- Email: [email protected]
Crown-formation time of a fossil hominid premolar tooth
0003~9969187 53.00 +O.OO
~rchs oral Bid.Vol.32,No. II,pp.773-780, 1987
Copyright C 1987 Pngamon Joumab Ltd
Printed in Great Britain. All rights resewed
CROWN-FORMATION TIME OF A FOSSIL HOMINID PREMOLAR TOOTH A. D. BEYNON' and M. C. DEAN’ ‘Department of Oral Biology, The Dental School, Framlington Place, Newcastle upon Tyne NE2 4BW and %epartment of Anatomy & Embryology, University College London, Gower Street, London WClE 6BT, England, U.K. Summary-Studies using surface or internal enamel growth indicators in hominids have suggested that crown-formation times were shorter than those in modem man. The crown-formation time in a robust australopithecine premolar tooth was calculated by counting enamel cross-striations, which correspond to daily increments of formation, on a replica of the fractured internal enamel surface of cuspal enamel using scanning electron microscopy. Cervical enamel completion time was estimated using other growth indicators including striae. and using measured and calculated cross-striation repeat intervals, giving a completion time of approx. 2.4 yr. This is much shorter than reported premolar crown formation times in modem man. These findings support the concept of an abbreviated period of dental development, with implications on the duration of the growth period in early hominids.
INTRODUCTION reliable data about the timing of hominid dental development it has been customary to age juvenile fossil hominid jaws and developing teeth on the basis of modem human and pongid dental erup tion sequences. Mann (1975) compared the pattern of dental development in four juvenile mandibles of Australopithecus robustus from South Africa with those patterns found in modem man and chimpanzee. He noted close similarities with developmental sequences in man and inferred a longer postnatal development period in hominids compared with pongids. At that time, however, there was no detailed information on the chronology of dental development in pongids; that was described in 1981 by Dean and Wood who noted that the crown formation times in pongids were broadly similar to those in man, but that in general pongid teeth erupted with less root formed; there was evidence of a faster rate of root formation in pongids. Incisor teeth erupted much later, nearer to second molars than first molars. Dean (1985) t-e-investigated a claim by Broom and Robinson (1951) that the eruption pattern of the permanent incisors and first permanent molars in robust australopithecines (A. robustus) was the same as that in man. He found that the permanent incisors and first molar erupted at a similar stage of development to that in man, whereas specimens attributed to A. africanus or afarends showed a pattern of eruption similar to that of pongids. These studies only provide information about the relative timing of dental developmental events during the growth period. However, Bromage and Dean (1985) and Beynon and Wood (1987) have provided data for crown formation times in early hominids. Bromage and Dean counted the numbers of perikymata on the labial surface of incisor teeth of early hominids. These structures are the surface manifestations of striae of Retxius, and have a periodicity of approx. seven to eight days in modem man (Gysi, 1939; Newman and Poole, 1974). They showed that perikymata on the surfaces of teeth of South African Without
robust australopithecines were fewer and more widely-spaced in the cervical region, suggesting a faster rate of incisor crown formation when compared with modem man, A. africanus and A. afare&s. They used this new data to prepare revised estimates of chronological age at death for several important hominid specimens. Beynon and Wood (1987) presented estimates for the duration of crown formation in molar teeth in East African hominids, based upon the degree of slope of incremental lines, and cross-striation repeat intervals in enamel of early Homo and robust australopithecines, concluding that molar crown-formation times were similar to or shorter than those in modem man. These estimates were derived from reconstructions of striae of several individual teeth and used composite values for crossstriation periodicities taken from replicas of the enamel surfaces, in some cases, of different teeth. The purpose of the present study is to report on a premolar tooth from a robust australopithecine in which it was possible to count cross-striations through the full thickness of occlusal enamel, and also to estimate the numbers of striae in the cervical enamel of the same specimen which improves the accuracy of estimation of crown-formation time for a single tooth. MATRRIAlSANDMRTHOD§ The tooth specimen was an unworn maxillary premolar (LP’) KMN-ER 733D housed in the National Museum of Kenya. The crown was complete and some root had formed, judged by the thickness of coronal dentine. The specimen was fractured axially in a me&-distal direction, and transversely at the approximate level of the cervical margin, damaging the most cervical 0.5-0.7mm of enamel (Plate Fig. I). The specimen was immersed in absolute ethanol (Beynon and Wood, 1986) and viewed with horizontally-polarized incident light, with an analyser over the objective lens of a Wild stereomicroscope to enhance the visualization of striae of Retzius. Striae were visible on the occlusal
773
774
A. D. BEYNONand M. C. DEAS
Imm
Fig. 4. Diagram showing examples of distinct striae (solid lines). and less distinct striae (dashed lines). The interpolated boundary between appositional and imbricational enamel is indicated (-.-.-). Enamel prism direction is indicated as dotted lines.
and cervical aspects of the crown (Plate Figs 2 and 3)
and a master tracing of the enamel outline was made at a magnification of x 50. Photographic negatives of the original specimen were projected on the tracing at the same magnification, and the course of distinct striae were transferred to the master tracing as solid lines (Text Fig. 4). Incomplete striae are indicated in broken lines, and the course of enamel prisms are indicated as dotted lines broadly perpendicular to the enameldentine junction (EDJ; Fig. 4). Crown enamel formation can be divided into two descriptive developmental stages (Beynon and Wood, 1987). The first cuspal or appositional stage corresponds to the production of full thickness enamel over the cusp tip, during which stage the enamel is being secreted in successional layers over the whole surface of the immature crown, and striae of Retxius do not reach the tooth surface. The second or imbricational (after Pickerill, 1913; from L. intbrex tile; overlapping) stage involves the asymmetric deposition of enamel on the sides of the crown, with successive increments associated with surface perikymata extending cervitally to complete the final crown height. The boundary between the appositional and imbricational stages is indicated by the discontinuous heavy line in Fig. 4. The fractured surface was replicated, using a twostage silicone-rubber impression technique, and a replica was made with Spurr resin. This methodology has been assessed for dimensional accuracy using replicas of an engraved incident-light micrometer, and a vernier eyepiece micrometer, and is accurate to within 1 per cent. It is capable of reproducing detail down to 0.2pm (Beynon, 1987). The replica was studied using a Cambridge S600 scanning electron microscope @EM).
Enamel
RESULTS above the dentine horns measured 2.5 mm
in thickness. Prisms showing cross-striations were clearly identifiable on the replica of the fractured enamel surface and it was possible to count all the cross-striations between the EDJ over the right dentine horn and the unworn occlusal surface (Plate Fig. 5), giving a figure of 500 f 3 counts by two independent observers on three separate occasions. The cross-striation repeat interval increased steadily from the EDJ to the external surface. Counts were made in five 0.5 mm lengths, with average values of 4.0 (innermost l/5), 4.3, 5.2, 6.0 and 6.5pm (outermost l/5) being obtained. Cross-striations were much less conspicuous in imbricational enamel, and it was only possible to obtain estimates in the outer l/5 of cervical enamel at the level where regular striae were present (Fig. 3). Values obtained were 4.7 f 0.5 pm in seven separate microscopic fields. Regular striae were visible in the cervical enamel (Fig. 3) and it was possible to identify 20 adjacent striae, in the mid-cervical enamel, which could be related at succeeding cervical levels, allowing a reconstruction of total striae in cervical enamel to be made (Text Fig. 6, see caption for details). We estimate that there were nine missing striae between the occlusal limit of the visible striae and the boundary between appositional and imbricational enamel; and 15 in the remaining cervical enamel. These estimates summed with the 20 visible striae indicate the presence of approx. 44 striae in imbricational enamel. The adjacent striae in the cervical enamel were fairly regularly spaced (Fig. 3). Measurements on the photomicrograph of the intervals between striae were made along the prism axis, which ranged from 34.2
Hominid crown-formation to 31.4 pm between adjacent striae. Striae could not be clearly distinguished in this region on replicas using the SEM.
775
time
/ l
/I
DI!XUSSION It is generally accepted that prism cross-striations represent daily increments of enamel growth (Asper, 1916; Gustafson, 1959; Osborne, 1973; Boyde, 1976). Weber and Glick (1975) suggested that crossstriations are optical artifacts in thick ground sections, but scanning electron microscopy of fractured enamel surfaces (Boyde, 1976) has revealed alternating varicosities and constrictions along prisms with a periodicity of 4-8 pm. SEM studies using backscattered electron imaging modes (Boyde, 1979; Boyde and Jones, 1983) on polished longitudinal enamel sections showed a rhythmic variation in atomic-number contrast of a similar periodicity to the constrictions seen on fractured surfaces, suggesting differences in chemical composition of the inorganic phase of enamel formed during the circadian cycle. Some experimental evidence also confirms the likely circadian nature of enamel cross-striations, at least in dog and pig (Mimura, 1939). The evidence presented here suggests that in our specimen it took approx. 500 days (1.36 yr) to form the appositional enamel. The imbricational enamel, although comprising much less mm of the enamel volume, forms more slowly than the appositional (Beynon and Wood, 1987). The thickness of cervical enamel at the level where the interpolated line meets the EDJ is approx. 1200 pm measured along the length of enamel prisms (midway between dotted lines b and c, Fig. 6). The cross-striation repeat interval in the outer cervical enamel is 4.7 pm and, assuming this figure represents the daily incremental rate, it would have taken Fig. 6. Diagram of cervical enamel, with interpolated line 1200/4.7 = 255 days (0.7 yr) to secrete this thickness (-.-.-) indicating boundary between appositional and imof enamel. This would be an underestimate because bricational enamel. Dotted lines indicate prism direction. firstly the incremental rate is likely to have been less Striae (i) to (iv) are representative of those which could be near the EDJ (Shellis, 1984; and as reported for the related at successive cervical levels in which individual striae cuspal enamel in this study) and secondly prisms may could be counted in regions a, b and c. The numbers of be longer due to slight decussation of the prisms. The striae in each respective level are indicated (6,6,8). Spacings remaining cervical enamel external to stria (iv) in Fig. between individual striae at each level were: a = 34.2 pm, 6 extrapolated to the EDJ is relatively much smaller b = 32.8pm, c = 31.4pm. The distance (x) between the and would have been completed in a shorter time interpolated boundary line and stria (i) was measured and period, estimated as less than 15 weeks (0.3 yr), divided by the spacing of striae in the adjacent level (a), giving an estimated stria count of nine. The cervical intermaking a totar cervical enamel formation time of section of stria (iv) was projected down to the enamelapprox. I .Oyr. dentine junction, and the width of enamel at that level (y) An alternative estimate for the time required to was measured, and divided by a calculated stria width of complete cervical enamel can be calculated from an 30.8 pm, giving an estimated stria count of 15. estimate of the total number of striae present. The reconstruction described suggests a total of approx. an imbricational enamel completion time of 44 weeks 44 striae in imbricational enamel. There is persuasive or approx. 0.85 yr, or 0.96 yr using an eight-day cycle. evidence that there are seven to eight cross-striations between striae in modem human teeth (Gysi, 1939; Both of these alternative estimates (enamel secretion rates, and striae counts) give a completion time of Fukuhara, 1959; Newman and Poole, 1974; Beynon approx. 1.0 yr for imbricational cervical enamel. and Reid, 1987). The spacing of striae in cervical This value of 1.Oyr summed with 1.36 yr for ap enamel, from 3 1.4 to 34.2 pm, when divided by seven, gives values of 4.5 and 4.9 pm, falling either side of positional cuspal enamel gives a crown completion the measured cross-striation repeat interval value in time of approx. 2.4yr. This is much shorter than the reported mean crown-formation times of 4.25 outer cervical enamel of 4.7 pm. This lends support (P,) and 4.5 (P,) yr in modem man (reviewed by to the hypothesis of a circaseptan rhythm during tooth formation, which applied during tooth for- Gustafson and Koch, 1974), despite the fact that modem human premolars are smaller and have mation in hominids. If we assume a weekly petiodicity between striae in this specimen, this would give thinner enamel. Radiographic studies on developing
776
A. D. BEYSONand M. C. DEAN
human premolar teeth suggest a range in ccownformation times from 3.2 to 3.4 (Moorrees, Fanning and Hunt, 1963), to 5.0yr (Nolla, 1960; using initial mineralization dates of Moorrees et al., 1963, and Schour and Massler, 1940) using longitudinal data. Schour and Massler (1940), using histological data derived from Logan and Kronfeld (1933), gave crown formation times of 3.75-4.25 yr. Shellis (1984) in an innovative study calculated crown-formation times based on measurements of ground sections and obtained values of 4.57* 0.57yr for first premolar teeth. There is only one study (Dean and Wood, 198 1), using cross-sectional radiographic data on pongids, which suggests a premolar crown-formation time of approx. 3 yr, but as yet there are no longitudinal or histological data to confirm this observation. Bromage and Dean (1985), using perikymata counts on hominid teeth, reported short incisor crown-formation times in robust australopithecines. Beynon and Wood (1987) presented data which suggest that molar crown-formation times in robust australopithecines were short compared with man, taking between 2.1 and 2.6 yr. These separate studies, using different dental growth indicators, considered together with Dean’s (1985) confirmation that incisor and molar teeth erupt at the same stage in A. robustus, suggest that tooth development was abbreviated and tooth eruption occurred earlier in the robust australopithecines than in man. The present finding of a short crown-completion time in a large premolar tooth with thick enamel lends further support to this conclusion. It is interesting to note that the premolars of robust australopithecines have become molarized in both their external morphology and crown-formation times. It seems probable that these hominids had an abbreviated period of dental development, allowing them to reach dental, and by inference skeletal and sexual maturity at a much earlier age than in modem man, and possibly even earlier than modern great apes.
Acknowledgemenu-We thank the Government of Kenya and the Director & Trustees of the National Museum of Kenya for allowing us to examine material in their care. We are &ateful for financial support from the Wellcome Trust, the Ntield Foundation. the Boise Fund and the Leakev Trust to M. C. Dean, gnd the Royal Society to A. d. Beynon. We thank D. J. Reid and A. Parker for technical assistance, W. Ashurst for illustrations and J. Rose for typing the manuscript. REFERENCES
Aspcr H. von (1916) Uber die ‘Braune Retzius’sche Parallelstreifung’ im Schmelz der menschlichen Zahne. Schweiz. Vierreljohr. Zahn. 26, 275-314. Beynon A. D. (1987) Replication technique for studying microstructure in fossil enamel. Scanng Microsc. 1, 663-669. Beynon A. D. and Wood B. A. (1986) Variations in enamel thickness and structure in East African hominids. Am. J. phys. Anthrop. 70, 177-195. Beynon A. D. and Reid D. J. (1987) Relationships between
perikymata counts and crown formation times in the human permanent dentition. J. dent. Res. 66, 889. Bcynon A. D. and Wood B. A. (1987) Patterns and rates of molar crown formation times in East African fossil hominids. Nolure 326. 493-496. Boyde A. (1976) Amelbgenesis land the development of teeth. In: Scientific Foundations of Dentistrv (Edited bv Cohen B. and Kramer I. R. H.)..Heinemann, London. Boyde A. (1979) Carbonate concentration. crystal centres, core dissolution, caries, cross striations, circadian rhythms and compositional contrast in the SEM. J, dent. Res. !%b, 981-983. Boyde A. and Jones S. J. (1983) Backkattered electron imaging of dental tissues. Anof. Embryol. 168, 211-226. Bromaae T. G. and Dean M. C. (1985) . , Re-evaluation of the age at death of Plio-Pleistocene fossil hominids. Nature 317, 525-528. Broom R. and Robinson J. T. (1951) Eruption of the permanent teeth in South African fossil ape-men. Nature 167, 443. Dean M. C. (1985) The eruption pattern of the permanent incisors and first molars in Austropirhecus [Paranthropus] robustus. Am. J. phys. Anthrop. 67, 251-237. _ Dean M. C. and Wood B. A. (1981) Develooinn wnaid dentition and its use for ageing -individual &&ia-in comparative cross-sectional growth studies. Foha Primal. 36, I I l-127. Fukuhara T. (1959) Comparative anatomical studies of the growth lines in the enamel of mammalian teeth. Acra onot. nippon. 34, 322-332. Gustafson A.-G. (1959) A morphologic investigation of certain variations in the structure and mineralisation of human dental enamel. Odont. Tihkr. 67, 361-472. Gustafson G. and Koch G. (1974) Age estimation up to 16 years of age based on dental development. Odonr. Revy 25, 297-306. Gysi A. (I 939) Metabolism in adult enamel. Dent. Digest 37, 661-668. Logan W. and Kronfeld R. (1933) Development of the human jaws and surrounding structures from birth lo the age of fifteen years. J. Am. denf. Ass. 20, 379-427. Mann A. E. (1975) Some Paleodemographic Aspects of the South African Ausrrolopithecines. University of Pennsylvania, Philadelphia. Mimura F. (1939) Horoshitsu ni mirareru Seicho-sen no shuki. (Periodicity of growth tines seen in enamel.] Kobyoshi 13, 454-455. Moorrees C. F. A., Fanning E. A. and Hunt E. E. (1963) Age variation of formative stages for ten permanent teeth. J. dent. Res. 42, 1490-1502. Newman H. N. and Poole D. F. G. (1974) Observations with scanning and transmission electron microscopy on the structure of human surface enamel. Archs oral Biol. 19, 1135-I 143. Nolla C. M. (1960) The development of the permanent teeth. J. dent. Child. 27, 2%266. Osborne J. W. (1973) Variations in structure and development of enamel. In: Dental Enamel. Oral Science Reviews, Vol. 3, pp. 3-83. Munksgaard. Copenhagen. Pickerill H. P. (1913) The structure of enamel. Dent. Cosmos LV, 969-988. Schour I. and Massler M. (1940) Studies in tooth development: the growth pattern of human teeth (II]. J. Am. dent. Ass. 27, 1918-1931. Shellis R. P. (1984) Variations in growth of the enamel crown in human teeth and a possible relationship between growth and enamel structure. Archs oral Eiol. 29, 697-705. Weber D. F. and Glick P. L. (1975) Correlative microscopy of enamel prism orientation. Am. J. Anar. 144,407-420.
Hominid crown-formation
time
Plates 1 and 2 overleaf.
178
A. D. BEYNONand M. C. DEAN
Plate I Fig. I. Survey view of fractured face of P (KNM-ER 733D). immersed in ethanol, and illuminated with horizontallv-oolarized light. White bar indicates line along which cross-striations were counted on the replica from the dentine horn to the tip of the cusp. Fig. 2. Detail of occlusal enamel, showing distinct striae (solid arrows) and less distinct striae (open arrows). Fig. 3. Detail of cervical region, showing regular striae in the outer half of enamel. Hunter-Schreger bands follow a straight course. Plate 2 Fig. 5. SEM montage of replica showing enamel prisms with cross-striations in the occlusal 1.5 mm of enamel, divided into 0.5mm sections. Occlusal surface is at the top of the figure. The total enamel thickness was 2.5 mm, the remaining 1.0 mm of enamel is not illustrated. Prisms follow a straight course, with little lateral or spiral deviation.
Hommd
crown-fonnatron
__ .Y
tfme
t Plate I
Imm
i
Plate 2
~rchs oral Bid.Vol.32,No. II,pp.773-780, 1987
Copyright C 1987 Pngamon Joumab Ltd
Printed in Great Britain. All rights resewed
CROWN-FORMATION TIME OF A FOSSIL HOMINID PREMOLAR TOOTH A. D. BEYNON' and M. C. DEAN’ ‘Department of Oral Biology, The Dental School, Framlington Place, Newcastle upon Tyne NE2 4BW and %epartment of Anatomy & Embryology, University College London, Gower Street, London WClE 6BT, England, U.K. Summary-Studies using surface or internal enamel growth indicators in hominids have suggested that crown-formation times were shorter than those in modem man. The crown-formation time in a robust australopithecine premolar tooth was calculated by counting enamel cross-striations, which correspond to daily increments of formation, on a replica of the fractured internal enamel surface of cuspal enamel using scanning electron microscopy. Cervical enamel completion time was estimated using other growth indicators including striae. and using measured and calculated cross-striation repeat intervals, giving a completion time of approx. 2.4 yr. This is much shorter than reported premolar crown formation times in modem man. These findings support the concept of an abbreviated period of dental development, with implications on the duration of the growth period in early hominids.
INTRODUCTION reliable data about the timing of hominid dental development it has been customary to age juvenile fossil hominid jaws and developing teeth on the basis of modem human and pongid dental erup tion sequences. Mann (1975) compared the pattern of dental development in four juvenile mandibles of Australopithecus robustus from South Africa with those patterns found in modem man and chimpanzee. He noted close similarities with developmental sequences in man and inferred a longer postnatal development period in hominids compared with pongids. At that time, however, there was no detailed information on the chronology of dental development in pongids; that was described in 1981 by Dean and Wood who noted that the crown formation times in pongids were broadly similar to those in man, but that in general pongid teeth erupted with less root formed; there was evidence of a faster rate of root formation in pongids. Incisor teeth erupted much later, nearer to second molars than first molars. Dean (1985) t-e-investigated a claim by Broom and Robinson (1951) that the eruption pattern of the permanent incisors and first permanent molars in robust australopithecines (A. robustus) was the same as that in man. He found that the permanent incisors and first molar erupted at a similar stage of development to that in man, whereas specimens attributed to A. africanus or afarends showed a pattern of eruption similar to that of pongids. These studies only provide information about the relative timing of dental developmental events during the growth period. However, Bromage and Dean (1985) and Beynon and Wood (1987) have provided data for crown formation times in early hominids. Bromage and Dean counted the numbers of perikymata on the labial surface of incisor teeth of early hominids. These structures are the surface manifestations of striae of Retxius, and have a periodicity of approx. seven to eight days in modem man (Gysi, 1939; Newman and Poole, 1974). They showed that perikymata on the surfaces of teeth of South African Without
robust australopithecines were fewer and more widely-spaced in the cervical region, suggesting a faster rate of incisor crown formation when compared with modem man, A. africanus and A. afare&s. They used this new data to prepare revised estimates of chronological age at death for several important hominid specimens. Beynon and Wood (1987) presented estimates for the duration of crown formation in molar teeth in East African hominids, based upon the degree of slope of incremental lines, and cross-striation repeat intervals in enamel of early Homo and robust australopithecines, concluding that molar crown-formation times were similar to or shorter than those in modem man. These estimates were derived from reconstructions of striae of several individual teeth and used composite values for crossstriation periodicities taken from replicas of the enamel surfaces, in some cases, of different teeth. The purpose of the present study is to report on a premolar tooth from a robust australopithecine in which it was possible to count cross-striations through the full thickness of occlusal enamel, and also to estimate the numbers of striae in the cervical enamel of the same specimen which improves the accuracy of estimation of crown-formation time for a single tooth. MATRRIAlSANDMRTHOD§ The tooth specimen was an unworn maxillary premolar (LP’) KMN-ER 733D housed in the National Museum of Kenya. The crown was complete and some root had formed, judged by the thickness of coronal dentine. The specimen was fractured axially in a me&-distal direction, and transversely at the approximate level of the cervical margin, damaging the most cervical 0.5-0.7mm of enamel (Plate Fig. I). The specimen was immersed in absolute ethanol (Beynon and Wood, 1986) and viewed with horizontally-polarized incident light, with an analyser over the objective lens of a Wild stereomicroscope to enhance the visualization of striae of Retzius. Striae were visible on the occlusal
773
774
A. D. BEYNONand M. C. DEAS
Imm
Fig. 4. Diagram showing examples of distinct striae (solid lines). and less distinct striae (dashed lines). The interpolated boundary between appositional and imbricational enamel is indicated (-.-.-). Enamel prism direction is indicated as dotted lines.
and cervical aspects of the crown (Plate Figs 2 and 3)
and a master tracing of the enamel outline was made at a magnification of x 50. Photographic negatives of the original specimen were projected on the tracing at the same magnification, and the course of distinct striae were transferred to the master tracing as solid lines (Text Fig. 4). Incomplete striae are indicated in broken lines, and the course of enamel prisms are indicated as dotted lines broadly perpendicular to the enameldentine junction (EDJ; Fig. 4). Crown enamel formation can be divided into two descriptive developmental stages (Beynon and Wood, 1987). The first cuspal or appositional stage corresponds to the production of full thickness enamel over the cusp tip, during which stage the enamel is being secreted in successional layers over the whole surface of the immature crown, and striae of Retxius do not reach the tooth surface. The second or imbricational (after Pickerill, 1913; from L. intbrex tile; overlapping) stage involves the asymmetric deposition of enamel on the sides of the crown, with successive increments associated with surface perikymata extending cervitally to complete the final crown height. The boundary between the appositional and imbricational stages is indicated by the discontinuous heavy line in Fig. 4. The fractured surface was replicated, using a twostage silicone-rubber impression technique, and a replica was made with Spurr resin. This methodology has been assessed for dimensional accuracy using replicas of an engraved incident-light micrometer, and a vernier eyepiece micrometer, and is accurate to within 1 per cent. It is capable of reproducing detail down to 0.2pm (Beynon, 1987). The replica was studied using a Cambridge S600 scanning electron microscope @EM).
Enamel
RESULTS above the dentine horns measured 2.5 mm
in thickness. Prisms showing cross-striations were clearly identifiable on the replica of the fractured enamel surface and it was possible to count all the cross-striations between the EDJ over the right dentine horn and the unworn occlusal surface (Plate Fig. 5), giving a figure of 500 f 3 counts by two independent observers on three separate occasions. The cross-striation repeat interval increased steadily from the EDJ to the external surface. Counts were made in five 0.5 mm lengths, with average values of 4.0 (innermost l/5), 4.3, 5.2, 6.0 and 6.5pm (outermost l/5) being obtained. Cross-striations were much less conspicuous in imbricational enamel, and it was only possible to obtain estimates in the outer l/5 of cervical enamel at the level where regular striae were present (Fig. 3). Values obtained were 4.7 f 0.5 pm in seven separate microscopic fields. Regular striae were visible in the cervical enamel (Fig. 3) and it was possible to identify 20 adjacent striae, in the mid-cervical enamel, which could be related at succeeding cervical levels, allowing a reconstruction of total striae in cervical enamel to be made (Text Fig. 6, see caption for details). We estimate that there were nine missing striae between the occlusal limit of the visible striae and the boundary between appositional and imbricational enamel; and 15 in the remaining cervical enamel. These estimates summed with the 20 visible striae indicate the presence of approx. 44 striae in imbricational enamel. The adjacent striae in the cervical enamel were fairly regularly spaced (Fig. 3). Measurements on the photomicrograph of the intervals between striae were made along the prism axis, which ranged from 34.2
Hominid crown-formation to 31.4 pm between adjacent striae. Striae could not be clearly distinguished in this region on replicas using the SEM.
775
time
/ l
/I
DI!XUSSION It is generally accepted that prism cross-striations represent daily increments of enamel growth (Asper, 1916; Gustafson, 1959; Osborne, 1973; Boyde, 1976). Weber and Glick (1975) suggested that crossstriations are optical artifacts in thick ground sections, but scanning electron microscopy of fractured enamel surfaces (Boyde, 1976) has revealed alternating varicosities and constrictions along prisms with a periodicity of 4-8 pm. SEM studies using backscattered electron imaging modes (Boyde, 1979; Boyde and Jones, 1983) on polished longitudinal enamel sections showed a rhythmic variation in atomic-number contrast of a similar periodicity to the constrictions seen on fractured surfaces, suggesting differences in chemical composition of the inorganic phase of enamel formed during the circadian cycle. Some experimental evidence also confirms the likely circadian nature of enamel cross-striations, at least in dog and pig (Mimura, 1939). The evidence presented here suggests that in our specimen it took approx. 500 days (1.36 yr) to form the appositional enamel. The imbricational enamel, although comprising much less mm of the enamel volume, forms more slowly than the appositional (Beynon and Wood, 1987). The thickness of cervical enamel at the level where the interpolated line meets the EDJ is approx. 1200 pm measured along the length of enamel prisms (midway between dotted lines b and c, Fig. 6). The cross-striation repeat interval in the outer cervical enamel is 4.7 pm and, assuming this figure represents the daily incremental rate, it would have taken Fig. 6. Diagram of cervical enamel, with interpolated line 1200/4.7 = 255 days (0.7 yr) to secrete this thickness (-.-.-) indicating boundary between appositional and imof enamel. This would be an underestimate because bricational enamel. Dotted lines indicate prism direction. firstly the incremental rate is likely to have been less Striae (i) to (iv) are representative of those which could be near the EDJ (Shellis, 1984; and as reported for the related at successive cervical levels in which individual striae cuspal enamel in this study) and secondly prisms may could be counted in regions a, b and c. The numbers of be longer due to slight decussation of the prisms. The striae in each respective level are indicated (6,6,8). Spacings remaining cervical enamel external to stria (iv) in Fig. between individual striae at each level were: a = 34.2 pm, 6 extrapolated to the EDJ is relatively much smaller b = 32.8pm, c = 31.4pm. The distance (x) between the and would have been completed in a shorter time interpolated boundary line and stria (i) was measured and period, estimated as less than 15 weeks (0.3 yr), divided by the spacing of striae in the adjacent level (a), giving an estimated stria count of nine. The cervical intermaking a totar cervical enamel formation time of section of stria (iv) was projected down to the enamelapprox. I .Oyr. dentine junction, and the width of enamel at that level (y) An alternative estimate for the time required to was measured, and divided by a calculated stria width of complete cervical enamel can be calculated from an 30.8 pm, giving an estimated stria count of 15. estimate of the total number of striae present. The reconstruction described suggests a total of approx. an imbricational enamel completion time of 44 weeks 44 striae in imbricational enamel. There is persuasive or approx. 0.85 yr, or 0.96 yr using an eight-day cycle. evidence that there are seven to eight cross-striations between striae in modem human teeth (Gysi, 1939; Both of these alternative estimates (enamel secretion rates, and striae counts) give a completion time of Fukuhara, 1959; Newman and Poole, 1974; Beynon approx. 1.0 yr for imbricational cervical enamel. and Reid, 1987). The spacing of striae in cervical This value of 1.Oyr summed with 1.36 yr for ap enamel, from 3 1.4 to 34.2 pm, when divided by seven, gives values of 4.5 and 4.9 pm, falling either side of positional cuspal enamel gives a crown completion the measured cross-striation repeat interval value in time of approx. 2.4yr. This is much shorter than the reported mean crown-formation times of 4.25 outer cervical enamel of 4.7 pm. This lends support (P,) and 4.5 (P,) yr in modem man (reviewed by to the hypothesis of a circaseptan rhythm during tooth formation, which applied during tooth for- Gustafson and Koch, 1974), despite the fact that modem human premolars are smaller and have mation in hominids. If we assume a weekly petiodicity between striae in this specimen, this would give thinner enamel. Radiographic studies on developing
776
A. D. BEYSONand M. C. DEAN
human premolar teeth suggest a range in ccownformation times from 3.2 to 3.4 (Moorrees, Fanning and Hunt, 1963), to 5.0yr (Nolla, 1960; using initial mineralization dates of Moorrees et al., 1963, and Schour and Massler, 1940) using longitudinal data. Schour and Massler (1940), using histological data derived from Logan and Kronfeld (1933), gave crown formation times of 3.75-4.25 yr. Shellis (1984) in an innovative study calculated crown-formation times based on measurements of ground sections and obtained values of 4.57* 0.57yr for first premolar teeth. There is only one study (Dean and Wood, 198 1), using cross-sectional radiographic data on pongids, which suggests a premolar crown-formation time of approx. 3 yr, but as yet there are no longitudinal or histological data to confirm this observation. Bromage and Dean (1985), using perikymata counts on hominid teeth, reported short incisor crown-formation times in robust australopithecines. Beynon and Wood (1987) presented data which suggest that molar crown-formation times in robust australopithecines were short compared with man, taking between 2.1 and 2.6 yr. These separate studies, using different dental growth indicators, considered together with Dean’s (1985) confirmation that incisor and molar teeth erupt at the same stage in A. robustus, suggest that tooth development was abbreviated and tooth eruption occurred earlier in the robust australopithecines than in man. The present finding of a short crown-completion time in a large premolar tooth with thick enamel lends further support to this conclusion. It is interesting to note that the premolars of robust australopithecines have become molarized in both their external morphology and crown-formation times. It seems probable that these hominids had an abbreviated period of dental development, allowing them to reach dental, and by inference skeletal and sexual maturity at a much earlier age than in modem man, and possibly even earlier than modern great apes.
Acknowledgemenu-We thank the Government of Kenya and the Director & Trustees of the National Museum of Kenya for allowing us to examine material in their care. We are &ateful for financial support from the Wellcome Trust, the Ntield Foundation. the Boise Fund and the Leakev Trust to M. C. Dean, gnd the Royal Society to A. d. Beynon. We thank D. J. Reid and A. Parker for technical assistance, W. Ashurst for illustrations and J. Rose for typing the manuscript. REFERENCES
Aspcr H. von (1916) Uber die ‘Braune Retzius’sche Parallelstreifung’ im Schmelz der menschlichen Zahne. Schweiz. Vierreljohr. Zahn. 26, 275-314. Beynon A. D. (1987) Replication technique for studying microstructure in fossil enamel. Scanng Microsc. 1, 663-669. Beynon A. D. and Wood B. A. (1986) Variations in enamel thickness and structure in East African hominids. Am. J. phys. Anthrop. 70, 177-195. Beynon A. D. and Reid D. J. (1987) Relationships between
perikymata counts and crown formation times in the human permanent dentition. J. dent. Res. 66, 889. Bcynon A. D. and Wood B. A. (1987) Patterns and rates of molar crown formation times in East African fossil hominids. Nolure 326. 493-496. Boyde A. (1976) Amelbgenesis land the development of teeth. In: Scientific Foundations of Dentistrv (Edited bv Cohen B. and Kramer I. R. H.)..Heinemann, London. Boyde A. (1979) Carbonate concentration. crystal centres, core dissolution, caries, cross striations, circadian rhythms and compositional contrast in the SEM. J, dent. Res. !%b, 981-983. Boyde A. and Jones S. J. (1983) Backkattered electron imaging of dental tissues. Anof. Embryol. 168, 211-226. Bromaae T. G. and Dean M. C. (1985) . , Re-evaluation of the age at death of Plio-Pleistocene fossil hominids. Nature 317, 525-528. Broom R. and Robinson J. T. (1951) Eruption of the permanent teeth in South African fossil ape-men. Nature 167, 443. Dean M. C. (1985) The eruption pattern of the permanent incisors and first molars in Austropirhecus [Paranthropus] robustus. Am. J. phys. Anthrop. 67, 251-237. _ Dean M. C. and Wood B. A. (1981) Develooinn wnaid dentition and its use for ageing -individual &&ia-in comparative cross-sectional growth studies. Foha Primal. 36, I I l-127. Fukuhara T. (1959) Comparative anatomical studies of the growth lines in the enamel of mammalian teeth. Acra onot. nippon. 34, 322-332. Gustafson A.-G. (1959) A morphologic investigation of certain variations in the structure and mineralisation of human dental enamel. Odont. Tihkr. 67, 361-472. Gustafson G. and Koch G. (1974) Age estimation up to 16 years of age based on dental development. Odonr. Revy 25, 297-306. Gysi A. (I 939) Metabolism in adult enamel. Dent. Digest 37, 661-668. Logan W. and Kronfeld R. (1933) Development of the human jaws and surrounding structures from birth lo the age of fifteen years. J. Am. denf. Ass. 20, 379-427. Mann A. E. (1975) Some Paleodemographic Aspects of the South African Ausrrolopithecines. University of Pennsylvania, Philadelphia. Mimura F. (1939) Horoshitsu ni mirareru Seicho-sen no shuki. (Periodicity of growth tines seen in enamel.] Kobyoshi 13, 454-455. Moorrees C. F. A., Fanning E. A. and Hunt E. E. (1963) Age variation of formative stages for ten permanent teeth. J. dent. Res. 42, 1490-1502. Newman H. N. and Poole D. F. G. (1974) Observations with scanning and transmission electron microscopy on the structure of human surface enamel. Archs oral Biol. 19, 1135-I 143. Nolla C. M. (1960) The development of the permanent teeth. J. dent. Child. 27, 2%266. Osborne J. W. (1973) Variations in structure and development of enamel. In: Dental Enamel. Oral Science Reviews, Vol. 3, pp. 3-83. Munksgaard. Copenhagen. Pickerill H. P. (1913) The structure of enamel. Dent. Cosmos LV, 969-988. Schour I. and Massler M. (1940) Studies in tooth development: the growth pattern of human teeth (II]. J. Am. dent. Ass. 27, 1918-1931. Shellis R. P. (1984) Variations in growth of the enamel crown in human teeth and a possible relationship between growth and enamel structure. Archs oral Eiol. 29, 697-705. Weber D. F. and Glick P. L. (1975) Correlative microscopy of enamel prism orientation. Am. J. Anar. 144,407-420.
Hominid crown-formation
time
Plates 1 and 2 overleaf.
178
A. D. BEYNONand M. C. DEAN
Plate I Fig. I. Survey view of fractured face of P (KNM-ER 733D). immersed in ethanol, and illuminated with horizontallv-oolarized light. White bar indicates line along which cross-striations were counted on the replica from the dentine horn to the tip of the cusp. Fig. 2. Detail of occlusal enamel, showing distinct striae (solid arrows) and less distinct striae (open arrows). Fig. 3. Detail of cervical region, showing regular striae in the outer half of enamel. Hunter-Schreger bands follow a straight course. Plate 2 Fig. 5. SEM montage of replica showing enamel prisms with cross-striations in the occlusal 1.5 mm of enamel, divided into 0.5mm sections. Occlusal surface is at the top of the figure. The total enamel thickness was 2.5 mm, the remaining 1.0 mm of enamel is not illustrated. Prisms follow a straight course, with little lateral or spiral deviation.
Hommd
crown-fonnatron
__ .Y
tfme
t Plate I
Imm
i
Plate 2