great apes both lower M,s. Estimates for root extension
come from Anemone et al. (1991). This longi- rates on the first permanent molars and
tudinal study demonstrates that it takes lower incisors are the first given for any
around 3 years to form MI roots in captive early fossil hominids. These fall close to estichimpanzees. If this same time were avail- mates of root extension estimated for great
able to grow the first permanent molar root apes. None of the data presented here offer
in Paranthropus robustus, which may be be- support for a previous hypothesis, based on
tween 18 and 20 mm long when completed, tooth wear and on comparative stages of
then the average rate of growth (or root ex- dental development (Mann, 19751, which
tension rate) would be between 16.4 and suggested that this specimen was aged be18.3 p d d a y . This range is close to that cal- tween 6 and 7 years of age at death. If other
culated in this study (13.3-24.1 p d d a y ) for juvenile early fossil hominids can consisthe average extension rate of the first 8 or 9 tently be shown to have erupted their first
mm of M, root of SK 63. It may be in early permanent molars at this young age, it
hominids (as in humans) that early root ex- would seem reasonable to presume that they
M.C. DEAN ET AL.
418
resembled modern great apes in their period
of dental and general growth and development.
ACKNOWLEDGMENTS
We are grateful to Don Reid and Ian Bell
for preparing the ground section of SK 63
and for their skilled technical assistance as
well as to Ian Barnes and Mark Pickersgill
for constructing a porcelain replica of the
canine. We are also grateful to Bob Brain,
David Panagos, and the staff of the Transvaal Museum, Pretoria who helped with this
project and made it possible. We would like
to thank Rashida Harman and all the staff
in the Radiology Department of the Hilbrow
Hospital, Johannesburg for allowing us to
make use of their CT and X-Ray facilities.
We would also like to express our thanks to
Fred Grime and to the other referees for
their helpful comments on the manuscript.
This study was financed by The Royal Society, The Leakey Foundation, and The Science Based Archaeology Board of the SERC.
LITERATURE CITED
Anemone RL, Watts ES, and Swindler DR (1991) Dental
development of known age chimpanzees Pun troglodytes (Primates Pongidae) Am. J . Phys. Anthropol.
86:229-242.
Beynon AD (1987) Replication technique for studying
microstructure in fossil enamel. Scanning Microsc.
1:663-669.
Beynon AD (1992) Circaseptan rhythms in enamel development in modern humans and Plio-Pleistocene
hominids. In P Smith and E Tchernov (eds.): Structure, Function and Evolution of Teeth. London and
Tel Aviv: Freund Publishing House Ltd., pp. 295-309.
Beynon AD, and Dean MC (1987) Crown formation time
of a fossil hominid premolar tooth. Arch. Oral Biol.
32:773-790.
Beynon AD, and Dean MC (1988) Distinct dental development patterns in early fossil hominids. Nature
335.509-514.
Beynon AD, and Dean MC (1991) Hominid dental development. Nature 351:196.
Beynon AD, Dean MC, and Reid DJ (1991) Histological
study on the chronology of the developing dentition in
gorilla and orangutan. Am. J . Phys. Anthropol. 86:
189-204.
Boyde A (1989) Enamel. In A. Oksche and L. Vollrath
(eds.): Handbook of Microscopic Anatomy, Vol. V/6,
Teeth. Berlin: Springer-Verlag, pp. 309473.
Boyde A (1990) Developmental interpretations of dental
microstructure. In C Jean DeRousseau (ed.): Primate
Life History and Evolution. New York Wiley-Liss,
Inc., pp. 229-267.
Brain CK (1988) New information from the Swartkrans
cave of relevance to “robust”australopithecines. In FE
Grine (ed.): Evolutionary History of the “Robust”Australopithecines. New York: Aldine de Gruyter, pp.
311-316.
Brain CK, Churcher CS, Clark JD, Grine FE, Shipman
P, Susman RL, Turner A, and Watson V (1988) New
evidence of early hominids, their culture and environment from the Swartkrans cave, South Africa. s. Afr.
J . Sci. 84:828-835.
Bromage TG (1987) The biological and chronological
maturation of early hominids. J . Hum. Evol. 16:257272.
Bromage TG (1990) Ontogeny of the early hominid face.
J . Hum. Evol. 18:751-773.
Bromage TG (1991) Enamel incremental periodicity in
the Pig-Tailed macaque: A polychrome fluorescent labeling study of dental hard tissues. Am. J . Phys. Anthropol. 86:205-214.
Bromage TG, and Dean MC (1985) Re-evaluation of the
age at death of Plio-Pleistocene fossil hominids. Nature 317.525-528.
Bullion SK (1986) The biological application of teeth in
archaeology. PhD thesis, University of Lancaster.
Chandrasekera MA, Reid DJ, and Beynon AD (1993)
Dental Chronology in chimpanzee Pun troglodytes. J.
Dent. Res. 72:729.
Conroy GC (1988) Alleged synapomorphy of the MlL1
eruption pattern in robust australopithecines and
Homo: Evidence from high resolution computed tomography. Am. J. Phys. Anthropol. 75:487-492.
Conroy GC, and Vannier MW (1987) Dental development of the Taung skull from computerized tomography. Nature 329:625-627.
Conroy GC, and Vannier MW (1991a) Dental development in South African australopithecines. Part 1:
Problems of pattern and chronology. Am. J . Phys. Anthropol. 86:121-136.
Conroy GC, and Vannier MW (1991b) Dental development in South African australopithecines. Part 11:
Dental stage assessment. Am. J . Phys. Anthropol.
86:137-156.
Dean MC (1985) The eruption pattern of the permanent
incisors and first permanent molars in Austrulopithecus (Parunthropus)robustus. Am. J . Phys. Anthropol.
67:251-257.
Dean MC (1987a) Growth layers and incremental markings in hard tissues; a review of the literature and
some preliminary observations about enamel structure in Purunthropus boisei. J . Hum. Evol. 16:157-172.
Dean MC (1987b) The dental developmental status of
six juvenile fossil hominids from Koobi Fora and
Olduvai Gorge. J . Hum. Evol. 16:197-213.
Dean MC, and Beynon AD (1991a) Histological reconstruction of crown formation times and initial root
formation times in a modern human child. Am. J .
Phys. Anthropol. 86:215228.
Dean MC, and Beynon AD (1991b) Tooth crown heights,
tooth wear, sexual dimorphism and jaw growth in
hominoids. 2. Morphol. Anthropol. 78t425-440.
Dean MC, Jones ME, and Pilley J R (1992) The natural
history of tooth wear, continuous eruption and perio-
DENTAL DEVELOPMENT IN P M T H R O P U S ROBUSTUS
dontal disease in wild shot great apes. J. Hum. Evol.
22t23-39.
Dean MC, and Wood BA (1981) Developing pongid dentition and its use for ageing individual crania in comparative cross-sectional growth studies. Folia Primatol. 36:111-127.
Eubanks BA, Cann CE, and Brant-Zawadzki M (1985)
CT measurements of the diameter of spinal and other
bony canals: Effects of section angle and thickness.
Radiology 157:243-246.
Fanning EA, and Brown T (1971) Primary and permanent tooth development. Austr. Dent. J . 16:4143.
Grine FE (1981)A new composite juvenile specimen of
Austrulopithecus africanus from Member 4 Sterkfontein Formation, Transvaal. Ann. S. Afr. Mus. 84:169201.
Grine FE (1991) Computed tomography and measurements of enamel thickness in extant hominoids: Implications for its palaeontological application. Palaeontol. Afr. 28:6149.
Gustafson G, and Koch G (1974) Age estimation up to 16
years based on dental development. Odont. Revy.
25:297-305.
Liversidge HM, (1993) Human tooth development in a n
archaeological population of known age. PhD Thesis
University of London.
Liversidge HM, Dean MC, and Molleson TA (1993) Increasing Human Tooth Length Between Birth and 5.4
years. Am. J. Phys. Anthropol. 90:307-313.
Logan WHG, and Kronfeld R (1933) Development of the
human jaws and surrounding structures from birth to
the age of fif'ceen years. J. Am. Dent. Assoc. 20r37S427.
Macho GA, and Thackeray JF (1992) Computed tomography and enamel thickness of maxillary molars of
Plio-Pleistocene hominids from Sterkfontein, Swartkrans and Kromdraai (South Africa): An exploratory
study. Am. J. Phys. Anthropol. 89:133-143.
Magnusson A (1987) Object size determination at computed tomography. Upsala J . Med. Sci. 92:277-286.
Mann AE (1975) Some Palaeodemographic Aspects of
the South African Australopithecines. Philadelphia:
University of Pennsylvania Publications.
Mann AE,Lamp1 M, and Monge M (1990) Patterns of
ontoeenv in human evolution: Evidence from dental
deveiopment. Yrbk. Phys. Anthropol. 33:111-150.
419
Moorrees CFA, Fanning EA, and Hunt EE (1963) Age
variation of formation stages for ten permanent teeth.
J. Dent. Res. 42:1490-1502.
Pickerill HP (1913) The structure of enamel. Dent. Cosmos 55:969-968.
Ripamonti U (1988) Palaeopathology in Australopithecus africanus: A suggested case of a 3 million year old
prepubertal periodontitis. Am. J. Phys. Anthropol.
76:197-210.
Risnes S (1986) Enamel appositional rate and the prism
periodicity in human teeth. Scand. J . Dent. Res.
94:394404.
Shellis RP (1984) Interrelationships between growth
and structure of enamel. In RW Fearnhead and S
Suga (eds.): Tooth Enamel IV.Amsterdam: Elsevier,
pp. 467-471.
Skinner MF (1978) Dental maturation, dental attrition
and growth of the skull in fossil hominidae. PhD Thesis, University of Cambridge, UK.
Smith BH (1986) Dental development in Australopithecus and early Homo. Nature 323:327-330.
Smith BH (1989a) Dental development a s a measure of
life history in primates. Evolution 43r683-688.
Smith BH (198913)Growth and development and its significance for early hominid behaviour. Ossa 14:63-96.
Smith BH (1991a) Age at weaning approximates age at
emergence of the first permanent molar in nonhuman
primates, abstracted. Am. J . Phys. Anthropol. Suppl.
12:163-164.
Smith BH (1991b) Dental development and the evolution of life history in Hominidae. Am. J . Phys. Anthropol. 86:157-174.
Smith BH (1992) Life history and the evolution of human maturation. Evol. Anthropol. 1:134-142.
Spoor CF, Zonneveld FW, and Macho GA (1993) Linear
measurements of cortical bone and dental enamel by
computed tomography: Applications and problems.
Am. J. Phys. Anthropol. (this issue).
Ulrich CG, Binet EF, Sanecki MG, and Kieffer SA (1980)
Quantitative assessment of the lumbar spinal canal
by computed tomography. Radiology 134:137-143.
Winkler LA, Schwartz J H , and Swindler DR (1991) Aspects of dental development in the orangutan prior to
eruDtion of the Dermanent dentition. Am. J . Phvs. Anthropol. 86:255-272.