Enamel thickness, microstructure and development in Afropithecus turkanensis

Journal of Human Evolution 44 (2003) 283–306

Enamel thickness, microstructure and development in Afropithecus turkanensis Tanya M. Smith 1*, Lawrence B. Martin 2, Meave G. Leakey 3 1

Interdepartmental Doctoral Program in Anthropological Sciences, Department of Anthropology, Stony Brook University, Stony Brook, NY 11794-4364, USA 2 Departments of Anthropology and of Anatomical Sciences, Stony Brook University, Stony Brook, NY 11794-4364, USA 3 Department of Palaeontology, National Museums of Kenya, P.O. Box 40658, Nairobi, Kenya Received 12 June 2002; accepted 14 November 2002

Abstract Afropithecus turkanensis, a 17–17.5 million year old large-bodied hominoid from Kenya, has previously been reported to be the oldest known thick-enamelled Miocene ape. Most investigations of enamel thickness in Miocene apes have been limited to opportunistic or destructive studies of small samples. Recently, more comprehensive studies of enamel thickness and microstructure in Proconsul, Lufengpithecus, and Dryopithecus, as well as extant apes and fossil humans, have provided information on rates and patterns of dental development, including crown formation time, and have begun to provide a comparative context for interpretation of the evolution of these characters throughout the past 20 million years of hominoid evolution. In this study, enamel thickness and aspects of the enamel microstructure in two A. turkanensis second molars were quantified and provide insight into rates of enamel apposition, numbers of cells actively secreting enamel, and the time required to form regions of the crown. The average value for relative enamel thickness in the two molars is 21.4, which is a lower value than a previous analysis of this species, but which is still relatively thick compared to extant apes. This value is similar to those of several Miocene hominoids, a fossil hominid, and modern humans. Certain aspects of the enamel microstructure are similar to Proconsul nyanzae, Dryopithecus laietanus, Lufengpithecus lufengensis, Graecopithecus freybergi and Pongo pygmaeus, while other features differ from extant and fossil hominoids. Crown formation times for the two teeth are 2.4–2.6 years and 2.9–3.1 years respectively. These times are similar to a number of extant and fossil hominoids, some of which appear to show additional developmental similarities, including thick enamel. Although thick enamel may be formed through several developmental pathways, most Miocene hominoids and fossil hominids with relatively thick enamel are characterized by a relatively long period of cuspal enamel formation and a rapid rate of enamel secretion throughout the whole cusp, but a shorter total crown formation time than thinner-enamelled extant apes.  2003 Elsevier Science Ltd. All rights reserved. Keywords: Afropithecus turkanensis; Miocene hominoid; enamel thickness; enamel microstructure; crown formation time; daily secretion rate; Retzius line; cross-striation; lamination; intradian line

* Corresponding author. Tel.: +1-(631)-632-1364; fax: +1-(631)-632-9165 E-mail addresses: [email protected] (T.M. Smith), [email protected] (L.B. Martin). 0047-2484/03/$ - see front matter  2003 Elsevier Science Ltd. All rights reserved. doi:10.1016/S0047-2484(03)00006-X

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Introduction Miocene hominoids and enamel development Leakey and Leakey (1986) first described Afropithecus turkanensis as a large-bodied early Miocene hominoid from northern Kenya dated between 17 to 17.5 mya, which appeared to have relatively thick enamel. Leakey et al. (1988) suggested that A. turkanensis shared postcranial features with Proconsul nyanzae, cranial features with Aegyptopithecus zeuxis, and dental features with Heliopithecus leakeyi, Kenyapithecus sp., and the large hominoid material from Moroto and Napak. Leakey and Walker (1997) recently reviewed this evidence and concluded that A. turkanensis was a primitive, arboreal quadruped similar to P. nyanzae, with a primitive facial morphology and derived dental characteristics specialized for a diet of hard fruits, which was similar to fossils from Maboko Island attributed to Kenyapithecus (since assigned to Equatorius africanus by Ward et al., 1999). Sherwood et al. (2002) suggested, based on an analysis of the partial skeleton of E. africanus from the Tugen Hills, that postcranial similarities between early Miocene apes Proconsul and A. turkanensis and the more terrestrial Equatorius are shared primitive features that do not indicate a close taxonomic affiliation. The thickness of molar enamel is often reported in descriptions of fossil material. Enamel thickness is commonly assessed as a linear measurement of enamel visible in worn or naturally fractured teeth, and is generally characterized as ‘thick’ or ‘thin’. Martin (1983) demonstrated that it was difficult to assess enamel thickness from exposed enamel accurately, and measured thickness from a buccallingual section cut across the mesial cusp tips, which could be scaled with a surrogate for body size to make comparisons across taxa (Martin, 1983, 1985; Grine and Martin, 1988; Andrews and Martin, 1991). In the first comparative synthesis of relative enamel thickness among several Miocene hominoids, Andrews and Martin (1991) reported values ranging from 8.5 for P. africanus (categorized as having thin enamel) to 28.3 for Graecopithecus freybergi (considered thick-hyper

thick enamel). They suggested that thin enamel was the primitive condition for Miocene hominoids, which was supported by data from two species of Proconsul, as well as data on Hylobates and cercopithecoids (Martin, 1983, 1985). Martin (1995) suggested that A. turkanensis is the oldest known thick-enamelled hominoid, although he did not provide a value for relative enamel thickness. Leakey and Walker (1997) also cite personal communication with Martin that this species had extremely thick molar enamel, which they suggested distinguished it from Kenyapithecus. Although it was not the intent of this study to examine the phylogenetic utility of enamel thickness, information on relative enamel thickness in fossil and living hominoids is reviewed and revised below to provide a comparative framework for the interpretation of the two Afropithecus molars examined in this study, which is then related to information on enamel microstructure. Together, these variables may provide a more complete picture of the dental development of this early Miocene ape, which may shed light on additional aspects of its paleobiology (Kelley and Smith, 2003). Since the publication of the first few studies of incremental enamel microstructure in extant apes (e.g., Fukuhara, 1959; Shellis and Poole, 1977; Dean and Wood, 1981), there has been a dramatic increase in the number of studies on hominoids during the past two decades. Martin (1983) undertook the first examination of fossil hominoids, including Sivapithecus and some material from Pas¸alar, Turkey that is currently attributed to Griphopithecus. Bromage and Dean (1985) reassessed the age at death of fossil hominids using incremental features, and concluded that early humans were characterized by ape-like dental development, in contrast to the previously assumed modern human pattern. These were followed by many more studies of fossil hominids that examined the nature of enamel development and enamel thickness as revealed by microstructure (Beynon and Wood, 1986; Dean et al., 1986; Beynon and Dean, 1987; Beynon and Wood, 1987; Dean, 1987a,b; Beynon and Dean, 1988; Grine and Martin, 1988; Mann et al., 1991; Beynon, 1992; Dean et al., 1993a; Ramirez Rozzi, 1993a,b; Mann

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et al., 1994; Ramirez Rozzi, 1994; Dean, 1995; Ramirez Rozzi, 1997; Ramirez Rozzi et al., 1997; Ramirez Rozzi, 1998; Dean et al., 2001; Dean and Reid, 2001). These investigations have provided information on age at death in individuals with developing dentitions, the absolute and relative timing of dental development, differences in the developmental pathways of enamel formation, and life history characteristics. Recent work on extant and fossil apes has begun to provide an improved comparative framework to complement the results of studies of fossil hominoids (Beynon et al., 1991a,b; Beynon and Reid, 1995; Reid and Beynon, 1995; Kelley, 1997; Beynon et al., 1998; Dean, 1998; Dean and Shellis, 1998; Dirks, 1998; Reid et al., 1998a; Kelley, 1999; Schwartz et al., 1999; Dean, 2000; Kelley and Bulicek, 2000; Smith and Martin, 2000; Kelley et al., 2001; Schwartz and Dean, 2001; Schwartz et al., 2001a,b; Smith et al., 2001; Dirks, 2002; Kelley and Smith, 2003; Schwartz et al 2003; Smith et al., 2003). Beynon et al. (1998) examined the enamel and dentine microstructure of two species of Proconsul from Rusinga Island. They found some features to be most similar to Pongo, while other similarities were found with Pan and Homo. Kelley et al. (2001) reported developmental similarities among Dryopithecus laietanus, Pan, and P. nyanzae. Schwartz et al. (2003) reported differences in both microstructure and enamel thickness between Lufengpithecus lufengensis and L. hudienensis, with the latter showing some similarities to species of Proconsul and Pongo. Additional ongoing work on other Miocene taxa, as well as on a large sample of extant apes, may permit more refined assessment of the significance of comparisons of limited fossil material, as well as on changes in hominoid dental development through time (Smith et al., 2003). The present study quantifies the molar relative enamel thickness of A. turkanensis, provides information on several classes of incremental features of enamel microstructure, and provides estimates of crown formation time derived from two lower second molars. Polarized light microscopy, scanning electron microscopy and tandem scanning reflected (confocal) light microscopy are used to generate complementary data on aspects of enamel

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development in A. turkanensis, as well as insight into specific methodological issues. These data are compared with those of other hominoids in an attempt to understand the developmental basis of various patterns of enamel thickness. Development of enamel microstructure Enamel development is characterized by the production of long- and short-period incremental lines that are formed in the enamel prisms, representing rhythmic changes or disturbances in enamel secretion (Fig. 1). Long-period lines, known as striae of Retzius in cross section, represent the two dimensional position of the entire enamel forming front at a given point in time. Crown growth in height occurs in two ways: as a cervical extension of newly differentiated enamel forming cells (ameloblasts) along the enamel dentine junction (EDJ), and in an appositional manner as the ameloblasts move away from the EDJ. Boyde (1964) suggested that the angles where Retzius lines intersect the EDJ provide evidence of the differentiation rate of new cells, with a smaller angle indicating a faster rate. The first formed long-period lines over the dentine horns do not meet the enamel surface, creating appositional or cuspal enamel. Later-formed Retzius lines extend to the surface of the tooth and form perikymata, which are circumferential imbrications in the lateral enamel surface. This region is referred to as the lateral or imbricational enamel. Short-period lines, known as cross-striations, are the result of rhythmic changes in enamel production that manifest in prisms perpendicular to the long axis. Numerous studies have demonstrated that cross-striations show a circadian repeat interval (see FitzGerald, 1998 for a review). As the time of formation between regularly spaced Retzius lines is uniform within all teeth of the same individual, many studies have used the number of cross-striations between adjacent Retzius lines, termed the periodicity, in conjunction with the number of Retzius lines, to reconstruct an individual’s age at death and/or the duration of crown formation. Recent work on several extant hominoids has demonstrated that this rhythm may

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Fig. 1. Schematic molar cross-section showing incremental features and regions of the enamel microstructure in Afropithecus turkanensis (KNM-WK 24300). Enamel prisms extend from the enamel dentine junction (EDJ) to the tooth surface and preserve longand short-period features. Striae of Retzius are long-period lines that run obliquely from the EDJ to the surface and represent the regular position of the enamel forming front at one moment in time. Cross-striations are short-period lines that cross enamel prisms perpendicularly and represent the daily secretion of the enamel forming cells. The box in the upper right shows the periodicity, or consistent relationship of cross-striations between pairs of Retzius lines. The crown may be divided into cuspal and imbricational enamel regions, which are distinguished from one another by the first stria to reach the surface of the tooth. Separate methods are used to determine the crown formation time in these two regions (see text). (Modified from Ramirez Rozzi, 1994.)

range from 6 to 12 days among taxa (Dean and Reid, 2001; Schwartz et al., 2001a; Reid et al., 2002). Additional extra-short-period features between cross-striations, known as ultradian or intradian lines, have been described as fine bands that divide cross-striations into two or three segments (Gustafson and Gustafson, 1967; Dean, 1995; Dean and Scandrett, 1996; FitzGerald, 1996). There are currently no empirical data concerning the periodicity or causation of intradian lines in enamel, although there is evidence of an 8–12 h secretion rhythm in dentine (Rosenberg and Simmons, 1980; Ohtsuka and Shinoda, 1995). More detailed reviews of enamel microstructure may be found in Boyde (1989), Risnes (1998) and standard texts such as Aiello and Dean (1990), Hillson (1996), and Ten Cate (1998).

Materials and methods Two teeth attributed to A. turkanensis were examined in this study: an isolated LM2 (KNM-WK 17024) and a single RM2 (KNM-WK 24300) that is associated with other mandibular and maxillary teeth from Kalodirr. Both teeth were sectioned in a buccal-lingual plane through the mesial cusps. Prior to this study, the talonid basin of KNM-WK 24300 was accidentally fractured during transport, also in a buccal-lingual plane, providing a further, naturally fractured surface for study. Prior to sectioning, molds of both teeth were created with Coltene President impression material, which will permit accurate reconstruction. The teeth were first refluxed and embedded in methyl methacrylate according to procedures

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described by Boyde (1989). Longitudinal cuts across the mesial cusps were made using a Unipress wire saw, which destroys approximately 50 µm of enamel per cut. Thin sections approximately 100 µm thick were cut from each tooth and glued onto microscope slides. These were ground and polished to a 40–60 µm thickness using a Buehler Metaserv grinder-polisher and finished with a 0.3 µm alumina suspension on a polishing cloth. Sections were then ultrasonicated, cleaned with alcohol, cleared in xylene, and cover slips were mounted with DPX mounting media (Fluka Chemicals). Photomontages of both sections were generated with 6.3, 12.5 and 25 objectives on a Zeiss polarizing light microscope (PLM). Images were also digitally captured with a Hitachi KP-C553 CCD color camera, and NIH Image software was used for all measurements. The remaining blocks, which represented the faces immediately anterior and posterior to the thin section taken from the mesial cusps of each tooth, were briefly polished with a series of finer grades of diamond abrasive (6 µm, 1 µm, 0.25 µm), lightly etched with dilute phosphoric acid, dried and sputter coated with silver. The fractured distal half of the talonid basin of KNM-WK 24300 was not embedded, polished, or etched, but was glued to a stub and coated with a thin layer of gold. The blocks were examined using back-scattered electron and secondary electron imaging in an Amray 1810 scanning electron microscope (SEM). Overviews of each block face were generated at low magnification, and montages of portions of both crowns were also generated at 250 and 350. Thin sections and block faces were also examined and photographed under a tandem scanning reflected light microscope (TSRLM), built by Milan Hadravsky. The TSRLM is a confocal imaging system that provides focal plane specific information about subsurface structures to a depth of approximately 100–150 µm (Petran et al., 1985). Digital overviews of all blocks and thin sections were also generated with a Nikon Coolpix 995. Relative enamel thickness Enamel thickness was measured on each tooth from enlarged overviews of the two exposed block

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faces of the mesial cusps and the thin section, in accordance with methods developed by Martin (1983) (Fig. 2). Measurements were made on a digitizing tablet with SigmaScan Pro software. Relative enamel thickness was calculated by dividing the area of the enamel cap (c) by the length of the enamel dentine junction (EDJ) (e), and this quantity was then divided by the square root of the area of the dentine (b) and finally multiplied by 100. This provides a dimensionless index of enamel thickness that is suitable for comparisons across taxa. The section of each tooth that showed the lowest relative enamel thickness was considered closest to the ‘ideal plane of section’ which passes through the tip of the dentine horns (minimizing obliquity). These two sections were used to calculate the average relative enamel thickness. As shown in Fig. 2, the enamel outline of the broken cervices of KNM-WK 17024 and the tip of the protoconid of KNM-WK 24300 were reconstructed due to fractured enamel and light attrition. To compensate for a fracture through the occlusal basin of KNM-WK 17024, the area and length represented by the gap between the two halves was subtracted from the total measurements. Enamel and dentine microstructure Several aspects of enamel microstructure were quantified in both teeth: periodicity, daily secretion rate, and angle of Retzius lines at the EDJ. In addition, imbricational, cuspal, and total crown formation times were determined (discussed in the following section). The periodicity (number of cross-striations between Retzius lines) was determined using two methods (Dean et al., 1993b; Swindler and Beynon, 1993). Where possible, direct counts were made of cross-striations between Retzius lines that clearly met the surface of the enamel (in contrast to other variable parallel accentuated lines). Additionally, the average spacing of the Retzius lines was divided by the average spacing of cross-striations measured from prisms in that immediate area. These two methods were also applied where possible to incremental lines in the dentine of KNM-WK 17024, as the relationship between long-period (Andresen) and shortperiod (von Ebner) lines in the dentine is

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Fig. 2. (a–d). Two Afropithecus turkanensis teeth showing reconstructions of the enamel cap and measurements used to determine the relative enamel thickness. The upper two sections represent the anterior (a) and posterior (b) faces of the mesial cusps of KNM-WK 17024 (LM2). The lower two sections represent the anterior (c) and posterior (d) faces of the mesial cusps of KNM-WK 24300 (RM2). Reconstructions of the original enamel cap were made at the cervices of KNM-WK 17024 and the tip of the protoconid of KNM-WK 24300. In (d) the area of the enamel cap is represented as c, the area of the dentine under the enamel cap is represented as b, and the length of the enamel dentine junction is represented as e. The relative enamel thickness may be calculated as ((c/e)/#b)*100. (SEM images with 1 mm scale bar shown beneath each section.)

equivalent to those in the enamel (Dean et al., 1993b; Dean, 1995). Daily secretion rate (DSR) was measured from the spacing of thousands of cross-striations throughout the enamel of both thin sections with a 50 objective under the PLM. Cross-striations were defined as light/dark band units rather than as prism varicosities/constrictions. Measurements are reported according to the region within the enamel cap: cuspal inner, middle, and outer thirds; lateral inner, middle, and outer thirds; and cervical inner and outer halves. Intradian lines were intentionally avoided when determining the DSR, particularly in certain subsurface regions that showed highly variable, closely spaced features. They were recognized as fine bands that appeared between square/slightly rectangular light and dark bands (cross-striations). In an attempt to clarify these poorly studied features, the position and

nature of intradian lines was noted and photographed. In addition, general observations were made on the appearance of Retzius lines and the presence of aprismatic enamel. The angle of intersection between the striae of Retzius and the EDJ was also measured in cuspal, lateral, and cervical regions of the protoconid and metaconid in each thin section. Repeated measurements were taken very close to the point of contact between the Retzius line and the EDJ, and averaged values and ranges are reported. Crown formation time Histological determination of crown formation time is most commonly accomplished by combining the time of imbricational enamel formation with the time of cuspal enamel formation. Determination of imbricational enamel formation time

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involves counting the number of Retzius lines that reach the surface as perikymata, and multiplying this number by the periodicity. In the thin section of KNM-WK 17024, it was only possible to count the number of Retzius lines in the protoconid, as a large portion of the cervix of the metaconid was missing. Two methods were employed to determine the amount of lost enamel. First, an accentuated line was found in the dentine that most likely intersected the EDJ at or near the point of crown completion, indicating the original position of the end of the cervical enamel (Reid, pers. comm.). The length of dentine tubules was measured from the EDJ at the position of the break in the enamel to the accentuated dentine line, and then divided by the average local dentine DSR to yield a time in days. To verify this estimate, the number of long-period lines within this interval was counted and multiplied by the periodicity. Both methods yielded similar results. In the enamel of KNM-WK 24300, the tip of the cervix of the metaconid was broken off, which was estimated to contain five to six striae that were added to the number observed. This estimate was derived from studies of the identical region of more complete hominoid material. Information from the dentine was not available in this tooth due to poor dentine preservation. The results for total number of Retzius lines are presented as a narrow range, due to the difficulty of determining the first stria to reach the surface (which delineates the boundary between imbricational and cuspal enamel), and the estimation of the tip of each metaconid. The issue of determining the cuspal enamel formation time has historically been the most difficult aspect of histological reconstruction, and several researchers have employed a number of methods. Estimates derived from different methods may vary by a few weeks to several months. Massler and Schour (1946) proposed that the duration of formation could be determined by dividing the length of the enamel prism from the EDJ to the tooth surface by the ‘characteristic rate of apposition’, or DSR. Risnes (1986) demonstrated that, because the prisms follow a sinusoidal course through the enamel, the linear enamel thickness must be corrected by a factor to yield the

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length of enamel prisms. He proposed a correction factor of 1.15 for multidimensional movement, derived from an empirical model of prism path in the lateral enamel of human premolars. In this study, cuspal enamel formation was determined by two similar methods, and compared to values obtained by applying Risnes’ correction factor. The first method involves the generation of a species-specific correction factor derived from each cusp. SEM montages (at 350) were made of the less oblique section of both cusps from each tooth. Tracings of several cohorts of prisms were made from the EDJ to the tooth surface, and the average length of three ‘path length’ tracings was divided by the linear cuspal enamel thickness, producing a ratio of two-dimensional prism deviation (or sinuosity). This deviation ratio was then doubled to compensate for the actual course of prisms three-dimensionally, which results in a factor that is slightly more conservative than that of Risnes’ (1986) calculations. Cuspal enamel formation time was calculated by multiplying the linear cuspal enamel thickness by this factor, which was then divided by the average cuspal DSR to produce a value for days of formation. A second method, based on work by FitzGerald et al. (1999), was employed for each protoconid, as this cusp is more relevant for the determination of total crown formation time and crossstriations were more visible than in the respective metaconid. FitzGerald et al. (1999) demonstrated that, in teeth that do not show a continuous series of cross-striations from the EDJ to the tooth surface, approximations of the number of cross-striations could be made using intervals along this distance. This involved dividing up the prism path length into 20 successive intervals (each representing 5% of the total length), determining the average DSR from as many crossstriations as may be measured within each interval, and then dividing the interval length by each average DSR, which yielded a time in days that was summed for the total time of cuspal enamel formation. Because it was difficult to assess the DSR in the final region of cuspal enamel due to light attrition and additional short-period features, the DSR from the adjacent zone was used as the divisor for this region.

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Table 1 Relative enamel thickness (RET) values for Afropithecus turkanensis KNM-WK

Face

b

c

e

c/e

((c/e)/#b)*100=RET

17024-LM2

anterior thin section posterior

24.57 26.32 27.71

16.21 16.52 17.99

15.35 16.14 15.93

1.06 1.02 1.13

21.37 19.88 21.48

24300-RM2

anterior thin section posterior

29.65 30.83 30.58

20.54 20.18 19.73

15.66 15.89 15.43

1.31 1.27 1.28

24.04 22.88 23.15 Mean 21.38

b=area of dentine under the enamel cap, c=area of enamel, e=length of enamel dentine junction. Values of b and c are in mm2, e is in mm. The final column, relative enamel thickness, is dimensionless. The mean reported was derived from averaging the two bold values as these sections showed a minimum relative enamel thickness and were considered closest to the ideal plane of section.

Due to the fact that all cusps within an individual tooth do not begin and end enamel formation at the same time, the order of initiation and completion must be considered when reporting the total crown formation time (Beynon et al., 1998). Histological studies of humans and chimpanzees have shown that the protoconid initiates first and takes longer to form than the metaconid, and that the last mandibular cusp to complete calcification is the hypoconid (Reid et al., 1998a,b). Total crown formation times in both A. turkanensis M2s were determined by adding the time of protoconid formation (imbricational plus cuspal enamel) to an estimate of 0.1 years for the final (nonoverlapping) period of hypoconid formation. This estimate is derived from histological studies of humans and chimpanzees (Reid et al., 1998a,b), and is assumed to apply to other large bodied hominoids. It is critical that differences between cusps are considered when total crown formation times are reported, as a number of previous studies do not specify which cusps were used to determine these values and may not be directly comparable.

Results Relative enamel thickness The relative enamel thickness values for the two teeth are reported in Table 1. The average value for A. turkanensis is 1.38. Table 2 shows that A.

turkanensis is one of the oldest known hominoids with relatively thick enamel; however, it is not as thick as was suggested by Martin (1995). Reexamination of the original figures and data has shown that Martin miscalculated relative enamel thickness, leading him to conclude that A. turkanensis had very thick enamel. The present results indicate that enamel thickness in A. turkanensis is similar to that of several other hominoids such as Griphopithecus sp., Sivapithecus sivalensis, P. nyanzae, and Australopithecus africanus, as well as to modern Homo sapiens (Martin, 1983; Grine and Martin, 1988; Andrews and Martin, 1991; Beynon et al., 1998). Enamel and dentine microstructure Counts and measurements made in both enamel and dentine show a periodicity of seven in KNM-WK 17024 and eight in KNM-WK 24300 (Fig. 3). The range of periodicities in A. turkanensis overlaps with those of most hominoids and some large cercopithecoids (Table 3). Table 4 shows the average DSR in the inner, middle, and outer zones of the cuspal, lateral, and cervical regions. The average DSR in these zones ranges from 3.46–5.54 µm and 3.27–5.26 µm for KNM-WK 17024 and KNM-WK 24300 respectively. The combined average DSR range of both teeth is 3.38–5.12 µm. Rates generally increase from inner to outer zones and from cervical to

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Table 2 Average relative molar enamel thickness (RET) in extant and fossil hominoids Taxon

RET

Range

n

Category*

Proconsul africanus3 Gorilla gorilla1 Pan troglodytes1 Hylobates lar1 Dryopithecus laietanus3,10 Oreopithecus bambolii3,11 Pan paniscus8 Proconsul major3,11 Lufengpithecus hudienensis5 Rangwapithecus gordoni5 Pongo pygmaeus1 Proconsul heseloni4 Sivapithecus sivalensis1,11 Griphopithecus sp.1,11 Afropithecus turkanensis6 Australopithecus africanus2,11 Homo sapiens1 Proconsul nyanzae4 Lufengpithecus lufengensis7 Graecopithecus freybergi3,11 Paranthropus robustus2,9

8.5 10.0 10.1 11.0 12.7 13.0 13.6 13.7 14.1 14.9 15.9 17.0 19.2 19.3 21.4 21.4 22.4 22.4 24.1 25.9 29.6

–

1 17 14 1 1 1 1 1 1 1 17 1 3 8 2 2 13 1 1 1 1

thin thin thin thin intermediate thin intermediate thin intermediate thin intermediate thin intermediate thin intermediate thick intermediate thick intermediate thick thick thick thick thick thick thick thick thick thick-hyper thick

6.8–13.4 7.0–13.3 – – – – – – – 11.3–20.5 – 16.3–20.9 16.5–23.0 19.9–22.9 21.3–21.6 13.8–32.3 – – – –

* Categories are defined by 95% confidence limits of species’ means reported by Martin (1985), and individual specimens may be found whose RET is not in the range that defines the species’ mean value. 1 Martin (1985). 2 Grine and Martin (1988). 3 Andrews and Martin (1991). 4 Beynon et al. (1998) mesial sections only. 5 Schwartz et al. (2003). 6 This study. 7 Reid and Schwartz (unpublished). 8 Olejniczak and Martin (in prep). 9 Grine (pers. comm.) attributes SKX 21841 to Paranthropus robustus rather than to Paranthropus crassidens as reported in Grine and Martin (1988). 10 Martin attributes this material to Dryopithecus laietanus rather than to D. fontani as reported in Andrews and Martin (1991). 11 Material has been reevaluated from additional images during the course of this study and original reported values have been updated. Due to methodological considerations that may affect accuracy, some data from Grine and Martin (1988) and Andrews and Martin (1991) on P. robustus, Paranthropus boisei, and Heliopithecus leakeyi have been omitted.

cuspal regions save for three exceptions. The DSR in the inner lateral enamel of KNM-WK 17024 is greater than in the inner cuspal enamel. In the middle lateral enamel of both teeth, the DSR is greater than in the middle cuspal enamel. In KNM-WK 24300, the middle cuspal enamel DSR is greater than that in the outer cuspal enamel DSR. The zones and regions that showed the greatest variation in DSR (outer lateral and outer cuspal) also showed the greatest frequency of intradian lines. A comparison between the two

teeth shows that rates are fairly similar in equivalent zones and regions. Regional differences greater than one standard deviation are observed only in the inner and outer cuspal enamel. Fine bands, which we interpret as intradian lines, are sometimes visible between square or slightly rectangular cross-striations (light and dark bands) in both teeth under PLM, SEM and TSRLM (Fig. 4). As noted above, they are most common in the outer cuspal enamel, although they are also observed in the outer cervical and lateral

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are not evident in either of the two A. turkanensis teeth examined. In addition, the SEM shows a few areas of aprismatic (prism-free) enamel, particularly in the outer cuspal enamel of KNM-WK 24300. Where present, subsurface aprismatic enamel ranges in maximum thickness from 21– 63 µm. Angular measurements of Retzius lines at the EDJ show that angles are low in cuspal enamel, highest in lateral enamel, and intermediate in cervical enamel (Table 5). An examination of the angular variation between the protoconid and metaconid of each tooth shows substantial differences in the cuspal and lateral regions of KNM-WK 24300, but not in KNM-WK 17024. It is not clear if differences between cusps are due to biological variability in this feature, or if they relate to differences in the timing of initiation and completion. When the two teeth are compared, the range of variation seen within KNM-WK 24300 encompasses the values of both cusps of KNM-WK 17024, with the exception of the cervical region. Crown formation time

Fig. 3. Polarized light micrograph of the outer cervical enamel of Afropithecus turkanensis (KNM-WK 24300). The surface of the tooth is at the right and the cervix is to the bottom. Enamel prisms are shown running from left to the right, with striae of Retzius (white arrows) and cross-striations crossing prisms. The relationship between Retzius lines and cross-striations, or periodicity, is shown (bracketed) as eight cross-striations and are clearly seen between pairs of Retzius lines. The scale bar in the lower right represents 50 µm.

enamel in association with Retzius lines. Additional evidence of sub-daily lines is apparent between daily lines in the coronal dentine of KNM-WK 17024. Observations of these regions under the SEM and TSRLM confirm that intradian lines are neither the result of light microscopy interference patterns from other layers, nor an artifact of preparation. ‘S-shaped striae’ as described and reported by Beynon et al. (1991b) and Dean and Shellis (1998) for P. nyanzae, Proconsul heseloni, Pongo pygmaeus, and Hylobates (Symphalangus) syndactylus

Table 6 shows the crown formation times of the mesial cusps of both teeth. The two-dimensional tracings of the cuspal enamel of KNM-WK 17024 yield a ratio of cohort path length to enamel thickness of 1.05 for both cusps. To compensate for prism undulation, a doubled ratio of 1.111 was used in calculations of the range of cuspal formation time (3-D column in Table 6), yielding a value of 354 days for the protoconid and 317 days for the metaconid based on average DSRs of 4.55 and 4.06 µm respectively. In KNM-WK 24300, the doubled ratio is 1.06 for the protoconid, and 1.11 for the metaconid, yielding 416 and 411 days respectively (4.38 and 4.29 µm DSRs). The methodology of FitzGerald et al. (1999) produced similar results of 387 and 383 days for the protoconid of each tooth. Risnes’ (1986) method produced

1

The value for two dimensional deviation was 1.055, which was doubled before rounding to yield a correction factor of 1.11.

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Table 3 Periodicity (number of cross-striations between Retzius lines) in extant and fossil primates Taxon

Periodicity

n

Source

Macaca nemestrina Macaca mulatta Hylobates lar Proconsul heseloni Theropithecus oswaldi Proconsul nyanzae Dryopithecus laietanus Pan paniscus Papio hamadryas Theropithecus gelada Lufengpithecus hudienensis Paranthropus boisei Afropithecus turkanensis Pan troglodytes Graecopithecus freybergi Gorilla gorilla Homo sapiens

4 4 4 5 6 6 6–7 6–7 7 7 7 7 7–8 6–9 8 7–10 6–12 7–11 7–11 8–12 8–9 9 8–11

1 3 1 2 unpublished 2 3 2 2 4 2 1 2 20 1 36 82 28 115 96 2 1 24

Smith and Sirianni (unpublished) Bowman (1991) Dirks (1998) Beynon et al. (1998) Macho et al. (1996) Beynon et al. (1998) Kelley et al. (2001) Reid (unpublished) Reid and Dirks (1997) Swindler and Beynon (1993) Schwartz et al. (2003) Dean (1987a) This study Schwartz et al. (2001a) Smith et al. (in prep) Schwartz et al. (2001a) Reid et al. (2002) Schwartz et al. (2001a) Reid and Dean (2000) FitzGerald (1996) Reid and Schwartz (unpublished) Dean et al. (1993a) Schwartz et al. (2001a)

Lufengpithecus lufengensis Paranthropus robustus Pongo pygmaeus

Values for n represent number of individuals sampled. Values for extant primates from Schour and Hoffman (1939), Okada (1943) and Fukuhara (1959) were not included because methods could not be verified. For extant hominoids, results from studies with larger samples were included over those based on few individuals.

results generally within a month of the other two estimates. The number of Retzius lines in the imbricational enamel that reach the surface is 71–75 and 52–59 in the protoconid and metaconid of KNM-WK 17024. This range is multiplied by a periodicity of seven, yielding a range of 497–525 and 364–413 days of imbricational enamel formation respectively. In KNM-WK 24300, 81–85 and 68–71 total striae are evident at the surface of the protoconid and metaconid. This is multiplied by an eight-day periodicity, resulting in a range of 648–680 and 544–568 days of imbricational enamel formation for each cusp. Summing the ranges of cuspal and imbricational enamel formation yields crown formation times of 2.33–2.50 years (851–912 days) and 1.87– 2.00 years (681–730 days) for the protoconid and metaconid of KNM-WK 17024, and 2.82–3.00 years (1031–1096 days) and 2.62–2.67 years (955–

979 days) for the protoconid and metaconid of KNM-WK 24300. Total crown formation time for A. turkanensis second molars is estimated to range from 2.43–3.10 years, which are the combined minimum and maximum protoconid formation times added to 0.1 years of final hypoconid formation. Table 7 shows that these values for A. turkanensis are similar to crown formation times reported for second molars of P. pygmaeus, Gorilla gorilla, and modern Homo. Values for A. turkanensis are greater than estimated crown formation times of second molars reported for Hylobates lar, P. heseloni, D. laietanus, and are less than that of P. troglodytes. Discussion Enamel thickness Histological analysis of dental material facilitates understanding of the final functional product

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Table 4 Average daily secretion rate (DSR) in Afropithecus turkanensis KNM-WK

Region

Inner Zone

Middle Zone

Outer Zone

17024

Cuspal Lateral Cervical

3.560.50 (40) 3.720.48 (38) 3.460.49 (25)

4.220.75 (32) 4.250.67 (35) –

5.541.12 (28) 4.990.91 (23) 4.040.59 (21)

24300

Cuspal Lateral Cervical

4.310.50 (49) 4.160.48 (17) 3.270.62 (19)

4.430.68 (42) 4.590.53 (18) –

4.290.63 (35) 5.261.35 (24) 3.500.62 (26)

Overall

Cuspal Lateral Cervical

3.970.62 (89) 3.850.52 (55) 3.380.55 (44)

4.340.71 (74) 4.360.64 (53) –

4.851.08 (63) 5.121.14 (47) 3.740.66 (47)

Data derived from polarized light microscopy. Three equal divisions made along the EDJ from dentine horn to cervix define regions. Zones represent enamel depth within a particular region. In the cervical enamel, zones were divided into inner and outer only. Values in µm represent the average of all prisms measured within each region, with number of prisms reported in parentheses. Standard deviation is reported asone deviation.

of the processes of development and growth, which may be understood in terms of enamel thickness (macrostructure) and enamel microstructure. Several issues regarding enamel thickness warrant discussion, including the degree of variation within and between species, as well as the polarity of this trait. Knowledge of the variation of this feature is particularly important when comparing values derived from small samples, such as the two A. turkanensis teeth. It has been shown that relative enamel thickness within extant great apes and humans varies by 100%, however 95% confidence intervals for species’ means define discrete taxonomic groupings with minimal overlap except when Pan and Gorilla are compared (Martin, 1983, 1985). Values of relative enamel thickness for the two teeth examined in this study differ by about 13%, which is within the variation seen in larger samples of Griphopithecus sp. and S. sivalensis. Previous studies have documented substantial intrageneric variation in small samples of Proconsul and Lufengpithecus (Beynon et al., 1998; Schwartz et al., 2003). Beynon et al. (1998) presented data that demonstrated that not all species of Proconsul have enamel as thin as Proconsul major and P. africanus (Andrews and Martin, 1991). Furthermore, recent work on Lufengpithecus also shows variation in enamel thickness between closely related species or sub-

species (Schwartz et al., 2003). These studies have serious implications for the determination of the polarity of this trait. Martin (1983, 1985) first suggested that thin enamel is the ancestral condition for early Miocene apes based on the possession of thin enamel in non-hominoid anthropoids and Hylobates, which was supported by the initial discovery of thin enamel in Proconsul (Andrews and Martin, 1991). However, evidence of thick enamel in A. turkanensis and P. nyanzae dating to 17–18.5 million years ago shows a greater early diversity than was previously assumed. It now appears that patterns of enamel thickness in hominoids throughout the last 20 million years are more complicated than previously suggested. In certain instances, this trait may have undergone a reversal to the ancestral condition, or evolved in parallel between taxa. Recent and ongoing work on the functional significance of enamel thickness may eventually facilitate an integration of traditional phylogenetic and functional perspectives of this trait (Andrews and Martin, 1991; Macho and Berner, 1993, 1994; Macho and Spears, 1999; Schwartz, 2000a,b; Olejniczak and Martin, 2002). Enamel microstructure The periodicity, numbers of cells secreting enamel, rate of secretion, and duration of secretion

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have been shown to vary within primates, leading to differences in enamel thickness, enamel distribution and crown formation time. As noted above, a meaningful examination of these traits requires information on a number of growth parameters determined from histological sections. Periodicity A recent study on a large combined sex sample of extant great ape and human canines demonstrated significant taxonomic differences in periodicity values for all taxa, except between Gorilla and Homo (Schwartz et al., 2001a). These authors suggested that a relationship might exist between periodicity and body size or a related correlate such as brain size or metabolic rate. When extant and fossil hominoids are considered exclusively, periodicity is found to be significantly correlated with estimated body mass (Smith et al., 2003). Afropithecus has an estimated body mass of approximately 34–35 kg (Leakey and Walker, 1997), which is similar to P. troglodytes, and periodicity ranges from seven to eight in the former and six to nine in the latter (Table 3). Although this relationship appears to hold true within catarrhines and/or hominoids, the inclusion of other primates complicates this hypothesis. Schwartz et al. (2002) recently described the microstructure of Palaeopropithecus ingens, a chimpanzee-sized subfossil Malagasy lemur that has a periodicity of two. In this instance, periodicity does not appear to correlate with body size, and may be influenced by phylogeny as well as life history (Schwartz, pers. comm.). Daily secretion rate DSR in A. turkanensis generally increased from inner to outer enamel within each region, and from cervical to cuspal regions, which is in keeping with the results of most studies of other hominoids (Beynon et al., 1991a; Beynon et al., 1998; Dean, 1998; Reid et al., 1998a; Kelley et al., 2001; Schwartz et al., 2001a). Exceptions to this pattern of consistent increase have been found in some primates (Beynon et al., 1998; Dean, 1998; Dirks, 1998; Schwartz et al., 2001a), as well as in this study. The most marked deviation in the two teeth examined here was seen in the middle and outer

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cuspal and lateral enamel, and may have been influenced by additional short-period features (discussed below). Dean (1998) noted that defining these rates in discrete inner, middle, and outer zones may mask variation and lead to a simplified categorization of this complex feature. He presented data in a graphical format with a monthly series of box plots of DSR from the beginning to the end of cuspal enamel formation. Inspection of this type of data illustrates that rates may level off or decrease slightly in the outer enamel, especially in Pongo and Hylobates (e.g., Beynon et al., 1998). This is similar to the decrease in rate seen in KNM-WK 24300. This trend may have been even more evident had DSR been measured and reported in consecutive monthly zones, but was not possible due to the variable visibility of cross-striations throughout the cuspal enamel. The mean values of DSR in the cuspal enamel of A. turkanensis are similar to values reported for P. nyanzae, excluding the final month of formation (Beynon et al., 1998). Cuspal DSRs for A. turkanensis are also similar to those of G. freybergi, L. hudienensis, P. pygmaeus, and D. laietanus, although A. turkanensis does not appear to begin enamel secretion as slowly as the three latter taxa (Beynon et al., 1998; Kelley et al., 2001; Smith et al., 2001; Schwartz et al., 2003). In some Miocene hominoid molars, cuspal enamel secretion begins at approximately 3.5–4 µm per day, while extant apes and humans begin at 2.5–3 µm per day (Beynon et al., 1998; Dean, 1998). It may be the case that Miocene hominoids share a common pattern of higher initial and overall average cuspal rates relative to extant apes, although additional work is necessary to address the issue of variation within and between individuals before definitive conclusions are reached. Ameloblast extension It is commonly held that the angle of intersection between Retzius lines and the EDJ may be regarded as a proxy for the extension rate of ameloblast activation in a cervical direction (Boyde, 1964; Shellis, 1984). Provided that DSR remains constant, lower angles represent more rapid extension as a larger number of cells are

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Fig. 4. (a–c). Intradian lines as seen under multiple forms of microscopy in Afropithecus turkanensis (KNM-WK 24300). In these figures, large arrows indicate cross-striations, and potential intradian lines are indicated by thin white lines. (a) Polarized light micrograph of the occlusal enamel showing enamel prisms running from the lower right (direction of EDJ) to the upper left (direction of tooth surface). Cross-striations are light and dark bands crossing enamel prisms in a perpendicular manner. Intradian lines are fine light and dark subdivisions of the cross-striations. The scale bar in the lower right represents 50 µm. (b) Split-image scanning electron micrograph of the outer and middle cervical enamel of a naturally fractured, unetched surface. The image on the left is an overview of the region, with the box outlined in white indicating an area of enlargement shown on the right. The scale bar in the lower left represents 50 µm. On the right, cross-striations and intradian lines are visible in the enamel prisms, which run from the bottom (EDJ) to the top of the image (tooth surface). The scale bar in the bottom right represents 10 µm. (c) Tandem scanning reflected light micrograph of the outer cuspal enamel. Enamel prisms run from the bottom (EDJ) to the top of the image (tooth surface) showing variable cross-striations and intradian lines. The scale bar in the lower right represents 25 µm. Faint, slightly curved lines run from the upper right corner to the bottom of the image are artifacts of microscopy (scanning lines) due to the holes in the Nipkow disc of the TSRLM.

activated to secrete enamel in a given time. In A. turkanensis, these angles seem to indicate that extension begins at a high rate, slows from cuspal to lateral enamel, and then increases from lateral to cervical enamel. When compared to values from other hominoids, the cuspal enamel of A. turkanensis does not have angles as low as extant apes and humans, nor do they increase as dramatically from cuspal to cervical enamel as in the other species (Beynon and Reid, 1995; Beynon et al., 1998). This may also be explained by the higher DSR in the inner enamel regions, and the more uniform pattern of secretion rate from cuspal to cervical inner enamel in A. turkanensis when com-

pared to other extant hominoids (Beynon et al., 1991a, 1998; Dean, 1998; Dirks, 1998; Reid et al., 1998a). Two species of Proconsul display variable angular patterns, which differ from that of A. turkanensis. Proconsul nyanzae shows a pronounced cervical slowing with high angles, while P. heseloni shows a gradual slowing similar to that of extant hominoids with moderate angles (Beynon et al., 1998). Schwartz et al. (2003) reported that L. hudienensis is similar to P. heseloni and extant apes, with a moderate cervical slowing. Afropithecus shares the condition of low cervical angles with some fossil hominids (Dean, 2000). At this point, it is not clear how the relative contributions

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Fig. 4. (b and c).

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Table 5 Angle of intersection of the striae of Retzius with the enamel dentine junction (EDJ) KNM-WK

Cusp

Cuspal

Lateral

Cervical

17024

Metaconid Protoconid

20.35.8 (12) 18.87.9 (5)

38.62.8 (5) 39.18.0 (13)

– 35.05.9 (7)

24300

Metaconid Protoconid

24.53.7 (4) 15.03.6 (3)

33.75.8 (9) 42.94.0 (10)

29.72.7 (9) 31.86.2 (9)

20.06.1 (24)

38.76.7 (37)

31.95.4 (25)

Overall

Angles are presented as degreesone standard deviation. The number of Retzius lines measured is in parentheses. Due to the fractured cervix of the metaconid of KNM-WK 17024, it was not possible to measure angles in this region. Overall values represent the average of weighted means of both cusps of each tooth.

Table 6 Crown formation time in Afropithecus turkanensis Cusp

KNM-WK 17024 Protoconid Metaconid KNM-WK 24300 Protoconid Metaconid

Cuspal

Imbricational

Thick

3-D

DSR

Path

5%

1.15

Ret

Per

Imb

Total

1450 1160

1.11 1.11

4.55 4.06

354 317

387 –

366 329

71–75 52–59‡

7 7

497–525 364–413

851–912 681–730

1720w 1590

1.06 1.11

4.38 4.29

416 411

383 –

452 426

81–85 68–71

8 8

648–680 544–568

1031–1096 955–979

Cusp=Protoconid or metaconid. Thick=Maximum cuspal enamel thickness in µm. 3-D=Cusp specific correction factor determined from path length montages. DSR=Average daily secretion rate in µm determined from measurements in cuspal enamel. Path=Number of days of cuspal enamel formation determined from the enamel thickness multiplied by the 3-D corrected path length and divided by the DSR. 5%=Number of days of cuspal enamel formation determined in 5% intervals from the dentine horn to the tooth surface. The interval length was divided by the local DSR and the days were summed. Determined for the protoconid in each tooth only. 1.15=Number of days of cuspal enamel formation determined from the thickness multiplied by a standard correction factor (1.15) and divided by the DSR. Provided for comparison only and not used in calculation of total. Ret=Number of imbricational Retzius lines. Per=Periodicity (number of cross-striations between Retzius lines). Imb=Number of days of formation of imbricational enamel, determined by the number of imbricational Retzius lines multiplied by the periodicity. Total=Total number of days of enamel formation. Range determined by combining the minimum and maximum of the Path and 5% cuspal estimates with the minimum and maximum Imb values. ‡ Metaconid cervical enamel missing for KNM-WK 17024, some Retzius lines estimated from dentine. wProtoconid enamel thickness for KNM-WK 24300 was slightly reconstructed, as a small amount was lost to attrition.

of changes in extension rate or local DSR impact differences in angles between A. turkanensis and other primates, or if these differences are due to a combination of both factors. Crown formation time and patterns of development Histological estimates of molar crown formation time in most fossil and some extant hominoids range from two to three years. H. lar and P.

heseloni display more rapid dental developmental schedules, while P. troglodytes appears to have the longest period of crown formation. Although crown formation time in the two A. turkanensis teeth differs by approximately 0.6 years, this variation is not as great as that seen in a recent study of four medieval human dentitions (Reid et al., 1998b). Few published data exist on crown formation time in large samples of extant ape molars, but differences of 0.5–0.7 years within

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299

Table 7 Histological crown formation times of hominoid molars (in years) Taxon/Tooth 1

Hylobates lar

Proconsul heseloni2

Dryopithecus laietanus3 Proconsul nyanzae2 Lufengpithecus hudienensis4 Paranthropus robustus5 Paranthropus boisei6 Early Homo6 Afropithecus turkanensis7 Pongo pygmaeus8 Gorilla gorilla8 Homo sapiens9

Lufengpithecus lufengensis11 Pan troglodytes10

Cuspal

Imbricational

n

Total

0.67 0.68 0.45 0.50 0.78 0.73 0.64–0.67 0.90 0.90–0.96 0.73–0.80 1.20 1.4–1.55 1.01 0.97–1.14 0.40 unpublished 0.5 0.5–0.6 0.79–1.14 1.10–1.25 1.10–1.30 1.00–1.32 0.53–0.65 0.60–0.92 0.70–0.90

0.65 0.48 0.70–0.90 0.9–1.05 0.84–1.12 1.23 1.57–1.58 0.92–1.13 1.04–1.58 1.38 1.23 0.72–1.04 1.41–1.60 1.36–1.86 2.33 unpublished 2.21–2.39 2.02–2.70 1.67–2.72 1.58–2.52 1.78–2.27 2.89 2.20 1.80–2.96 2.78–3.14

1-M1 1-M2 1-M1 1-M2 1-M3 1-M1 2-M2 1-M1 1-M2 1-M1 1-M1 2-(M1/M3) 2-M1 2-M2 2-M1 2-M2 2-M1 2-M2 8-M1 7-M2 5-M3 2-M2 5-M1 3-M2 3-M3

1.32 1.16 1.0–1.2 1.3–1.6 1.7 1.96 2.22–2.25 1.8–2.0 2.1–2.5 2.11–2.18 2.43 2.12–2.59 2.42–2.62 2.43–3.10 2.7–3.0 2.8–3.3 2.7–3.1 2.6–3.3 2.61–3.59 2.83–3.62 3.08–3.37 2.83–3.89 2.73–2.85 3.56–3.69 3.48–4.04

1 Dirks (1998). 2Beynon et al. (1998). 3Kelley et al. (2001). 4Schwartz et al. (2003). 5Dean et al. (1993a). 6Beynon and Wood (1987). These authors did not specify the tooth from which specific values were measured. 7This study. Total crown formation time includes a correction of 0.1 years added to the protoconid formation time of each tooth to compensate for final hypoconid formation. 8Beynon et al. (1991b). 9Reid et al. (1998b). 10Reid et al. (1998a). 11Reid and Schwartz (unpublished data). The total value of one of these two teeth was determined using information from the dentine.

small samples of the same tooth type are not uncommon. Differences in crown formation times between the mesial cusps of A. turkanensis support the results of previous studies, as the protoconid is the first mesial mandibular cusp to calcify (Butler, 1956; Oka and Kraus, 1969; Reid et al., 1998a,b; Kelley et al., 2001). Subsequent formation proceeds over a longer amount of time compared to the metaconid, making the protoconid (or the protocone in the maxillary dentition) the more appropriate mesial cusp for estimations of total crown formation time. In a thorough study of several human dentitions, Reid et al. (1998b) demonstrated that the metaconid represented only approximately 80% of the total crown formation time, while the protoconid represented more than

95% of this period in second molars. This difference may relate to differences in cuspal enamel thickness, as the protoconid is the thicker mesial mandibular cusp (Khera et al., 1990; Schwartz, 2000b). Recent histological studies of chimpanzee and human molars have suggested that crown formation time increases in the same cusps from first to third molars (Reid et al., 1998a,b), which may be related to a trend of increased enamel thickness, particularly in humans. Although a direct relationship between formation time and enamel thickness may exist between cusps within a tooth or along the molar row within a taxon, a comparison of extant and fossil hominoids with varying degrees of enamel thickness showed no statistical relationship between total crown formation and relative

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Fig. 5. Polarized light image of several classes of incremental features in Afropithecus turkanensis (KNM-WK 24300). Enamel prisms run horizontally to the tooth surface at the right, four striae of Retzius (large arrows) run from the lower left to the upper right and meet the enamel surface, four to five laminations (small arrows) run parallel between each stria, and numerous faint bands can be seen crossing the enamel prisms perpendicularly. The periodicity, or number of cross-striations between Retzius lines, was determined in other regions to be eight. This micrograph illustrates the difficulty of determining the periodicity in regions where laminations and intradian lines are evident. In addition, this image suggests that laminations are not equivalent to daily lines.

enamel thickness (Smith et al., 2003). Second molar crown formation times of thinner-enamelled gibbons, gorillas, and chimpanzees range from the shortest to the longest reported values. Hominoids with relatively thick enamel, such as A. turkanensis, Paranthropus and P. nyanzae, show intermediate molar formation times. It appears that cuspal crown formation time may show a more direct relationship with relative enamel thickness than total crown formation time. Compared to extant apes, the development of

thick enamel in A. turkanensis results from a relatively greater ratio of cuspal enamel to imbricational enamel formation time (Table 7). Extant great ape cuspal enamel formation represents only approximately 15–20% of total crown formation time, compared to approximately 40% in A. turkanensis. The A. turkanensis ratio is similar to the pattern seen in Paranthropus robustus and P. nyanzae, while an even higher ratio is seen in G. freybergi and Paranthropus boisei, which have extremely thick enamel (Beynon and Wood, 1987; Grine and Martin, 1988; Beynon et al., 1998; Smith et al., 2001). Grine and Martin (1988) considered three variables that relate to enamel thickness: ameloblast secretion rate, the total period of secretion, and the number of cells that are active at any given time. They hypothesized that similar degrees of enamel thickness could result from multiple developmental pathways. Dean (2000) substantiated their hypothesis with a comparison of cuspal enamel formation in second molars of P. nyanzae and a modern human. He showed that equally thick cuspal enamel resulted from a higher secretion rate in the former and a longer period of secretion in the latter. Like P. nyanzae, A. turkanensis formed thick cuspal enamel at a high overall secretion rate and completed cuspal enamel formation several months earlier than do modern humans. Methodological considerations During the course of this study, it became clear that a number of factors may potentially influence histological assessments of enamel microstructure, which have received little attention in previous reports. It is not our intent to provide a systematic methodological revision here, rather we illustrate some challenges that future work must not only take into consideration, but should attempt to improve upon. Periodicity Several factors may complicate the accurate determination of periodicity. It is well known that, in an ideal section, counts should be made on entire series of well-defined cross-striations between adjacent Retzius lines that clearly meet

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the surface and form perikymata. In the teeth examined in this study, however, cross-striations often appear immediately adjacent to a Retzius line, but become less defined within the interval between two Retzius lines as prisms course towards the tooth surface. Risnes (1998) has speculated that ameloblasts may lose and reform their secretory Tomes’ processes between the production of successive Retzius lines, which may result in poorly defined or absent cross-striations. Both SEM and PLM observations made on subsurface enamel during this study support this hypothesis, demonstrating well-defined crossstriations frequently near Retzius lines with a ‘stair-step’ appearance, but we feel that this warrants further study. In addition, calculated values of periodicity are not always consistent with direct counts of crossstriations, as the DSR does not always remain constant between pairs of Retzius lines. This may be due to local variation in secretion rate, often causing the convergence of striae at the tooth surface. Even in regions with clear Retzius lines and cross-striations, additional features such as intradian lines and laminations may complicate determination of the periodicity (Fig. 5). Daily secretion rate In order to collect data that are methodologically consistent with other published results on hominoids (e.g., Beynon et al., 1991a, 1998; Dean, 1998; Schwartz et al., 2001a), crossstriations were recorded wherever possible in all regions of the enamel. However, Dirks (1998) and Reid et al. (1998a,b) have suggested that measurements should not be made in the first 100 µm of enamel at the EDJ or the last 100 µm at the surface, because aprismatic enamel in these regions and the convergence of striae at the tooth surface may obscure or complicate measurements of daily lines. This disparity may be seen when comparing data from Reid et al. (1998a) and Dean (1998), as reported cuspal DSR in chimpanzees in the former do not show as wide a range as values reported by the latter. Dean’s inclusion of the first and last month of cuspal enamel formation (corresponding approximately to the first and last 100 µm) often increases the

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minimum and maximum range of DSR values (Dean, 1998; Beynon et al., 1998). In addition, categorizing and averaging data in three discrete enamel depths (inner, middle, and outer) tends to minimize the range of values. It is critical that this is considered when comparing results between studies. We would also like to suggest that, in the final month of cuspal enamel formation, the DSR in fossil material may be difficult to assess due to a high proportion of additional short-period features of uncertain periodicity, which may be difficult at times to distinguish from cross-striations (e.g., Fig. 4c). Additional short-period features Gustafson and Gustafson (1967) appear to have been the first to observe and report on intradian lines, which they referred to as a “double band effect” (in relation to typical cross-striations). They dismissed the possibility that these lines were optical artifacts, a conclusion that has recently been advocated (Boyde, 1989; Shellis, 1998; Antoine et al., 1999). Others researchers have not specifically addressed them or may have regarded them as equivalent to daily lines (e.g., Whittaker, 1982; Martin, 1983). Whittaker’s and Martin’s micrographs likely represented the first published SEM evidence of these features (Whittaker: Figure 7, p.392; Martin: Figure 5.4e, p.332, Figure 5.7a, p.341), although they were not identified as such. This may have led Martin to conclude erroneously that certain regions of ape and human enamel have extremely slow DSRs, which has not been substantiated by other studies. In this study, SEM and TSRLM documentation of intradian lines that are distinct from crossstriations provides additional direct evidence that these lines are not the result of interference from underlying layers, as both of these forms of microscopy present information from a single plane of section only. Another class of incremental feature, known as laminations, was described by Ripa et al. (1966) and Whittaker (1982) in association with aprismatic enamel. These features, recognized here as closely spaced incremental lines that run parallel to regular Retzius lines, were observed in the two teeth in this study using various forms of

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microscopy, particularly in the lateral and cuspal enamel near the EDJ and the tooth surface (Fig. 5). It is not yet known how these features develop, though it appears they are sometimes associated with the production of aprismatic or Pattern 1 enamel as they are variably visible near the EDJ and tooth surface. We find the presence of additional short-period features to be one of the most challenging complications of this type of study, particularly as the positive identification of known period increments is a fundamental requirement for analyses of incremental development. Experimental work on rat dentine by Rosenberg and Simmons (1980) and Ohtsuka and Shinoda (1995) demonstrated the presence of 2–3 intradian increments per day. FitzGerald (1996) reported a similar observation in human enamel, but his conclusions are difficult to verify without experimental evidence. In regard to laminations, Risnes (1998) reported that this feature shows ‘a relationship’ to cross-striations; however, we present evidence from KNM-WK 24300 that this feature does not have a daily periodicity (Fig. 5). If laminations are a circadian feature, one would expect seven lines (eight with one Retzius line included) between and parallel to each Retzius line, as there is an eight day periodicity in this individual. It is clear that only four to five laminations are present between the two Retzius lines, which imply a repeat interval that is greater than that of circadian cross-striations. Work in progress on fluorescent-labelled macaque teeth may provide more rigorous empirical data on the specific periodicity of both intradian lines and laminations (Smith et al., 2002).

interpreting or comparing results, as it is difficult to determine this curvilinear relationship with precision and accuracy (Shellis, 1984; Grine and Martin, 1988). Crown formation time The most direct method of determining the cuspal enamel formation time involves counting cross-striations from the beginning of enamel formation at the dentine horn to the end of formation at the tooth surface (Gysi, 1931; Boyde, 1963). However, histological material of a quality that permits this is quite rare. An alternative to the methods described here and above was proposed by Dean (2000), who suggested that cuspal enamel formation time may be predicted by taxon specific regression equations that require knowledge of the enamel thickness only. The derivation of these equations, however, requires information about DSR in sufficiently large samples, which limits the application of this approach to taxa in which teeth have previously been sectioned. In addition, Reid et al. (1998a) suggested that section obliquity may have a significant influence on the accuracy of certain methods, and advocated methods other than those that involve utilizing the linear cuspal enamel thickness. Although Dean’s regression equations may provide the simplest method of estimating this growth parameter in non-oblique sections where the DSR is well sampled, additional work on fossil and living apes is necessary before these regressions can by extended to other Miocene hominoids such as A. turkanensis.

Summary and Conclusions Ameloblast extension It appears that published reports of this angle may not always be comparable due to methodological differences. In certain studies, it is not clear if reported values represent the angle of the overall trend of the Retzius line or the portion immediately adjacent to the EDJ. Striae may begin at a relatively low angle, which quickly becomes more dramatic as the prisms or forming front courses cervically (see images of Proconsul teeth in Beynon et al., 1998). Additionally, the possibility of measurement error must be considered when

Molar enamel thickness in Afropithecus turkanensis is not as thick as was previously suggested (Martin, 1995). Relative enamel thickness in the two second molars examined here is 21.4, which is similar to values for Griphopithecus sp., Sivapithecus sivalensis, Australopithecus africanus, modern Homo, and Proconsul nyanzae, and is unlike extant apes. Features of the microstructure, such as the periodicity and daily secretion rate, do not conclusively distinguish A. turkanensis from Proconsul nyanzae, Lufengpithecus, Dryopithecus

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laietanus, or extant apes and humans, although some variation exists in the patterning of these features among hominoids. The periodicity is found to overlap with some cercopithecoids, extant great apes and humans, D. laietanus, Graecopithecus freybergi, Lufengpithecus, and Paranthropus boisei. The cuspal enamel daily secretion rates are most similar to those of G. freybergi, L. hudienensis, Pongo pygmaeus, P. nyanzae and D. laietanus. Angles of Retzius lines at the EDJ are most similar to those of fossil hominids and differ from living and fossil apes. Evidence was also found of additional incremental features known as intradian lines and laminations, which may affect determination of the periodicity and daily secretion rate if not properly identified. The developmental basis and periodicity of these two features are not well understood, and warrant further study. Crown formation times of the two A. turkanensis M2s are 2.4–2.6 and 2.9–3.1 years. These values are most similar to those of second molars of P. pygmaeus, Gorilla gorilla and modern Homo, and overlap slightly with P. nyanzae and L. lufengensis. Afropithecus shows a relatively longer period of cuspal enamel formation than thinnerenamelled African apes, although the latter have a longer period of total crown formation. Teeth with relatively thick enamel may result from a longer period of cuspal enamel formation, higher cuspal daily secretion rate, and/or a greater number of active cells than in thin-enamelled extant hominoids. In Miocene hominoids, thick enamel appears to result from higher daily cuspal enamel secretion rates and/or longer cuspal formation times relative to extant apes and humans. Additional studies are needed to document the variation in these parameters in larger samples of extant species, which will lead to more informed interpretation of limited fossil material. Afropithecus turkanensis may be categorized as a primitive hominoid with relatively thick enamel, which formed in a manner similar to other Miocene hominoids. The possession of thick enamel may have permitted the exploitation of additional food resources unavailable to earlier catarrhines, which are presumed to have relied on soft-fruits that required little processing (Andrews and Martin, 1991). Aspects of the developmental

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biology of A. turkanensis, such as crown formation time and age at M1 emergence (Kelley and Smith, 2003), indicate that by 17 million years ago, hominoids had begun to show a more prolonged period of dental development relative to species of Proconsul, Hylobates or extant cercopithecines. Evidence for even greater periods of dental development characteristic of great apes and humans is not apparent until the late Miocene.

Acknowledgements We are grateful to the Government of Kenya and the National Museums of Kenya for permission to study these valuable teeth. We would especially like to thank Don Reid for his invaluable advice and assistance with this work. Chris Dean, Gary Schwartz, Wendy Dirks, and Jay Kelley provided generous technical advice and/or helpful discussions. We would also like to thank Jay Kelley, Anthony Olejniczak, Don Reid, Chris Dean, Fred Grine, Gabriele Macho, Summer Arrigo-Nelson, Allison Cleveland and two anonymous reviewers for helpful comments on this manuscript. Milan Hadravsky provided essential technical support with the TSRLM. Randy Susman provided access to the Pan paniscus tooth. This study was supported by the National Science Foundation, SBR 8918695.

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