Megadontia, striae periodicity and patterns of enamel secretion in Plio-Pleistocene fossil hominins

J. Anat.

(2008)

213

, pp148–158 doi: 10.1111/j.1469-7580.2008.00938.x

© 2008 The AuthorsJournal compilation © 2008 Anatomical Society of Great Britain and Ireland

Blackwell Publishing Ltd

Megadontia, striae periodicity and patterns of enamel secretion in Plio-Pleistocene fossil hominins

Rodrigo S. Lacruz,

1,2

M. Christopher Dean,

3

Fernando Ramirez-Rozzi

4

and Timothy G. Bromage

5

1

Center for Craniofacial Molecular Biology, School of Dentistry, University of Southern California, Los Angeles, USA

2

B.P.I. Palaeontology, School of Geosciences; and Institute for Human Evolution, University of the Witwatersrand, Johannesburg, South Africa

3

Department of Anatomy and Developmental Biology, University College London, UK

4

UPR 2147 CNRS, Paris, France

5

Departments of Biomaterials & Basic Sciences, New York University College of Dentistry, USA

Abstract

Early hominins formed large and thick-enamelled cheek-teeth within relatively short growth periods as comparedwith modern humans. To understand better the developmental basis of this process, we measured daily enamelincrements, or cross striations, in 17 molars of Plio-Pleistocene hominins representing seven different species,including specimens attributed to early

Homo

. Our results show considerable variation across species, although allspecimens conformed to the known pattern characterised by greater values in outer than inner enamel, andgreater cuspal than cervical values. We then compared our results with the megadontia index, which representstooth size in relation to body mass, for each species to assess the effect of daily growth rates on tooth size. Ourresults indicate that larger toothed (megadont) taxa display higher rates or faster forming enamel than smallertoothed hominins. By forming enamel quickly, large tooth crowns were able to develop within the constraints ofshorter growth periods. Besides daily increments, many animals express long-period markings (striae of Retzius) intheir enamel. We report periodicity values (number of cross striations between adjacent striae) in 14 new specimensof

Australopithecus afarensis

,

Paranthropus aethiopicus

,

Paranthropus boisei

,

Homo habilis

,

Homo rudolfensis

and

Homo erectus

, and show that long-period striae express a strong association with male and average male–femalebody mass. Our results for Plio-Pleistocene hominins show that the biological rhythms that give rise to long-periodstriae are encompassed within the range of variation known for modern humans, but show a lower mean andmodal value of 7 days in australopithecines. In our sample of early

Homo

, mean and modal periodicity values were8 days, and therefore similar to modern humans. These new data on daily rates of enamel formation and periodicityprovide a better framework to interpret surface manifestations of internal growth markings on fossil hominintooth crowns. Importantly, our data on early hominin cross striation variation may now contribute towards solvingdifficult taxonomic diagnoses where much may depend on fragmentary molar remains and enamel structure.

Key words

body mass; cross striations; enamel development; megadontia; striae of Retzius.

Introduction

Enamel is the hardest of all vertebrate tissues and becauseof its high mineral content, tooth enamel preservesremarkably well in the fossil record. It is not surprising,therefore, that inferences about the evolutionary historyand past biology of many organisms have been made fromstudies of dental remains. In this regard, fossil homininsare no exception. Studies of the quantity or thickness anddistribution of dental enamel in hominin teeth have

figured prominently in recent years. These are importantcharacters relevant to aspects of hominin taxonomy andalso for providing insights into hominin tooth functionand diet (Molnar & Gantt, 1977; Martin, 1985; Beynon &Wood, 1986; Grine & Martin, 1988; Macho & Thackeray,1992; Teaford & Ungar, 2000). Enamel also incorporatesinto its microstructure a hierarchical set of temporalevents through the course of its development, which canbe imaged using a variety of microscopic and micro-tomographic techniques. These have enabled aspects ofthe life history of these extinct species to be reconstructed(Bromage & Dean, 1985; Beynon & Wood, 1987; Beynon &Dean, 1988; Dean et al. 2001; Schwartz et al. 2002; Kelley& Smith, 2003; Ramirez Rozzi & Bermudez de Castro, 2004;Lacruz et al. 2005; Smith et al. 2007a).

Correspondence

Dr Rodrigo S. Lacruz, 2250 Alcazar St, CSA 103, Los Angeles, CA 90033, USA. T: 323 442 3170; F: 323 442 2981; E: [email protected]

Accepted for publication

25 March 2008

Enamel secretion in Plio-Pleistocene fossil hominins, R. S. Lacruz et al.

© 2008 The Authors Journal compilation © 2008 Anatomical Society of Great Britain and Ireland

149

A defining characteristic of early hominins, observed inthe genera

Australopithecus

,

Paranthropus

and in earlyrepresentatives of the genus

Homo

, is the large size of thepost canine teeth in relation to their body mass (McHenry,2002). The megadontia quotient, calculated by McHenry(1984, 1988), defined as ‘the observed area of the mandi-bular last premolar and first two molars divided by the areapredicted from the body weight’ (McHenry, 1988, p. 144),indicates that the genus

Paranthropus

displays the greatestrelative tooth size, followed by the australopithecines andfossil

Homo

(McHenry, 1984, 1988, 2002) (Table 1). Thispattern is similar to that described in the literature forenamel thickness among hominins (Martin, 1985; Beynon& Wood, 1986; Grine & Martin, 1988; Macho & Thackeray,1992; Teaford & Ungar, 2000).

The thickness and volume of enamel results from theinterplay between the number of active enamel secretorycells (ameloblasts), the length of time that each cellremains active and the rates of secretion of these cells(Grine & Martin, 1988; Dean et al. 2001). Heterogeneity inprimate enamel thickness and formation time results fromvariation in one or more of these parameters (Grine & Martin,1988; Beynon et al. 1991; Dean, 1998, 2000; Schwartz, 2000;Dean et al. 2001; Hlusko et al. 2004).

Importantly, the development of mammalian enamel isknown to undergo periodic oscillations on a 24-h timescale, giving rise to daily increments, or markings, knownas cross striations (Boyde, 1989), which are one of the mostuseful tools to interpret differences in enamel developmentin the fossil record. These daily markings appear either aslinear features aligned perpendicular to the enamel prismaxis when viewed by conventional compound light micro-scopy and backscattered electron imaging in the scanningelectron microscope (SEM), as alternating varicosities and

constrictions when imaged by secondary electron imagingin the SEM, and as fine dark periodic lines in confocalmicrocopy (Beynon & Dean, 1987; Dean, 1987; Boyde,1989; Bromage et al. 2007). The long-period markings,known as striae of Retzius, staircase along cross striationsoblique to the enamel prism axis and reach the surfaceenamel within troughs of undulating surface featurescalled perikymata (Dean, 1987). The number of cross stria-tions between striae, referred to as the repeat interval orperiodicity, is the same for all teeth of an individual but isvariable within and between species (FitzGerald, 1998).Although the nature of cross striations is associated withchanges in cell secretory activity from fast to slow duringenamel formation (Boyde, 1989), the aetiology of normalstriae remains less certain despite the periodic nature ofits expression. Previously, estimates of the periodicitytogether with total perikymata counts made on the toothsurface were the only method available to estimate thelateral crown formation times of early fossil hominin crowns(Bromage & Dean, 1985; Beynon & Wood, 1987; Beynon &Dean, 1988; Ramirez Rozzi, 1995) and so it is of considerableimportance that actual data for the periodicity in Plio-Pleistocene fossil teeth are observed and determineddirectly on as many original specimens as possible.

More than a century ago, Williams illustrated long-periodstriae of Retzius (or ‘lines of stratification’ as he describedthem) in chimpanzee and human surface enamel with eightor nine daily increments between adjacent striae (Williams,1897). More recently, in humans, periodicities of between6 and 12 days have been reported and, in chimpanzees,periodicities of between 6 and 9 days (Schwartz et al.2001; Smith et al. 2007b,c), having a mean and modalvalue of 8 and 6–7 days, respectively (Schwartz et al. 2001;Smith et al. 2007b,c). Given that smaller bodied primatesshow lower periodicities (Bowman, 1991; Dirks, 1998) andthat larger bodied primates show higher periodicities(Dean & Reid, 2001; Dean & Schrenk, 2003), it has beensuggested that there may be a correlation between perio-dicity and body mass (Dean 2000; Smith et al. 2003; Smith,2008). Currently, periodicity values are known for onlyfour Plio-Pleistocene hominin species (Dean, 1987; Wardet al. 2001; Lacruz et al. 2006; Bromage et al. 2007), butdo not include early

Homo

, and thus a more completeinterpretation of the association between body mass andperiodicity in hominins is wanting.

Given the central role that characters such as tooth sizeand enamel thickness play in interpreting fossil hominintaxonomy and adaptation, it is important to analyse thevariation of long (striae of Retzius) and short (cross stria-tions) temporal markings in enamel to understand differ-ences in the development of these characters better. Tothis end, we have undertaken a comprehensive analysis ofdaily enamel secretion rates (DSR) or cross striations on ataxonomically diverse sample of Plio-Pleistocene hominins.The main aims of this study are two-fold: to assess whether

Table 1 Body mass (male/female) and megadontia quotient (MegQ) taken from McHenry (2002) for Australopithecus, Paranthropus, Homo and Pan. Megadontia is defined as the observed area of the mandibular last premolar and first two molars divided by the area predicted from the body weight (McHenry, 1988). No megadontia values have been recorded for P. aethiopicus

Species

Body mass (kg)

Male–female MegQ

A. anamensis 51–33 1.4A. afarensis 45–29 1.7A. africanus 41–30 2.0P. boisei 49–34 2.7P. robustus 40–32 2.2H. habilis 37–32 1.9H. rudolfensis 60–51 1.5H. ergaster/erectus 66–56 0.9H. sapiens 58–49 0.9Pan troglodytes 49–41 0.9



150

faster daily secretion rates are associated with larger toothsize using McHenry’s (1988, 2002) megadontia quotient,and to test whether long-period stria periodicity ofPlio-Pleistocene hominins is correlated to body mass.

Materials and methods

Table 2 provides details of the specimens examined in this study.All molars were permanent teeth with fully developed crowns.Because some specimens were sectioned for a previous study (Deanet al. 2001), two microscopic techniques were used in this work.Specimens available as ground sections were studied usingtransmitted polarized light microscopy. The remaining specimenswere studied using portable confocal scanning optical microscopy(PCSOM), the details of which have been previously described(Bromage et al. 2005; Lacruz & Bromage, 2006; Lacruz et al. 2006;Bromage et al. 2007). Briefly, the PCSOM is based on the Nipkowdisc technique, which, in this case, employs a confocal moduleconfigured to a custom stand. The microscope returns imagedetail in real time from a very thin optical plane at and immediatelybelow the object surface (1–50

μ

m, depending upon specimencharacteristics). In-focus image content through

Z

-series imagestacks was acquired and measurements of cross striations weremade using Auto Montage software (Syncroscopy, Frederick, MD,USA) from calibrated fields. The specimens listed in Table 2 andstudied using PCSOM were selected for this study based on threecriteria. First, cross striations had to be visible in at least one regionof the enamel corresponding to a defined area of the crown

(described below). Secondly, in those specimens for which theperiodicity is reported, striae and cross striations would have to beobserved with confidence in the same field of view, permittingeither direct counts of cross striations between striae or usinglinear distances of both features to assess the likely periodicity asexplained below in more detail. Thirdly, the specimens had tohave reasonably sheer post-mortem occluso-cervical fractureslocated at or near the cusps.

Cross striations were measured in defined regions of the enamelcrown, divided into cuspal, lateral and cervical thirds. Each regionwas also subdivided into inner, middle and outer zones followingprotocols described in Lacruz & Bromage (2006: fig. 2, p. 16),following closely the method originally proposed by Beynon et al.(1991). This protocol was used because of variation in the com-pleteness of fractured enamel crowns, and because in some instances,diagenetic processes had altered fractured surface characteristicsin such a way as to prevent visualization of cross striations fromthe enamel–dentine junction (EDJ) to the outer surface, as hasbeen possible in previous studies (Dean et al. 2001). Daily secretionrates were obtained by measuring a minimum of three to fiveadjacent cross striations in any one location (e.g. Fig. 1), andtypically, a minimum of four sets of at least three cross striationswere measured in each zone, giving a total of at least 12 individualcross striations per zone. Striae periodicity was recorded in theouter enamel where both striae of Retzius and cross striations aretypically most clear, generally within the boundary of lateral andcervical enamel as discussed in Lacruz et al. (2006). Striae periodicitywas assessed by counting the number of cross striations betweenadjacent striae, or by measuring the distance between three adjacentstriae and then dividing by the average distance between crossstriations in the same area, as previously described (Swindler &Beynon, 1993; Schwartz et al. 2001).

A number of tests have been made to ascertain differences inthe measurements made with the PCSOM and other microscopictechniques, including the SEM and incident stereoscopic microscopy(Lacruz, 2006; Lacruz et al. 2006). In Lacruz (2006), cross striationswere measured about 600

μ

m cervically from the apparent dentinehorn of the protocone of the

Australopithecus africanus

specimenStw 284, and about 250–300

μ

m from the EDJ using SEM and the

Table 2 Specimens of Australopithecus, Paranthropus and Homo analysed in this study for DSR and/or periodicity showing taxonomic attribution and tooth type. All specimens had completed crown development

Specimen Taxa Tooth

KNM-ER-30749* A. anamensis LM1KNM-ER-30748* A. anamensis UMAL-333-52 A. afarensis LM1AL-366-1 A. afarensis LM3L-2-79 (OMO) A. afarensis LM2/3F-22-1b P. aethiopicus LM3OMO 47-46 P. boisei LM2OMO 76-37 P. boisei LM3OMO 136-1 P. boisei LM3L 209-17 P. boisei LM2/1L-398-847 P. boisei LM?OMO 47-47 P. boisei LM3KNM-ER-1802 H. rudolfensis LM3KNM-ER-1483* H. rudolfensis LM?KNM-ER-1482 H. rudolfensis LM?UR-501 H. rudolfensis frgKNM-ER-1805* H. habilis PMKNM-ER-3733* H. erectus PMS7-37* H. erectus LM1KNM-ER-809* H. erectus LM?

*Specimens studied using laser confocal microscopy from ground sections. Remaining specimens studied using portable confocal microscopy from natural breaks on the enamel. U = upper; L = lower; PM = premolars.

Fig. 1 Image of cross striations on the cuspal enamel of the Australopithecus afarensis specimen AL 366-1. This image was obtained using the PCSOM (see text for details). Cross striations (fine white arrows) can be seen as darker lines perpendicular to the enamel prisms (longer arrow). Scale bar = 100 μm.



151

PCSOM. Both microscopic techniques revealed a value of

c

. 4

μ

mfor the distance between cross striations. In addition, a blind testwas performed by two of the authors by imaging with the SEM ahigh-resolution replica of the

Paranthropus boisei

premolar KNM-ER-733 (M.C.D.), previously described in Beynon & Dean (1987),and by PCSOM on the same specimen (R.S.L.) following themeasurement scheme described above. SEM and PCSOMmeasurements were nearly identical (unpublished data), withdifferences of < 0.3

μ

m.The taxonomic allocations of dental specimens used in this study

derive from Boaz (1977), Johanson et al. (1982), Wood (1992),Bromage et al. (1995), Suwa et al. (1996) and Ward et al. (2001).Data for body mass and megadontia are taken from McHenry(1992, 2002), which are summarized in Table 1. Information onhominin body mass is generally classified by sex (e.g. McHenry,1992, 2002). Because there is some disagreement as to whetherthere may be differences in striae periodicity between sexes acrossprimates (Schwartz et al. 2001; Smith et al. 2007c), and because itmay be possible that male–female hominin body mass classificationsmay include members of the opposite sex, we have comparedperiodicity values using male, female and species averages (meanof male and female body mass values) as our comparative variables.Spearman’s rank correlation coefficient was used to assess thedegree of data correlation, and the Mann–Whitney

U

-test was usedto compare cuspal outer DSR values between taxa in the followingmanner. All cuspal outer DSR values obtained for each specimenof a given taxon were pooled, and were then compared with thepooled values of other taxa. Finally, given that only one tooth of

Homo habilis

was available for study (KNM-ER 1805), and that aprevious work by Beynon et al. (1991) showed almost identicalDSR values for molars and premolars in the genus

Homo

(

Homosapiens

), we have included DSR values of this tooth in our study,as well as the premolar of

Homo erectus

KNM-ER 3733.

Results

Appendix 1 gives all values of DSRs and standard deviations(SD) for each of the 17 specimens studied. These resultshave been summarized in Table 3, which provides the

mean for each enamel zone of each species considered.Table 3 also includes values of cross striations measured ina sample of 10 modern human molars reported by Lacruz& Bromage (2006). DSRs for

Pan troglodytes

derive fromthe study of Smith et al. (2007b), and values for

A. africanus

and

Paranthropus robustus

from Lacruz & Bromage (2006).The right column of Table 3 includes average cuspal DSRsfor each species, which is used to relate DSRs to megadon-tia values from Table 1. The Spearman rank correlationcoefficient between DSRs for the cuspal zone of enameland megadontia was significantly correlated (

r

s

= 0.71;

P

< 0.01) (Fig. 2). Table 4 shows

P

values resulting from theanalysis of the Mann–Whitney

U

-test in which the outercuspal values of each taxon were pooled and were thencompared with the pooled values of other taxa. Figure 3

Table 3 Summary of daily secretion rates (DSRs) for for Australopithecus, Paranthropus, Homo and Pan species included in this study. The number of specimens used to calculate values in each area of the crown is indicated in parentheses. The right-hand column is the average of cuspal DSR (CUDSR), which is then used to compare the association between DSRs and tooth size as cuspal enamel reflects the greatest differences in enamel thickness among hominins (Beynon & Wood, 1986). The standard deviations of the average values shown here were small, less than 1, and are not shown

Taxon cu.out cu.mid cu.inn lat.out lat.mid lat.inn cer.out cer.inn CUDSR

A. anamensis 5.47 (2) 5.04 (2) 4.17 (2) ? ? ? ? ? 4.89A. afarensis 5.84 (3) 4.66 (3) 3.31 (3) 5.32 (3) 4.76 (3) 3.69 (2) 4.19 (1) 3.22 (1) 4.60A. africanus† 6.62 (5) 5.80 (4) 4.18 (2) 6.11 (6) 5.25 (5) 4.20 (2) 4.46 (4) 3.74 (4) 5.51P. aethiopicus 6.53 (1) 5.31 (1) 3.5 (1) 5.52 (1) 4.86 (1) 3.18 (1) 4.81 (1) 2.83 (1) 5.11P. boisei 7.15 (4) 5.74 (4) 2.94 (4) 5.84 (5) 4.99 (2) 3.40 (1) 4.50 (5) 3.23 (4) 5.30P. robustus† 7.25 (5) 6.12 (4) 4.16 (1) 6.59 (5) 5.63 (5) 3.95 (2) 4.83 (7) 3.89 (3) 5.80H. rudolfensis 5.38 (3) 4.76 (2) 3.01 (3) 4.73 (3) 3.82 (1) 2.90 (1) 3.62 (2) ? 4.47H. habilis 5.22 (1) 4.60 (1) 3.68 (1) 5.30 (1) 5.04 (1) 3.38 (1) ? ? 4.70H. erectus 5.19 (2) 4.46 (2) 3.05 (1) 4.86 (3) 4.20 (2) 3.15 (2) 3.61 (2) ? 4.23H. sapiens 5.20 (10) 4.50 (10) 2.80 (10) 4.80 (10) 4.30 (10) 2.70 (10) 3.60 (9) 2.60 (10) 4.15Pan troglodytes* 4.61 (75) 4.28 (75) 3.62 (75) 4.17

*Data from Smith et al. (2007b) and †Lacruz & Bromage (2006). Enamel regions: cu = cuspal; lat = lateral; cer = cervical; out = outer; mid = middle; inn = inner.

Fig. 2 Bivariate plot of megadontia values (MegQ) taken from McHenry (2002) compared with the average daily rates (DSR) in the cuspal area shown in Table 3 with the exception of Paranthropus aethiopicus for which no megadontia values have been reported.



152

shows error bars using the same values at the 95%confidence interval.

Table 5 provides periodicity values for each specimenfrom which we were able to obtain this information. Theperiodicities obtained for the australopiths (

Australo-pithecus

and

Paranthropus

) have lower mean and modalvalues than those obtained for

H. sapiens

reported by Reid& Dean (2006) and Smith et al. (2007c), and our meanvalue for early

Homo

was 8 days (Table 5).Hominin body mass was also compared with periodicity

values for each species. The Spearman’s rank correlationcoefficient is statistically significant when male body mass(

P

< 0.05), and combined average male–female body massare compared with periodicity (

P

< 0.05), but female bodymass did not correlate significantly with periodicity (

P

> 0.05).

Discussion

The main aims of this study were to assess the relationshipsbetween hominin DSRs and megadontia on the one hand,

and between hominin periodicity and body mass on theother. Figure 2 shows the correlation between the mega-dontia quotient (MegQ) and average DSRs in the cuspalzone for 11 fossil and extant hominin species including thecommon chimpanzee. This correlation is highly significant(

P

< 0.01;

r

s

= 0.71), suggesting that high DSRs have animportant contribution to tooth size in hominins; taxawith greater tooth size display greater daily secretion rates.These results are in agreement with previous studies onthe developmental characteristics of fossil hominin enamel

Fig. 3 Error bar graph at the 95% confidence interval (95% CI) of DSR values on the cuspal outer zone of each species included in this study. From this graph it is clear that there is a trend from high to low values across taxa, with Paranthropus (P. boisei and P. robustus) showing the highest values, and the lowest being recorded in Homo, which is a similar pattern described for enamel thickness in hominins (e.g. Teaford & Ungar, 2000).

Table 4 P values resulting from the analyses of DSR in the cuspal outer zone using Mann–Whitney U-test on a one to one comparison. Values shown in bold are not statistically significant (P > 0.05)

afarensis africanus aethiopicus boisei robustus rudolfensis habilis erectus sapiens

anamensis 0.373 0.018 0.001 0.000 0.000 0.940 0.456 0.428 0.125afarensis 0.001 0.000 0.000 0.000 0.119 0.003 0.001 0.000africanus 0.768 0.006 0.008 0.000 0.000 0.000 0.000aethiopicus 0.000 0.003 0.000 0.000 0.000 0.000boisei 0.751 0.000 0.000 0.000 0.000robustus 0.000 0.000 0.000 0.000rudolfensis 0.137 0.050 0.008habilis 0.496 0.794erectus 0.759

Table 5 Periodicity values for each specimen

Specimen Periodicity

Australopith specimensKNM-ER-30749 7*KNM-ER-30748 7*AL-333-52 7AL-366-1 7L-2-79 (OMO) 7OMO 47-46 7OMO 76-37 7F-22-1b 7L 209-17 7

Australopith mean/modal 7 daysHomo specimens

KNM-ER-1802 8KNM-ER-1482 7UR-501 8KNM-ER-1805 8KNM-ER-3733 9S7-37 7KNM-ER-809 8

Homo mean/modal 8 days

*Periodicity originally reported by M. C, Dean in Ward et al. (2001). Mean and modal values in the australopithecines (Australopithecus and Paranthropus) is 7 days, compared with 8 days in our sample of fossil Homo. The periodicity of Stw 11 and Stw 284 previously reported by Lacruz et al. (2006) was re-examined by measuring the distance between two adjacent striae, which was divided by the average daily rates in that area yielding a periodicity of 7 days. Taxonomic attributions of each specimen are detailed in Table 2.



153

(Beynon & Wood, 1987; Grine & Martin, 1988), althoughthe samples used in these studies were qualitatively andrelatively limited in numbers of specimens examined. Ourtaxonomically broad sample permits a clearer understandingof enamel growth differences across Plio-Pleistocene hominins.We show that the greatest outer cuspal rates are foundin the hyper-thick enamel Paranthropus, with means of7.25 and 7.15 μm day–1 in P. robustus and P. boisei, respectively.Among hominins, such fast daily rates appear to be uniqueto this genus (Beynon & Wood, 1987; Grine & Martin, 1988;Lacruz & Bromage, 2006; but see Schwartz et al. 2002,2005 for lemurs). The geochronologically oldest taxonstudied, Australopithecus anamensis, shows similar meanvalues to its purported daughter species A. afarensis, andboth show lower values than A. africanus. The mean DSRsvalues in Homo are somewhat lower than to those of Aus-tralopithecus. Although these findings fit the generallyaccepted trends in enamel thickness among fossil homininsdiscussed earlier, it should be noted that neither linear norrelative enamel thickness in A. anamensis and A. afarensishave yet been well documented.

Based on the results presented in Table 3, two otherimportant observations can be highlighted. First, mosthominin taxa have absolutely higher average DSRs valuesthan modern humans, including the inner zone values,although in some instances, such as in the more recentfossil Homo, these differences are small or are overlapping.Secondly, the pattern of DSR variation along the crown inPlio-Pleistocene hominins follows previous reports indicatingfaster rates in cuspal than in cervical enamel, and whereinner zone values are smaller than outer zone values (Table 3;Beynon et al. 1991; Lacruz & Bromage, 2006). Because thebulk of our study was conducted on fortuitous randomlyfractured fossil enamel surfaces, the data presented inTable 3 sampled an unequal number of different cusp andtooth types. However, given that a previous study onchimpanzee DSRs derived from various molar and cusptypes showed no significant differences (Smith et al. 2007b),we suggest that the variation observed in this study can beregarded for now as independent of both cusp and molartype.

Variations in daily enamel growth have been previouslyused to interpret aspects of growth and development infossil hominins (e.g. Dean et al. 2001). The results presentedin Table 3 now allow us to elaborate on this further. Atleast three cellular processes affect enamel thickness andvolume: enamel secretion rates, the number of active cellsinvolved in enamel secretion at any one time, and thesecretory lifespan of each cell. However, these processesare under certain time and metabolic constraints, whichultimately depend on the life-history profile of a species.Thus, the time invested by each species in forming a toothdepends on the schedule of growth and development ofthat species and the time available to do this (e.g. Bromage,1987; Dean, 2006). The developmental schedules of early

hominins belonging to the genera Paranthropus andAustralopithecus most likely resembled that observed inthe great apes today rather than that in modern humans(Bromage & Dean, 1985; Bromage, 1987; Dean, 1987;Anemone 2002). In addition, these taxa developed their molarcrowns in less time than modern humans (Beynon & Wood,1987; Beynon & Dean, 1988; Ramirez Rozzi, 1993a; Lacruzet al. 2006; Lacruz, 2007). Therefore, to form thick enamelin relatively short periods of time, these hominins increaseddaily secretion rates compared with those, for example, inhumans (Table 3; Fig. 2). Based on our results (Table 3), itwould seem that slower rates of enamel formation becamepossible as either enamel thickness reduced and/or prolon-gation of the growth period reduced the time constraintson tooth formation (Dean, 2006). This is further evidencedby the lower values obtained for H. erectus, which appearsto have had a more extended life-history profile thanearlier hominins and in which DSRs are more similar tomodern H. sapiens (Dean et al. 2001).

As previously discussed, the mechanisms underlying enameldevelopment do not appear to be uniformly homologousacross primates. Therefore, whether the relationship betweenfaster DSRs and enamel thickness and/or tooth size is ageneral mechanism that exists more widely across all extantand extinct primates or whether they operated onlyamong hominins remains unclear. Thick-enamelled pri-mates such as Pongo, Gigantopithecus and Theropithecusappear to have high DSRs (Swindler & Beynon, 1993; Dean,1998; Dean & Schrenk, 2003) although other known thick-enamelled taxa such as Graecopithecus apparently show amore similar pattern to the DSRs known for chimpanzees(Smith et al. 2004).

The second aim of this study was to assess the relationshipbetween periodicity and body mass. Previous studies havepointed to this relationship across a wide taxonomic pri-mate data set (Smith et al. 2003; Smith, 2008). Here wereport striae periodicity for previously unknown taxa thatinclude A. afarensis, Paranthropus aethiopicus, H. habilis,Homo rudolfensis and H. erectus, and on increased samplesof P. boisei. A previous work did not find significantcorrelations between striae periodicity and body mass inhominins (Smith, 2008), but this may be attributed to theuse of a less encompassing sample, which only includedfive out of the nine hominins represented in the presentstudy. Based on our available sample, there appears to bean association between long-period stria periodicity andbody mass among Plio-Pleistocene hominins. However,this relationship is only statistically significant whenperiodicity is compared with male body mass (P < 0.05),and with average male–female body mass (P < 0.05),whereas with female body mass the correlation is notsignificant (P > 0.05). Two previous studies on moderntaxa have indicated that there was either no differencebetween male and female periodicity (Schwartz et al.2001) or that there were differences between sexes (Smith



154

et al. 2007c). Thus, it is currently unclear why this relation-ship between periodicity and body mass does not apply tofemale body mass. However, sex determination of fossilhominin specimens is fraught with difficulty and this mayinfluence the accuracy of estimates for average male andfemale body mass. Interestingly, Macchiarelli et al. (2006)have reported that the periodicity in two Neanderthal per-manent molars (one from Tabun C1 from Israel reportedpreviously by Dean et al. 2001 and one from the site of LaChaise-de-Vouthon, Charente, France) were 8 and 7 days,respectively. Moreover, Ramirez Rozzi (1993b) reported an8-day periodicity in a Neanderthal molar from Zafarraya,Spain. Taken together, these studies suggest that Nean-derthal periodicities may be lower than would beexpected given their larger body mass, posing interestingquestions as to the nature of the relationship betweenperiodicity and body mass in this species. Future studieswill allow us to explore further the effects of phylogeny onperiodicity in a broader taxonomic setting.

In our broad taxonomic sample of ten newly reportedspecimens representing three taxa (A. afarensis, P. aethiopicusand P. boisei), the mean and modal periodicity value was7 days (Fig. 4), and the mean and modal periodicity valuein our sample of three species of early Homo (n = 7) was8 days (Table 5). When data presented in this study forperiodicity among australopithecine taxa (Australo-pithecus and Paranthropus) are combined with those fromprevious studies (Dean, 1987; Dean et al. 1993; Lacruzet al. 2006; Bromage et al. 2007; Tafforeau & Smith, 2008),the mean and modal value in 29 cases reported is 7 days(Fig. 5; the nearest whole value to the mean shown in thisfigure is 7 days as cross striations reflect a 24-h period).This is lower than both the mean and the modal values of8 days observed in modern humans (Smith et al. 2007c).The mean and modal periodicity in Pan, however, wasdetermined to be lower than this (6 days) by Smith et al.(2007c; but see Schwartz et al. 2001 where the periodicityin ten males and ten females was 7 days). In our sample ofearly Homo, the mean and modal value was 8 days and soin this respect is similar to modern humans. In the study ofSmith et al. (2007c), which reported on the largest sampleof modern humans thus far (n = 365), the periodicity was8 days in about 44% of the total, whereas it was 9 days in28% of their sample. In our sample, 59% (n = 29) of theaustralopithecines examined showed a periodicity of7 days. Previously, when only perikymata counts have

been available for calculating crown formation times,average values equivalent to those determined for modernhumans have been used to estimate the total crownformation times of australopithecine anterior teeth andmolars (Dean & Reid, 2001; Dean et al. 2001). Given thatthe 7-day periodicity determined here for australo-pithecines represents 59% of the sample studied, it nowseems more appropriate to use this periodicity as anaverage in calculations of crown formation times foraustralopithecines when the true periodicity is not known.Indeed, this was the original average value suggested byBromage & Dean (1985). Better, perhaps in these circum-stances, will be to now use the range of known periodicitiesas reported here, which can be used with more confidencein comparisons between various early hominin taxa andmodern humans.

Although these periodicities are not very differentamong Plio-Pleistocene hominin taxa, the values presentedhere demonstrate that the underlying physiology giving

Fig. 4 (A) Periodicity on the Australopithecus anamensis specimen KNM-ER-30748 (7 days). (B) Periodicity on the Homo habilis specimen KNM-ER-1805 (8 days). Both images taken with transmitted light microscopy.

Fig. 5 Frequency distribution of striae periodicity in australopithecines (Australopithecus and Paranthropus) in a sample of 29 specimens from this and all previous published records (Dean et al. 1993; Dean, 1987; Lacruz et al. 2006; Bromage et al. 2007; Tafforeau & Smith, 2008). The mean and modal value is 7 days. In our sample of fossil Homo (n = 7) the value is 8 days (see text and Table 5 for details).



155

rise to long-period striae are likely to have a similar aetiologyto that in modern humans (FitzGerald, 1998). Interestingly,other primates more distantly related to hominins, such asthe Madagascar lemurs, show markedly different periodic-ities. Schwartz et al. (2002, 2005) describe periodicities of2 and 3 days, respectively, for two species of lemurs thatranged in body mass from chimpanzee- to gorilla-like. Sucha marked difference in periodicity to those in hominoidspoints to a complex interplay between body mass and phy-logeny across the Primate order. A clearer understandingof the biological basis for the development of long-periodstriae in enamel is likely to shed more light on theseintriguing observations.

Besides providing a better understanding of the develop-mental processes involved in enamel formation amongfossil hominins, the results presented here may bear onissues of taxonomy. A previous study suggested that DSRswere inconclusive as a taxonomic indicator (Lacruz, 2007),but those results were based only on values obtained fora single molar tooth compared with a limited data setreported by Beynon & Wood (1987). The present study,however, with a much larger data set, permits a moreaccurate assessment of comparisons between taxa. Thedata on DSRs presented in Table 3 demonstrate muchvariation across taxa. However, some general observationscan be made that may be useful for assessing the taxo-nomic status of isolated teeth or fragments of teeth. Whenconsidering the outer cuspal values for instance (Table 4,Fig. 3), the differences that exist between the generaParanthropus and Homo are statistically significant in allcases (P < 0.05), and the same can be said for the differ-ences between A. africanus and Homo (P < 0.05). More-over, the three early Homo taxa do not appear to besignificantly different from each other in the outer cuspalenamel (Table 4), and although the A. anamensis meanvalues in that zone are slightly higher than in early Homo,this difference is not statistically significant (P > 0.05).In the case of H. rudolfensis, there are no significant differ-ences with A. anamensis or A. afarensis (P > 0.05). Differ-ences, however, are found when these two Australopithecustaxa are compared with their purported daughter speciesP. aethiopicus (P < 0.05). Previously, Beynon & Wood(1987) reported a DSR for Homo that, in the middle cuspalarea, was 5.8 μm day–1. However, based on data presentedhere (Table 3), this value appears to have been overestimated.

If the hypothesis suggested by data presented in thisstudy holds true, then faster DSRs in hominins are associ-ated with thicker enamel and slower DSRs with thinnerenamel, so long as life-history schedules are relativelyconstant. This allows us to make predictions about earlierhominins, such as Ardipithecus, which appear to havethinner enamel. For instance, based on the reported enamelthickness for Ardipithecus (White et al. 1994) we wouldexpect that this species would have slower DSRs than thosereported here for thick-enamelled taxa. Importantly, it

may now be possible to diagnose the taxonomic status ofisolated or fragmentary molar material with better resolu-tion than was possible before based on the analysis ofdaily incremental lines in enamel.

Conclusion

The results presented here show that when life-historyschedules are held constant, large thick-enamelled teethcomplete their crown formation in the same time as smallerthin-enamelled teeth through several processes. Of these,faster daily rates of enamel formation appear to be amongthe most important in hominins (Beynon & Dean, 1987;Beynon & Wood, 1987; Grine & Martin, 1988; Lacruz &Bromage, 2006). Slower daily rates of enamel formationare associated with thinner enamelled crowns among earlyhominins, but also with both the crowns of H. erectus, wheresome prolongation of the growth period had occurredwith respect to early australopithecines, and again withmodern H. sapiens, where the available time in the growthperiod is more than likely greater still than it was inH. erectus (Smith, 1993; Dean et al. 2001). We documentedperiodicity values for five Plio-Pleistocene hominin speciesfor which no data were available (A. afarensis, P. aethiopicus,H. rudolfensis, H. habilis and H. erectus), including additionalvalues for P. boisei for which only one recorded value wasknown (Beynon & Dean, 1987; Dean, 1987). Additionally,we show that significant correlations exist between long-period striae periodicity and estimates for male andaverage male–female body mass across the Plio-Pleistocenehominin taxa. Taken together with previous findings onlong-period stria periodicity in lemur species, this suggeststhat long-period stria periodicity in primates generally isan expression that involves a complex interplay betweenbody mass, phylogenetic relatedness and the physiologicalprocesses underlying their formation during enamel secre-tion. These new data on fossil hominin daily enamel secretionrates provide a clearer framework with which to interpretthe taxonomic attribution of fossil hominin molar teeth.

Acknowledgements

We would like to thank the Ethiopian Government, Mamitu Yilmaand staff at the Ethiopian National Museum, Addis Ababa, foraccess to the fossil material in their care. We acknowledge theGovernment of Kenya and the National Museums of Kenya forallowing us access to fossil material in their care and we thankEmma Mbua for enabling this research in the Department ofPalaeontology. We thank Friedemann Schrenk and the Forsc-hungsinstitut Senckenberg, Frankfurt am Main, Germany, forongoing access to fossil material. A. Chimenez is thanked fortechnical assistance. We are indebted to the Leakey Foundationand especially to Diana McSherry for their continuous financialcontributions that have made much of this work possible. R.L. isgrateful to the Palaeontological Scientific Trust (PAST) in SouthAfrica for financial assistance, and in particular to A. Leenen, C. &



156

M. Read, C. K. Brain, B. Rubidge and L. R. Berger for their enduringsupport. Aspects of this study were also supported by a grant toM.C.D. from The Leverhulme Trust. We thank two anonymousreviewers for providing useful comments on previous drafts of thispaper. Lastly, R.L. would like to express heartfelt gratitude to SariTaicher for her unwavering kindness and for the emotional andfinancial support, all of which is deeply appreciated.

References

Anemone RL (2002) Dental development and life history in hominidevolution. In Human Evolution through Developmental Change(eds Minugh-Purvis N, McNamara KJ), pp. 223–248. Baltimore:Johns Hopkins University Press.

Beynon AD, Dean MC (1987) Crown formation time of a fossilhominid premolar tooth. Arch Oral Biol 32, 773–780.

Beynon AD, Dean MC (1988) Distinct dental development patternsin early fossil hominids. Nature 335, 509–514.

Beynon AD, Wood B (1986) Variations in enamel thickness andstructure in East African hominids. Am J Phys Anthropol 70, 177–193.

Beynon AD, Wood B (1987) Patterns and rates of enamel growthon the molar teeth of early hominids. Nature 326, 493–496.

Beynon AD, Dean MC, Reid DJ (1991) On thick and thin enamel inhominoids. Am J Phys Anthropol 86, 295–310.

Boaz N (1977) Palaeoecology of Plio-Pleistocene Hominidae in theLower Omo Basin, Ethiopia. PhD Thesis, University of CaliforniaBerkeley.

Bowman E (1991) Life history, growth and development in youngprimates: a study using captive rhesus macaques. PhD Dissertation,University of Cambridge.

Boyde A (1989) Enamel. In Teeth. Handbook of Microscopic Anatomy,vol. 6 (eds Berkovizt BKB, Boyde A, Frank RM, Hohling HJ, MoxhamBJ, Nalbandian J, Tonge CH), pp. 309–473. Berlin: Springer-Verlag.

Bromage TG (1987) The biological and chronological maturationof early hominids. J Hum Evol 16, 257–272.

Bromage TG, Dean MC (1985) Re-evaluation of the age at death ofimmature fossil Hominids. Nature 317, 525–527.

Bromage TG, Lacruz RS, Perez-Ochoa A, Boyde A (2007) Portableconfocal scanning optical microscopy of Australopithecus africanusenamel microstructure. In Dental Palaeoanthropology (edsBailey S, Hublin JJ), pp. 191–207. Berlin: Springer-Verlag.

Bromage TG, Perez-Ochoa A, Boyde A (2005) Portable confocalmicroscope reveals fossil hominid microstructure. Microsc Anal19, 5–7.

Bromage TG, Schrenk F, Zonneveld FW (1995) Paleoanthropologyof the Malawi Rift: an early hominid mandible from the ChiwondoBeds, northern Malawi. J Hum Evol 28, 71–108.

Dean MC (1987) Growth layers and incremental markings in hardtissues, a review of the literature and some preliminary observationsabout enamel structure of Paranthropus boisei. J Hum Evol 16,157–172.

Dean MC (1998) A comparative study of cross striation spacing incuspal enamel and four methods of estimating the time takento grow molar cuspal enamel in Pan, Pongo and Homo. J HumEvol 35, 449–463.

Dean MC (2000) Progress in understanding hominoid dentaldevelopment. J Anat 197, 77–101.

Dean MC (2006) Tooth microstructure tracks the pace of humanlife-history evolution. Proc Royal Soc B 273, 2799–2808.

Dean MC, Reid DJ (2001) Perikymata and distribution on Hominidanterior teeth. Am J Phys Anthropol 116, 209–215.

Dean MC, Schrenk F (2003) Enamel thickness and development ina third permanent molar of Gigantopithecus blacki. J Hum Evol45, 381–387.

Dean MC, Beynon AD, Thackeray JF, Macho GA (1993) Histologicalreconstruction of dental development and age at death of ajuvenile Paranthropus robustus specimen, SK 63, fromSwartkrans, South Africa. Am J Phys Anthropol 91, 401–419.

Dean MC, Leakey M, Reid D, et al. (2001) Growth processes inteeth distinguish modern humans from Homo erectus andearlier hominins. Nature 44, 628–631.

Dirks W (1998) Histological reconstruction of dental developmentand age at death in a juvenile gibbon (Hylobates lar). J Hum Evol35, 411–426.

FitzGerald CM (1998) Do enamel microstructures have regulartime dependency? Conclusions from the literature and a large-scale study. J Hum Evol 35, 371–386.

Grine FE, Martin LB (1988) Enamel thickness and development inAustralopithecus and Paranthropus. In The Evolutionary Historyof the Robust Australopithecines (ed. Grine FE), pp. 3–42.Aldyne de Gruiter.

Hlusko LJ, Suwa G, Kono RT, Mahaney MC (2004) Genetics and theevolution of primate enamel thickness: a baboon model. Am JPhys Anthropol 124, 223–233.

Johanson DC, White TD, Coppens Y (1982) Dental remains fromthe Hadar Formation, Ethiopia: 1974–1977 Collections. Am JPhys Anthropol 57, 545–603.

Kelley J, Smith TM (2003) Age at first molar emergence in earlyMiocene Afropithecus turkenensis and life history evolution inthe Hominoidea. J Hum Evol 44, 307–329.

Lacruz RS (2006) Primate enamel development with emphasis onSouth African Plio-Pleistocene hominins. PhD Dissertation,University of the Witwatersrand.

Lacruz RS (2007) Enamel microstructure of the hominin KB 5223from Kromdraai, South Africa. Am J Phys Anthropol 132,175–182.

Lacruz RS, Bromage TG (2006) Appositional enamel growth inmolars of South African fossil hominids. J Anat 209, 13–20.

Lacruz RS, Ramirez Rozzi FV, Bromage TG (2005) Linear enamelhypoplasia, weaning, and age at death in the Taung child. S AfrJ Sci 101, 567–569.

Lacruz RS, Ramirez Rozzi FV, Bromage TG (2006) Variation inenamel development of South African fossil hominids. J HumEvol 51, 580–590.

Macchiarelli R, Bondioli L, Debénath A, et al. (2006) How Neanderthalmolar teeth grew. Nature 444, 748–751.

Macho GA, Thackeray JF (1992) Computed tomography andenamel thickness of maxillary molars of Plio-Pleistocene hominidsfrom Sterkfontein, Swartkrans and Kromdraai (South Africa): anexploratory study. Am J Phys Anthropol 89, 133–143.

Martin LB (1985) Significance of enamel thickness in hominoidevolution. Nature 314, 260–263.

McHenry HM (1984) Relative cheek-tooth size in Australopithecus.Am J Phys Anthropol 64, 297–306.

McHenry HM (1988) New estimates of body weight in early hominidsand their significance to encephalization and megadontia in‘Robust’ Australopithecus. In The Evolutionary History of theRobust Australopithecines (ed. Grine FE), pp. 133–148. Aldynede Gruiter.

McHenry HM (1992) Body size and proportions in early hominids.Am J Phys Anthropol 87, 407–431.

McHenry HM (2002) Introduction to the fossil record of humanancestry. In The Primate Fossil Record (ed. Hertwig C), pp. 401–405. Cambridge: Cambridge University Press.



157

Molnar S, Gantt DG (1977) Functional implications primate enamelthickness. Am J Phys Anthropol 46, 447–454.

Ramirez Rozzi FV (1993a) Tooth development in East AfricanParanthropus. J Hum Evol 24, 429–454.

Ramirez Rozzi FV (1993b) Microstructure et développement del’émail dentaire du néandertalien de Zafarraya, Espagne. Tempsde formation et hypocalcification de l’émail dentaire. C. R. AcadSci Paris 316, 1635–1642.

Ramirez Rozzi FV (1995) Time of formation in Plio-PleistoceneHominid teeth. In Aspects of Dental Biology: Palaeontology,Anthropology and Evolution (ed. Moggi-Cecchi J), pp. 217–238.Florence: International Institute for the study of Man.

Ramirez Rozzi FV, Bermudez de Castro JM (2004) Surprisinglyrapid growth in Neanderthals. Nature 428, 936–939.

Reid DJ, Dean MC (2006) Variation in modern human enamel for-mation times J Hum Evol 50, 329–346.

Schwartz GT (2000) Taxonomic and functional aspects of the pat-terning of enamel thickness distribution in extant and large-bodied hominoids. Am J Phys Anthropol 111, 221–244.

Schwartz GT, Mahoney P, Godfrey LR, Cuozzo FP, Jungers WL,Randria GFN (2005) Dental development in Megaladapisedwardsi (Primates, Lemuriformes): implications for under-standing life history variation in subfossil lemurs J Hum Evol 49,702–721.

Schwartz GT, Reid DJ, Dean MC (2001) Developmental aspects ofsexual dimorphism in hominoid canines. Int J Primatol 22, 837–860.

Schwartz GT, Samonds KE, Godfrey LR, Jungers WL, Simmons EL(2002) Dental microstructure and life history in subfossil Malagasylemurs. Proc Natl Acad Sci USA. 99, 6124–6129.

Smith BH (1993) The physiological age of KNM-WT 15000. In TheNariokotome Homo erectus Skeleton (eds Walker A, Leakey R),pp 195–220. Cambridge, MA: Harvard University Press.

Smith TM (2008) Incremental dental development: methods andapplications in hominoid evolutionary studies J Hum Evol 54,205–224.

Smith TM, Martin LB, Leakey MG (2003) Enamel thickness,

microstructure and development in Afropithecus turkanensis.J Hum Evol 44, 283–306.

Smith TM, Martin LB, Reid DJ, de Bonis L, Koufos GD (2004) Anexamination of dental development in Graecopithecus freybergi(= Ouranopithecus macedoniensis). J Hum Evol 46, 551–577.

Smith TM, Tafforeau P, Reid DJ, et al. (2007a) Earliest evidence ofmodern human life history in North African early Homo sapiens.Proc Natl Acad Sci USA 104, 6128–6133.

Smith TM, Reid DJ, Dean MC, Olejniczak AJ, Martin LB (2007b)Molar development in common chimpanzees (Pan troglodytes).J Human Evol 52, 201–216.

Smith TM, Reid DJ, Dean MC, Olejniczak AJ, Ferrell RJ, Martin LB(2007c) New perspectives on chimpanzee molar crown development.In Dental Palaeoanthropology (eds Bailey S, Hublin JJ), pp. 177–192. Berlin: Springer-Verlag.

Suwa G, Wood BA, White TD (1996) Further analysis of mandibularmolar crown and cusp areas in Pliocene and early Pleistocenehominids. Am J Phys Anthropol 93, 407–426.

Swindler DR, Beynon AD (1993) The development and microstructureof the dentition of Theropithecus. In Theropithecus: The Riseand Fall of a Primate Genus (ed. Jablonski NG), pp. 351–381.Cambridge: Cambridge University Press.

Tafforeau P, Smith TM (2008) Nondestructive imaging of hominoiddental microstructure using phase contrast X-ray synchrotronmicrotomography. J Hum Evol 54, 272–278.

Teaford MF, Ungar PS (2000) Diet and evolution of the earliesthuman ancestors. Proc Natl Acad Sci USA 97, 13506–13511.

Ward CV, Leakey M, Walker A (2001) Morphology of Australopithecusanamensis from Kanapoi and Allia Bay, Kenya. J Hum Evol 41,255–368.

White TD, Suwa G, Asfaw B (1994) Australopithecus ramidus, anew species of early hominid from Aramis, Ethiopia. Nature 371,306–312.

Williams JL (1897) A contribution to the study of pathology ofenamel. Dental Cosmos 391.

Wood BA (1992) Origin and early evolution of genus Homo.Nature 355, 783–790.



158

Appendix 1 Full list of specimens used to obtain DSRs for each species shown in Table 3. Standard deviations are in parentheses

Specimen/taxa cu.out cu.mid cu.inn lat.out lat.mid lat.inn cer.out cer.inn

Australopithecus anamensisKNM-ER 30748* 4.67 (0.12) 5.34 (0.57) 3.78 (0.35) ? ? ? ? ?KNM-ER 30749* 5.96 (0.40) 4.74 (0.61) 4.42 (0.28) ? ? ? ? ?

Australopithecus anamensisAL-333-52 5.32 (0.38) 4.48 (0.36) 3.91 (0.31) 4.79 (0.36) 4.48 (0.28) 3.52 (0.28) ? ?AL-366 6.05 (0.47) 4.98 (0.40) 2.88 (0.23) 5.50 (0.50) 4.86 (0.14) ? 4.19 (0.25) 3.22 (0.55)L-2-79 (OMO) 6.16 (0.37) 4.54 (0.22) 3.14 (0.25) 5.67 (0.42) 4.95 (0.24) 3.85 (0.29) ? ?

Paranthropus aethiopicusF-22 6.53 (0.36) 5.51 (0.23) 3.59 (0.42) 5.52 (0.39) 4.86 (0.36) 3.18 (0.24) 4.81 (0.24) 2.89 (0.23)

Paranthropus boiseiOMO 46-47 7.36 (0.28) 5.54 (0.20) ? 5.79 (0.27) ? 3.44 (0.10) 4.58 (0.30) 2.99 (0.51)OMO 76-37 7.03 (0.28) 5.48 (0.32) 3.0 (0.29) 5.55 (0.52) 4.57 (0.37) ? 4.23 (0.27) ?OMO 136-1 7.08 (0.28) ? 2.92 (0.10) 5.74 (0.34) ? ? 4.68 (0.34) ?L 209-17 7.10 (0.37) 6.59 (0.30) 2.87 (0.18) 6.05 (0.44) 5.41 (0.36) ? 4.82 (0.35) ?L-398-847 ? 5.39 (0.24) 2.89 (0.23) 6.05 (0.09) ? ? 4.20 (0.21) 2.93 (0.48)OMO 47-47 ? ? ? ? ? ? ? 3.31 (0.26)

Homo rudolfensisKNM-ER 1483* 5.26 (0.20) ? ? 4.67 (0.12) ? ? 3.66 (0.43) ?KNM-ER 1482 5.06 (0.25) 4.35 (0.18) 3.69 (0.21) ? ? ? ? ?KNM-ER 1802 5.77 (0.36) 4.96 (0.36) 2.77 (0.26) 4.96 (0.26) 3.79 (0.17) 2.92 (0.22) ? ?

Homo habilisKNM-ER 1805* 5.21 (0.14) 4.60 (0.30) 3.68 (0.19) 5.30 (0.20) 5.04 (0.16) 3.47 (0.25) ? ?

Homo erectusKNM-ER3733 5.28 (0.35) 4.54 (0.42) 4.0 (0.19) ? ? ? ? ?S7-37* 5.14 (0.35) 4.42 (0.29) 2.70 (0.26) ? ? ? ? ?

*Specimens studied using polarizing microscopy of ground sections; the remaining specimens studied using portable confocal scanning optical microscopy. Enamel regions: cu = cuspal; lat = lateral; cer = cervical; out = outer; mid = middle; inn = inner. Interrogation signs indicate that we were unable to obtain values in that region of the crown.

Megadontia, striae periodicity and patterns of enamel secretion in Plio-Pleistocene fossil hominins

Documents

Transcript of Megadontia, striae periodicity and patterns of enamel secretion in Plio-Pleistocene fossil hominins