williams and patterson 2010

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PALAIOS, 2010, v. 25, p. 439448

Research Article

DOI: 10.2110/palo.2009.p09-116r

RECONSTRUCTING THE PALEOECOLOGY OF TAUNG, SOUTH AFRICA FROM LOWMAGNIFICATION OF DENTAL MICROWEAR FEATURES IN FOSSIL PRIMATES

FRANK L9ENGLE WILLIAMS* and JAMES W. PATTERSON

Department of Anthropology, Georgia State University, Atlanta, Georgia 30303, USAe-mail: [email protected]

ABSTRACT

Taung, South Africa yielded the first Pliocene Hominini fossil,

Australopithecus africanus, recovered from a lime quarry in 1924. To

identify whether the habitat of the site differed from present-day

conditions, dietary preferences of fossil papionins from Taung, including

Parapapio antiquus (n 5 8), Papio izodi (n 5 12), and indeterminatespecimens (n 5 10) were examined under low magnification to discernpatterns of dental microwear. The comparative fossil sample from

Sterkfontein Member 4 includes Parapapio broomi (n 5 10) andParapapio jonesi (n 5 5). Extant Papio ursinus (n 5 20), a savanna-dwelling baboon from South Africa, provides a modern analogue. Six

dental use-wear scars on the paracone of the second molar (M2) were

recorded and the data analyzed using ANOVA with Tukeys test to detect

whether group differences were present for each feature; linear regression

identified significant covariation of microwear features. Principal

components analysis and discriminant function analysis were utilized to

identify species-specific dietary signals. Extant Papio ursinus is separated

from the extinct taxa solely by a relatively greater number of fine

scratches with respect to the other microwear features. Papio izodi

overlaps primarily with extant Papio and secondarily with Parapapio,

which forms a more discrete grouping that includes Parapapio antiquus

from Taung. A wetter, more closed environment is suggested for Taung

and Sterkfontein Member 4 compared to the habitat of present-day

central South Africa.

INTRODUCTION

The limestone cave deposits of the Transvaal and adjoining regions

of South Africa preserve a wide variety of fauna dating to the Plio

Pleistocene (, 2.51.5 Ma). Foremost among these are the australo-

piths, which provide evidence of early hominin evolution. Unique

among these specimens, the famous Taung child is the first

Australopithecus africanus specimen discovered and the only hominin

specimen found at Taung. Like other South African sites, Taung is

difficult to date chronometrically. Nevertheless it has been assigned a

late Pliocene age on the basis of first and last appearance dates of

extinct taxa correlated with East African controls. Fossil papionin

monkeys, well represented across East and South African sites, havefactored heavily in these analyses, yielding a date for Taung of,2.3 Ma

(Delson, 1984). As they evolved concurrently and exploited similar

environments, papionins have proven to be useful hominin analogues

(Elton, 2007; Hughes et al., 2008). Taung fossil papionins Parapapio

antiquus (herein Pp.) and Papio izodi(herein P.) provide insight into the

ecological conditions experienced by the four-year-old Taung child.

Identifying the diets of these papionin specimens, through the

examination of dental microwear using low-magnification stereomi-

croscopy, presents a novel approach to reconstructing the paleoecology

of Taung.

Previous Habitat Reconstructions for South Africa

The discovery of the Taung child led Dart (1926) to develop the

savanna hypothesis, i.e., that inhabiting an open, savanna environment

was the primary factor in the origin and evolution of hominins,

assuming that the environment of the Taung child was similar to the

modern dry and open scrub brush typical of central South Africa. There

is abundant research, however, that indicates substantial variability in

regional and global climate during this period. While the savanna

hypothesis does not reflect the variability observed in the paleoclimate,the general trend toward drier environments during the Plio

Pleistocene in southern Africa has undoubtedly influenced hominin

evolution, and this appears to be the case with a variety of taxa

(deMenocal, 1995). Yet southern Africa presents some difficulties in

paleoecology due to the irregular and complex depositional history of

the cave sites. Furthermore, at least four global climatic processes had

some bearing on regional climatic variation in Africa, including (1)

orbital forcing; (2) the emergence of C4-dominated biomes, a gradual

process beginning ,8 Ma with substantial regional variation; (3)

intensification of Northern Hemisphere glaciation (INGH), occurring

,2.5 Ma; and (4) the development of Walker Circulation, easterly trade

winds across the Pacific Ocean that maintain sea-surface temperatures

(Maslin and Christensen, 2007). The interaction of these processes

appears to account for much of the observed fluctuations in the climate

of PlioPleistocene southern Africa.These global climatic processes directly contributed to the regional

fluctuations and the general drying trend observed in southern Africa

(Fig. 1). Analyses of stable carbon isotopes have provided evidence that

variation in biome composition is related to changes in global climate

affecting patterns of temperature and rainfall in southern Africa. This

transition has been highly variable across the region with contractions

and expansions of C4 and C3 biomes. A general trend toward drier

conditions, characterized by the expansion of C4 vegetation, is observed

in the region. Isotopic studies of two speleothems at Makapansgat

provide evidence of the initial shift from C3 to C4 vegetation (Hopley et

al., 2007). A late Mioceneearly Pliocene speleothem (Collapsed Cave)

indicates large quantities of C3 vegetation, while a 1.7 Ma speleothem

indicates a marked increase in C4 vegetation with variability of the

proportions of C3/C4 vegetation throughout its formation. Moreisotopic evidence from Makapansgat, derived from the tooth enamel

ofA. africanus, indicates that 25%50% of its diet consisted of C4 food

sources, either directly through the consumption of C4 plants or

indirectly through the exploitation of animals with a diet of C4 plants

(Sponheimer and Lee-Thorp, 1999). This also appears to be the case forA. africanus from Sterkfontein Member 4 as well, with ranges of 30%

60% reported (van der Merwe et al., 2003). Dietary reconstructions

based on dental morphology suggest Australopithecus subsisted on hard

foods requiring little incisal preparation, possibly fruits with hard husks

or seed pods (Kay, 1985). It appears that early hominins, both

australopiths and early Homo, exploited C4 resources whether theirenvironments were closed or open (Sponheimer and Lee-Thorp, 2003;

Lee-Thorp et al., 2007).* Corresponding author.

Copyright G 2010, SEPM (Society for Sedimentary Geology) 0883-1351/10/0025-0439/$3.00


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Segalen et al. (2007) provide isotopic evidence, from pedogenic and

biomineral carbonate d13C, suggesting that C4 vegetation was present in

southern Africa during the early Pliocene, only coming to dominate

ecosystems during the early Pleistocene, with extensive regional

variability (deMenocal, 2004). These climatic changes appear to be

largely related to patterns of rainfall. Exemplifying this relationship,

oceanic core samples from the western coast of South Africa (ODP leg

175 Site 1085), exhibit four peaks in the biogenic and terrigenous

components of the sediment, reflecting increased preservation and

higher productivity at 3.2, 3.0, 2.4, and 2.25 Ma (Christensen et al.,

2002). Eolian and fluvial processes are implicated in the sedimentation

while fluctuation of sediment composition is correlated with monsoonal

activity, indicating a wetter climate around the peaks. Periods of

increased wetness are also indicated by an examination of youngerdeposits at Gladysvale when compared to sedimentation at older sites

(Pickering et al., 2007). Effective precipitation seems to be the primary

factor affecting the type of sedimentation at these sites. Flowstone

deposition is correlated with greater effective precipitation and clastic

deposition with shorter arid periods. Isotopic evidence implies an

increase in C3 vegetation outside of the caves during the periods of

flowstone deposition suggesting that the South African deposits were

episodic in nature, representing relatively short geological periods of

time.

Pollen recovered from hyena coprolites found at Equus Cave, Taung,

provides further evidence for climate reconstruction (Scott, 1987). A

shift from cool and moderately humid habitats supporting open

grasslands with small shrubs and occasional trees occurred during the

late Pleistocene, followed by a warmer and drier environment

supporting shrubby karoid (Karoo-type) vegetation with open Acacia

savanna. A thornveld biome (open-mixed bush and tree savanna) is

evidenced in the palynological record from the terminal Pleistocene to

the present. Scott (1987) suggests denser woodland was present earlier

in the Pleistocene; however, this portion of the deposit could not be

accurately dated. Another indirect reconstruction of Taung during the

PlioPleistocene suggests that a large raptor played a major role in the

accumulation of fossil fauna at the site based upon taphonomic signals

of raptor predation and the type of bones preserved at Taung (Berger

and Clarke, 1995). A more recent study of the taphonomic aspects of

crowned eagle predation reinforces this argument (Sanders et al., 2003).

The involvement of a raptor in the accumulation at Taung implies a

woodland or forest environment at the site. Taung and SterkfonteinMember 4 appear to have accumulated under somewhat similar

climates. Faunal assemblages from Sterkfontein suggest open woodland

with bushveld (mixed grassland and woodland typical of the Transvaal)

and thicket areas (Reed, 1997), medium density woodland (Vrba, 1975),

open woodland to forest (McKee, 1991), moderately open savanna

(Vrba, 1985), open savanna (Benefit and McCrossin, 1990), and a

succession of riverine grasslands to open savanna (Avery, 2001).

Dating of Taung and Sterkfontein Member 4

Taung was once thought to be the oldest australopith site and at

other times the youngest (McKee, 1993). The Hrdlicka deposits are

considered to be the youngest at Taung and McKee (1993) suggests that

FIGURE 1Summary diagram of the chronological orientation of Taung and Sterkfontein Member 4 using Delsons African cercopithecid zones (Delson, 1984). Climatic

data is also shown, from left to right: (a) Pliocene to recent geomagnetic polarity; (b) African climate variability, representing the influence of precessional insolation forcing of

monsoonal climate and glacial cycles (beginning after 2.8 Ma and intensifying after 1 Ma) on the increasing aridity of African climates (differences along the horizontal serve to

visually distinguish major time intervals); (c) East African soil carbonate; (d) d13C illustrating the shift from woodland to grassland in this area [the solid boxes represent data

from Cerling and Hay (1988); the solid triangles are from Cerling (1992); and the open circles are from Wynn (2000)], d18O showing glacial cover; (e) African cercopithecid zones

(where U indicates the upper and L indicates the lower levels of each zone), and likely geochronological position of (f) Taung and (g) Sterkfontein. Columns a, e, f, and g from

Ciochon (1993; used with permission from the University of California Press); columns b, c, and d from deMenocal (2004; reprinted with permission from Elsevier).

440 WILLIAMS AND PATTERSON PALAIOS


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all of the cercopithecid specimens except for Parapapio broomi (or Pp.

antiquus) are associated with these deposits. Parapapio specimens are

associated with the Dart (1926) deposits, which are seen as the likely

origin of the australopith specimen and as being no younger, and likely

older than the Hrdlicka deposits. In faunal comparisons between Taung

and the other sites, Makapansgat Member 34 and Sterkfontein

Member 4 emerge as the most similar. McKee (1993) suggests that

considerable time depth characterizes many of the deposits, butestablishes a range of dates for each species represented at Taung,

reaching a terminus of 2.62.4 Ma, roughly contemporaneous with

Sterkfontein Member 4 (see also McKee, 1996; Berger et al., 2002).

Tobias et al. (1993) argue that parts of the Dart and Hrdlicka deposits

are associated and accept Delsons (1984) estimate of 2.3 Ma for Taung.

The climatic and chronometric information relating to Taung and

Sterkfontein Member 4 are summarized in Figure 1. Simulations of

climatic conditions and vegetation cover for the mid-Pliocene glacial

conditions and interglacial conditions illustrate the effects of the INHG

on the paleoclimate of South Africa (Fig. 2). These simulations were

produced with HadCM3 and BIOME 4 (Hughes et al., 2008), and when

compared to the d18O record, the frequency of vegetation shifts from

glacial to interglacial periods is apparent.

Papionin Evolution in Southern Africa

Gear (1926) was the first to provide preliminary descriptions of

papionin specimens found at Taung and concluded that there were two

forms present. The differentiation ofParapapio from Papio has relied on

morphological differences including a shortened muzzle, lack of an ante-

orbital drop, a sloping face, and the reduction of the hypoconulid of M3,

among other traits (Williams et al., 2007). Gilbert (2007) has suggested

that specimens from Taung referred to Pp. antiquus should be reclassified

as Procercocebus antiquus to support evidence of polyphyly in mangabeys.

This change is of particular interest to this study as this species is only

found at Taung. Although Pp. antiquus exhibits a microwear signal

distinct from those species from Sterkfontein Member 4, substantial

overlap across the genus does not support thisnew taxonomic attribution.

Approaches to Examining Dental Microwear

Various methods have been employed in order to understand how

dental microwear preserves information concerning food processing

and consumption; each has strengths and weaknesses that can be

summarized using three criteria: (1) resolution, referring to the degree

FIGURE 2Maps of South Africa showing simulated vegetation cover for the mid-Pliocene, glacial and interglacial periods, and the present day, along with d18O data,

illustrating paleoenvironmental variability; T 5 Taung site; S 5 Sterkfontein Member 4. Paleoclimate models modified after Hughes et al. (2008); present-day vegetation cover

adapted from Cowling et al. (2008); d18O values adapted from deMenocal (2004).

PALAIOS PALEOECOLOGICAL RECONSTRUCTION OF TAUNG, SOUTH AFRICA 441


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of detail detected and the type of information collected; (2) expense, interms of both resources and time; and (3) reliability. Methods for

observing dental microwear at different scales include low-magnifica-tion stereomicroscopy (LMS), scanning electron microscopy (SEM),

and confocal microscopy (CM).

LMS was one of the earliest methods employed to examine dentalmicrowear. While LMS provides a relatively low resolution (353), it

features high repeatability and low observer error (Semprebon et al.,

2004). SEM provides the highest resolution (e.g., Teaford et al., 1996)and micrographs can be analyzed with various computer programs(Ungar, 2002) to compare dimensions and frequencies (Walker et al.,

1978; Gordon, 1984; Teaford et al., 1996; Grine et al., 2002). CM is a

more recent alternative and has proven effective in differentiating thefracture properties of foods ingested by extinct hominins (Scott et al.,

2005, 2006). All of these methods are capable of covering a similar areaof the tooth and have been demonstrated to be effective in determining

some of the physical properties of the food resources exploited by anindividual.

Further complicating the study of dental microwear are taphonomic

alterations, which can render dental microwear features unreadable;however, King et al. (1999) examined the effect of taphonomic

processes on dental microwear and found that microwear was either

obliterated by the taphonomic process or survived unchanged. Theresulting obliteration is easily distinguishable and is the primarydeterminant of the appropriateness of a tooth for dental microwear

examination. Additionally, mandibular corpus width and depth andmandibular length have been demonstrated to have predictable effects

on molar microwear by variably affecting the amount of compressionand shear and therefore the size of microwear features in humans

(Mahoney, 2006). The unintended ingestion of materials during feedingalso appears to affect dental microwear signals. Mainland (2003) found

that the ingestion of soil during grazing and browsing could affect thedental microwear signals of Gotland sheep (Ovis aries). Similar effects

have been noted in Papio ursinus, where the ingestion of large amountsof exogenous grit from the exploitation of hypogeous foods during the

dry season resulted in larger microwear features and higher numbers of

pits (Daegling and Grine, 1999).

Dental microwear evidence can provide information about the dietarydifferences between specimens and the types of resources that are

available in a given environment. To the degree that there is aphylogenetic component to similarity in diet, dental use-wear scars may

reflect phylogenetic relationships among the fossil primates. Comparingthe dental microwear of fossil Parapapio and Papio to extant Papio ursinus

can help to clarify differences between the types of foods utilized by eachgroup. These potential differences are employed here to address whether

the habitat of the Taung child, A. africanus, differed from the fairly xericecology characterizing the Cape region of present-day South Africa.

MATERIALS AND METHODS

Resin dental casts were obtained from dental impressions molded

directly on the molars of specimens using polyvinylsiloxane (PresidentPlus Jet Regular Body-Surface Activated 4605, Coltene/WhaledentInc.). When necessary, previously applied shellac was removed from the

specimens using Zip Strip (Star Bronze Co.), followed by theapplication and drying of 95% isopropyl alcohol to remove the Zip

Strip (Semprebon et al., 2004). Dental microwear was observed onepoxy resin casts of the dental molds. These casts were created by

mixing resin and hardener (EpoKwick, made by Buehler Ltd.). The

catalyzed casting material was centrifuged to remove air pockets. Thecasting resin was then poured into putty crucibles that were stabilized

using putty hardener (Coltene/Whaledent Inc.).

A total of 65 specimens were examined, consisting of Pp. antiquus (n

5 8), P. izodi (n 5 12), and indeterminates (n 5 10) from Taung; Pp.

broomi (n 5 10) and Pp. jonesi (n 5 5) from Sterkfontein Member 4;

and the only living papionin native to the Cape region of southernAfrica, P. ursinus (n 5 20). Papio ursinus from the Western Cape,Orange Free State, and Transvaal region were examined from thecollections of the South African Museum (Cape Town). All Pp. broomi

and Pp. jonesi specimens were molded at the Transvaal Museum

(Pretoria). Fossils attributed to Pp. antiquus, P. izodi, and indetermi-nate Taung specimens were molded at the University of theWitwatersrand (Johannesburg), the Transvaal Museum, and the

American Museum of Natural History (AMNH, New York). Thespecimens from the AMNH were on loan from the University ofCalifornia (Berkeley) to Eric Delson at the time. All of the specimen

numbers with associated repositories are listed in Supplementary Data 11.

To safeguard against misinterpreting postmortem taphonomic fea-tures as resulting from diet, El-Zaatari et al. (2005) examined resin dentalcasts under light microscopy before preparing specimens for SEM, and asimilar procedure was followed here. Evidence of postmortem taphon-

omy included shiny or polished surfaces or an overabundance ofrefractive (small) pits indicative of highly crenulated surfaces which areatypical of dietary scars. Extant Papio ursinus was observed to identifypatterns of dental microwear that are relatively free of postmortemtaphonomy for comparison with the fossil specimens. Areas of the

occlusal surface that were obviously damaged from casting, molding, or

taphonomic processes were excluded from the study.

Observations of Dental Microwear

Using LMS, microwear features were distinguished by their lightrefractive properties through the use of external illumination with afiber-optic light source positioned obliquely to the occlusal plane of aresin dental cast. Sampling was limited to a 0.4 mm2 area on the

paracone of the second molar and six variables were counted perspecimen: (1) small pits, (2) large pits, (3) fine scratches, (4) coarsescratches, (5) hypercoarse scratches, and (6) puncture pits (Godfrey etal., 2004; Semprebon et al., 2004). Two trials were conducted per

specimen and the average value for each feature was included insubsequent analyses (see Supplementary Data 11 for these data and

Supplementary Data 21 for descriptive statistics by taxon).

Small pits are shallow, easily refract light, and the entire range ofthem can be observed when an external light source is maneuveredobliquely. Large pits are deeper, less refractive, and at least two timeslarger than small pits. Excessive pitting has been associated with hard-

object exploitation in both ungulates and primates (Semprebon et al.,2004). Fine scratches, possibly resulting from the silicates in grasses, areshallow, refractive, and associated with graminivory (Godfrey et al.,2004). Coarse scratches are also somewhat refractive, but they aredeeper and reflect coarser dietary items than those typical of grasses.

Hypercoarse scratches and puncture pits are much heavier, nonrefrac-tive features. Hypercoarse scratches are steep-sided furrows etched ontothe occlusal surface, possibly from a particle being dragged along themolar cusps during mastication. Particles might include grit adhering torhizomes, tubers, corms, or bulbs as well as particles from the hard

endocarp of seed coats. Puncture pits (and smaller pits) may also resultfrom seed predation, hard-object feeding, or possibly from theinadvertent mastication of exogenous grit and small rocks during theconsumption of underground storage organs (USOs); these scars haveirregular edges and can be described as perforations of the occlusalsurface. A large puncture pit can be 25% of a 0.4 mm2 ocular reticle.

The paracone is a large mesial-buccal cusp on the maxillary secondmolar (M2). It exhibits a broad surface that is only moderately steepand does not extend deeply into the talon basin. Therefore, theparacone is relatively flat and thus captures the dietary signal of foodsthat are crushed and pulverized rather than sheared. Use-wear scars

were counted along the broad flat face of the paracone unless

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taphonomic evidence obscured this surface. The cuspal edge was

avoided to standardize the observations.

All of the data were collected by one of the authors (JWP) toeliminate possible intra-observer error. An error study was performed

on microwear counts of 10 specimens. The microwear features of each

specimen were counted on two separate occasions and the resulting

counts were examined by a t-test and a Mann-Whitney U test tomeasure the intra-observer error, yielding insignificant differences

between the trials (p values 5 0.8570.264 for t-test and 0.300.875 for

the Mann-Whitney U). We acknowledge that one can have high error

and no significant difference between two trials. To address this issue,JWP counted microwear features on eight teeth twice in succession andthe mean percent difference for each microwear feature was calculated

(100 3 absolute difference between trial1 and trial2/mean of two

observations). The smallest mean percent difference for the two trials

was lowest for small pits (4.8%) and coarse scratches (6.7%) andsomewhat higher for fine scratches (11%) and large pits (11.7%). Both

puncture pits and hypercoarse scratches had mean percent differencesof 0% owing to the scarcity of these heavy use-wear scars in the

specimens. These absolute error rates are consistent with other studies

of dental microwear (Grine et al., 2002; Semprebon et al., 2004).

As Semprebon et al. (2004) found in their assessment of the validity

of LMS in determining primate diets, graminivory is associated withhigh frequencies of scratches. In their study, graminivores made up the

lower right angle of what they called the use-wear trophic triangle,while browsers occupied the left corner and mixedhard-object feeders

were at the apex. In general their results indicate that primate

graminivores, hard-object specialists, and leaf browsers are distin-guished by relative frequencies of pits and scratches, i.e., high numbers

of scratches and low numbers of pits for graminivores, low numbers of

scratches and pits for folivores; and high numbers of scratches and pits

for seed predators and extractive foragers. It is important to note thatwhile primates often concentrate on certain resources, many of their

diets can be quite flexible and difficult to categorize.

One-way analysis of variance (ANOVA), with posthoc TukeysHonestly Significant Differences (HSD), was employed to compare

differences between the four taxa separately for each microwear feature.

Linear regressions were performed to assess the significance of the

relationship between each pair of microwear features. For significant

associations between traits, a bivariate plot was used to show the overalldifferences between the taxa with respect to these features, and linear

regressions with 95% confidence ellipses around group centroids wereused to assess differences (Figs. 34). Since the heavier microwear

features, such as hypercoarse scratches and puncture pits, were only

rarely observed in these taxa, ANOVA and linear regression for these

traits were impractical. In this case we utilized a bar graph to show the

mean counts of these features within two standard deviations. Principal

components analysis (PCA) of four common microwear features showsthe patterns of variance and covariance within the dataset. Canonicalscores generated from a discriminant function analysis show the

placement of indeterminate specimens from Taung. Finally, total pit

and scratch counts were compared to an approximation of the use-wear

trophic triangle of Semprebon et al. (2004).

RESULTS

Analysis of Variance

The ANOVA results (Table 1) demonstrate significant differences

exist across taxa for each dental microwear feature. The F values show

that substantial between-group differences are evident; however, the F

value for fine scratches is an order of magnitude larger than thoseassociated with the other use-wear features.

Tukeys Honestly Significant Differences

Table 2 shows that indeterminate specimens exhibit significant

differences in small pits compared to Pp. antiquus and Pp. broomi. TheP. ursinus sample is significantly different in counts of small pits from allParapapio species, including Pp. antiquus from Taung. The fossils

attributed to Pp. broomishow a significant difference in presence of large

pits compared to P. ursinus and indeterminate Taung specimens.

Indeterminate specimens are also significantly different in the presence

of fine scratches when compared to Pp. broomiand P. ursinus (Table 3);

however, it is P. ursinus that is significantly different from all of the fossil

FIGURE 3Bivariate comparison of number of small pits versus number of finescratches. For each taxon, 95% confidence ellipses around group centroids are shown.

Star5 P. ursinus (P. u.); X 5 P. izodi(P. i.); cross 5 Pp. antiquus (Pp. a.); circle 5 Pp.

jonesi (Pp. j.); triangle 5 Pp. broomi (Pp. b.); rectangle 5 indeterminate (indet.).

FIGURE 4Bivariate comparison of small pit and coarse scratch counts, showing

95% confidence ellipses around group centroids. Star 5 P. ursinus (P. u.); X 5 P.

izodi (P. i.); cross 5 Pp. antiquus (Pp. a.); circle 5 Pp. jonesi (Pp. j.); triangle 5 Pp.

broomi (Pp. b.); rectangle 5 indeterminate (indet.).



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taxa for the presence of fine scratches. The sample of Pp. broomi also

shows a significant difference in fine scratches compared to Pp. antiquus

and P. izodi, suggesting that distinctions between the signals from

Sterkfontein and Taung also exist. Reinforcing this distinction is the

significantly great number of coarse scratches in P. izodi from Taung

compared to Pp. jonesifrom Sterkfontein. Sterkfontein specimens are not

uniform, however, as significant differences exist between Pp. jonesiand

Pp. broomi in the presence of coarse scratches.

Linear Regression

Linear regression of each pair of microwear features yielded

significant values only for the comparison between small pits and fine

scratches (p 5 0.024), and between small pits and coarse scratches (p 5

0.036; Table 4). These significant differences are emphasized in

bivariate plots to show the extent to which differences among taxa

can be demonstrated with these pairs of use-wear features. The 95%

confidence ellipses around group centroids show that P. ursinus is

distinct with its higher number of fine scratches, while Pp. broomi is

divergent in its presence of small pits (Fig. 3). The other taxa show a

large degree of overlap. For the comparison between small pits and

coarse scratches, Pp. jonesiis distinct from other taxa and only overlaps

with Pp. antiquus (Fig. 4). The range for indeterminate specimens

completely surrounds the relatively small confidence ellipse of P.

ursinus and extends into that ofP. izodiand Pp. broomi, suggesting that

some indeterminates may be classified as either Papio or Parapapio.

Mean Counts of Hypercoarse Scratches and Puncture Pits

The heaviest microwear featuresare relatively rarein the taxa examined

and mean counts with two standard deviations are shown in Figure 5.

The largest number of heavy microwear features is exhibited by P. izodi,

followed by Pp. broomi. The Taung indeterminate specimens and Pp.

antiquus resembleone anotherin the number of hypercoarse scratches and

the lack of puncture pits, whereas P. ursinus exhibits the opposite

configuration with some puncture pits but no hypercoarse scratches.

Principal Components Analysis

In Figure 6, a PCA is shown and the associated component loadings

are listed in Table 5. PC Axis 1 explains 37.5% of the variation, while PC

Axes 2 and 3 each explain 26.0% of the variation (PC Axis 3 not shown).

The first axis largely separates extant baboons (P. ursinus) with positivescores and fossil taxa with negative scores. The primary exception is theplacement of the fossil P. izodi, which overlaps slightly within the 95%

confidence ellipse of the group centroid for P. ursinus. Some individualswith scores close to zero were difficult to classify and included primarily

the indeterminate specimens, suggesting that dental microwear mimicsthe morphological ambiguities of these specimens. Parapapio antiquus

overlaps extensively with Pp. jonesi and the two exhibit a more eclecticdental microwear signal on PC Axis 1 compared to Pp. broomi from

Sterkfontein and P. izodifrom Taung. Some indeterminate specimensfallwithin the range of Pp. antiquus (T 125958, T 56658, and T 13), whileothers share more similarities with P. izodi. These observations arereflected in the high negative loading of small pits and high positiveloadings of fine and coarse scratches on PC Axis 1 (Table 5).

Along PC Axis 2, Pp. broomi from Sterkfontein is distinct fromindeterminate individuals and P. izodi from Taung due to the greaterproportion of large pits (Table 5). The Taung fossils, including Pp.antiquus, P. izodi, and indeterminate specimens, are not well separatedfrom one another. The Pp. antiquus sample shares substantial overlap

with Pp. broomiand Pp. jonesifrom Sterkfontein, but is not distinct fromfossil and extant Papio. The sample ofPp. antiquus has a larger range ofvalues than P. izodion PC Axis 2, overlapping somewhat more with Pp.broomifrom Sterkfontein than other fossil primates from Taung.

Discriminant Function Analysis

Canonical scores axes derived from discriminant function analysis,plotted with 95% confidence ellipses around group centroids, show cleardistinctions between the taxa (Fig. 7). The fossils are largely distinct fromextant P. ursinus along the first axis, based on the relatively large number

of fine scratches compared to other microwear features for this taxon(Table 5). Parapapio broomi is isolated from Pp. jonesi on canonicalscores axis 1; these two Sterkfontein taxa are also distinct from the Taungfossils which show extensive overlap. The relative number of coarsescratches and small pits with respect to the other features helps to explainthe positive projection of the taxa from Taung (Pp. antiquus, P. izodi, andindeterminates). Along the second axis, P. ursinus is largely distinct fromParapapio, particularly Pp. broomiand Pp. jonesi, by the relatively large

number of small pits in the latter two taxa. Also along the second axis, P.ursinus and P. izodiare similar, along with most indeterminate specimensfrom Taung, primarily due to the relatively large number of coarsescratches (Table 5).

TABLE 1ANOVA results for each dental microwear feature compared to taxon

(significant results in bold).

F value p value

Small pits 7.736 0

Large pits 2.651 0.031

Fine scratches 28.204 0

Coarse scratches 5.159 0.001

TABLE 2Tukeys Honestly Significant Differences Post-Hoc ANOVA for small

pits (below) and large pits (above) by taxon (significant results in bold). Pp. 5

Parapapio; P. 5 Papio.

Indeterminate

P.

izodi

Pp.

antiquus

Pp.

broomi

Pp.

jonesi

P.

ursinus

Indeterminate 1 1 0.05 0.957 1

P. izodi 0.636 1 0.07 0.957 1

Pp. antiquus 0.008 0.219 0.083 0.97 1

Pp. broomi 0.006 0.209 1 0.612 0.029

Pp. jonesi 0.096 0.662 0.998 0.999 0.977

P. ursinus 0.999 0.261 0.001 0.001 0.026

TABLE 3Tukeys Honestly Significant Differences Post-Hoc ANOVA for fine

scratches (below) and coarse scratches (above) by taxon (significant results in bold).

Pp. 5 Parapapio; P. 5 Papio.

Indeterminate

P.

izodi

Pp.

antiquus

Pp.

broomi

Pp.

jonesi

P.

ursinus

Indeterminate 0.574 0.242 1 0.075 1

P. izodi 0.872 0.004 0.773 0.001 0.248

Pp. antiquus 0.999 0.703 0.136 0.963 0.221Pp. broomi 0.001 0.004 0 0.04 0.989

Pp. jonesi 0.853 1 0.71 0.083 0.065

P. ursinus 0.001 0.001 0.001 0.015 0.001

TABLE 4Linear regression results for each pair-wise comparison of dental

microwear features (significant results in bold).

F value p value

Small pits vs. large pits 1.476 0.229

Small pits vs. fine scratches 5.312 0.024

Small pits vs. coarse scratches 4.592 0.036

Large pits vs. coarse scratches 0.01 0.921

Coarse scratches vs. fine scratches 2.387 0.127



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Comparisons to the Use-Wear Trophic Triangle

All of the taxa examined fall into the upper and lower left areas of

Semprebon et al.s (2004, fig. 3) use-wear trophic triangle. Many

specimens display a relatively high degree of pitting and a range of

scratches from very few to moderate amounts (Fig. 8). Some P. ursinus

specimens correspond to primate leaf browsers while others exhibit

relatively greater numbers of pits. None of the fossils falls within the

range of primate grazers characterized by a high scratch and low pit

count (Semprebon et al., 2004). Additionally, none of the specimens

examined exhibit relatively large numbers of both pits and scratches

typical of seed predators and hard-object specialists. All of the fossil

specimens exhibit a greater number of pits than observed in Semprebon

et al.s primate leaf browsers (Fig. 8).

DISCUSSION

It is generally possible to distinguish fossil from extant taxa and evenParapapio from fossil Papio based on dental microwear signals. This

implies a difference in the exploitation or availability of resourcesbetween the extinct and extant taxa. The results offer no support for the

attribution of Pp. antiquus at Taung to Procercocebus as proposed by

Gilbert (2007).

Paleoenvironment

The initial appearance of C4 grasses during the late Mioceneearly

Pliocene and the subsequent expansion of this biome around 1.7 Ma

(Hopley et al., 2007) seem to be related to regional climatic variation

driven by global climatic changes. Taung and Sterkfontein appear to

be roughly contemporaneous, dating to a little before 2 Ma, and

likely shared similar although not identical environments. Fine

scratches and their relationship to small pits emerge as one of the

FIGURE 5Histogram showing average counts of hypercoarse scratches and

puncture pits per taxon with two standard deviations; star 5 P. ursinus; X 5 P.

izodi; cross 5 Pp. antiquus; circle 5 Pp. jonesi; triangle 5 Pp. broomi; rectangle 5

indeterminate (indet.); X 5 P. izodi; star 5 P. ursinus; cross 5 Pp. antiquus; triangle 5

Pp. broomi; circle 5 Pp. jonesi.

FIGURE 6Principal components axes 1 and 2 shown with 95% confidence ellipses

around group centroids. Star 5 P. ursinus (P. u.); X 5 P. izodi (P. i.); cross 5 Pp.

antiquus (Pp. a.); circle 5 Pp. jonesi(Pp. j.); triangle 5 Pp. broomi (Pp. b.); rectangle

5 indeterminate (indet.).

TABLE 5Component loadings for principal components axes and canonical

discriminant functions standardized by within variance for canonical scores axes.

Principal

components axis 1

Principal

components axis 2

Canonical

scores axis 1

Canonical

scores axis 2

Small pits 20.769 0.193 0.15 0.854

Large pits 20.192 0.937 20.157 0.488

Fine scratches 0.67 0.252 21.021 0.17

Coarsescratches 0.651 0.245 0.278 21.161

FIGURE 7Canonical scores axes 1 and 2 shown with 95% confidence ellipses

around group centroids. Star 5 P. ursinus (P. u.); X 5 P. izodi (P. i.); cross 5 Pp.

antiquus (Pp. a.); circle 5 Pp. jonesi (Pp. j.); triangle 5 Pp. broomi (Pp. b.); and

rectangle 5 indeterminate (indet.).



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distinguishing factors between extant P. ursinus and fossil specimens(Figs. 67).

There is a significant amount of overlap between P. ursinus and P.

izodi, suggesting that increased dietary flexibility may have played apivotal role in the success of this genus. Fecal isotope studies of P.ursinus with distinctly different diets in two separate South Africansavanna habitats demonstrate this flexibility (Codron et al., 2006).

Diets in the two environments were shown to consist of ,10%20%

and ,30%50% C4 grasses and CAM-photosynthesizing succulents.

Based on this isotopic data, it is likely that some portion of theobserved scratches on the teeth of P. ursinus resulted from the

utilization of grasses. In addition, P. ursinus has been observed toexploit USOs, which are typically found in non-graminaceous C4 plants

(Hill and Dunbar, 2003). Papio ursinus, however, generally lacks thelarge number of heavy use-wear scars found in fossil P. izodi (Fig. 5)

and lacks the heavy pitting associated with fossil Parapapio and Papio

(Fig. 3). The practice of washing USOs prior to consumption in P.

ursinus may significantly reduce the exogenous grit ingested.The fossil specimens display higher degrees of pitting than are typical

of primate leaf browsers (Fig. 8). This suggests the possibility that these

primates were incorporating foods with more resistant properties suchas USOs. Other fossil primates with extremes in pit frequencies, such asHadropithecus stenognathus, have been postulated as USO exploiters(Catlett et al., 2010; L.R. Godfrey, personal communication, 2010).

Plants with USOs typically occur in arid areas but are often found in

riverine habitats as well. Dominy et al. (2008) found that the USOs arehard and tough, consistent with higher incidences of pitting. The heavy

pitting observed in fossil Parapapio may stem from the consumption ofexogenous grit adhering to USOs or the USOs themselves. The two

primate taxa from Taung, P. izodi and Pp. antiquus, exhibit some

overlap in the hard components of their diets. Although fossil P. izodi

exhibits larger average numbers of hypercoarse scratches and puncturepits (Fig. 5), Pp. antiquus may have generally incorporated greater

amounts of gritty foods as evidenced by their higher small and large pitfrequencies.

It is important to emphasize that microwear can provide information

about the physical properties of the foods that were consumed. While

lighter microwear features have become associated with softer foods(often graminaceous C4 plants) and heavier features with harder foods

(often C3 plants), the distinction between C3 and C4 plants based onmicrowear is not straightforward. In fact, discrepancies between

analyses of dental microwear that indicate hard objects in the dietand associated muscularity (and therefore C3 resources) and stable

carbon isotopes, indicating high proportions of C4 resources, have beennoted among the australopiths leading to what has been termed the C 4conundrum (Sponheimer and Lee-Thorp, 2003).

Isotopic analysis ofParapapio specimens from Sterkfontein Member4 indicates that #40% of their diet consisted of C4 resources (Codron et

al., 2005). USOs, however, occur in both C3 and C4 plants and the

exploitation of USOs by mole rats has been shown to produce variableisotopic signatures (Yeakel et al., 2007). The dental microwear signals

of the extinct specimens from both Taung and Sterkfontein Member 4

may indicate that gritty foods were available and exploited at these

sites. Nevertheless, substantial scratch frequencies in both Pp. broomiand P. izodi (although much less than in P. ursinus) indicate thepossibility of grasses contributing to the diet at each of these sites.

The two taxa from Sterkfontein Member 4 exhibit some degree of

overlap. While both groups appear to have largely exploited harder

foods as indicated by their high pit frequencies, Pp. broomistands apartfrom Pp. jonesi with respect to scratch and puncture-pit frequency.

These microwear features appear to support the conclusions of Fourieet al. (2008), who found no craniometric evidence to support separateParapapio species at Makapansgat but found that two dietary groupsexisted thereone with a mixed C3 diet, including significant amounts

of rootstocks (loosely correlated with Pp. broomi), and another with a

mixed C4 diet (Pp. whitei and Pp. jonesi). The likelihood that USOswere exploited to some degree by the taxa examined in the present study

agrees with isotopic evidence of C4 utilization in Parapapio atSterkfontein Member 4 (Codron et al., 2008). It appears that in some

cases, such as in P. izodi, grassland components were more heavilyincorporated into the dietary repertoire. The microwear signals of the

specimens seem to reflect the regional variability of climate, includingthe general trend toward increasingly drier conditions associated with

the expansion of C4 grasses, which must have been experienced at some

level by the Taung child.

Parapapio antiquus from Taung

Gilbert (2007) suggests that Pp. antiquus from Taung should be

reassigned to a new taxon, Procercocebus antiquus, based on theobserved similarities in premolar dimensions and craniomandibular

morphology between these specimens and living mangabeys of the

genus Cercocebus. Gilbert (2007) also points to genetic data to supporta taxonomic shift in African papionins by 6.96.1 Ma into two groups,Theropithecus-Lophocebus-Papio and Mandrillus-Cercocebus, with each

group sharing a common ancestor 3.43.0 Ma and 4.13.6 Ma,respectively (Tosi et al., 2003). It is also suggested that based on the

divergence dates, the Cercocebus lineage was present in Africa by 2.0

1.5 Ma. While this is a reasonable assumption, it does not necessitatethe presence of Procercocebus at Taung. To the extent that diet

approximates phylogeny, the use-wear patterns observed at Taung canalso be considered in the discussion of species attribution. As shown

here, the Parapapio specimens display a considerable degree of overlapin their microwear signals, and the genus can generally be distinguished

from fossil and particularly from extant Papio. The sample of Pp.

antiquus is more similar to Sterkfontein Parapapio than its purported

FIGURE 8Total pits and total scratches in sample compared to an approximated

use-wear trophic triangle (Semprebon et al., 2004; fig. 3). The three points of the

triangle consist of average counts of pits and scratches for (1) primate leaf browsers

with relatively low numbers of pits and scratches (including Lepilemur, Avahi,

Alouatta, Trachypithecus, Nasalis, Colobus, and Symphalangus), (2) primate

graminivores (e.g., Hapalemur and Theropithecus) characterized by high scratch

low pit counts, and (3) primate hard-object specialists (including seed predators such

as Cacajao, Chiropotes and Pithecia, as well as extractive foragers such as Cebus and

Daubentonia), which exhibit relatively large numbers of both pits and scratches. Taxa

from Semprebon et al. (2004). Star 5 P. ursinus (P. u.); X 5 P. izodi (P. i.); cross 5

Pp. antiquus (Pp. a.); circle 5 Pp. jonesi (Pp. j.); triangle 5 Pp. broomi (Pp. b.); and

rectangle 5 indeterminate (indet.).



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contemporaries at Taung and lacks any discernable evidence for seedpredation or extractive foraging (Fig. 8) that might link it to extantCercocebus. Therefore, the reassignment of Parapapio antiquus to anovel primate genus, Procercocebus, lacks support from analyses ofdental microwear. Furthermore, a few indeterminate specimens fall

within the range of Pp. antiquus (e.g., T 13, T 125958, and T 56658).Most other indeterminate specimens may be affiliated with P. izodi.

CONCLUSIONS

The dental microwear evidence presented in this study appears to fitwell with previous paleoecological reconstructions. It also agrees withsuggestions that dietary flexibility played an important role in thesuccess of papionin and hominin taxa in adapting to the shift to morearid and open environments across southern Africa beginning in thelate Miocene (Codron et al. 2008). Based on these results, extinct P.izodi stands apart from Parapapio sp. and resembles extant P. ursinus

more than the other fossil taxa. While diet represents only one aspect ofthe evolution of species, the increased dietary flexibility of Papio

undoubtedly contributed to the success of this genus in southern Africa.These findings also help to infer the ecological habitat experienced bythe Taung child. It is likely that the open woodland environment of

Taung, with significant proportions of C4 resources, may haveconstrained the dietary resources available to both australopiths andpapionins, although the isotopic signatures of australopiths appear tobe more variable than both extinct and extant papionins (Codron et al.,2008). The incorporation of C4 resources into the diets of papionins andhominins may be related to this dietary shift. About 2 Ma, however, the

habitat at Taung (and Sterkfontein Member 4) probably containedfewer open grassland resources than is typical of much of contemporarycentral South Africa.

ACKNOWLEDGMENTS

We thank the curators who generously allowed FLW to make dentalmolds, including Francis Thackeray at the Transvaal Museum(Pretoria), Mike Raath at the University of the Witwatersrand Medical

School (Johannesburg), Denise Hammer at the South African Museum(Cape Town), and Eric Delson at the American Museum of NaturalHistory (New York City). Brian Carter, Gretchen Clymer, Kathryn

Hudson, Sean Kiskel, Robin McLauchlin, Michael McPherson, DarbyProctor, Jessica Raines, and Lindsay Slowiczek kindly assisted in

preparing the resin casts. We thank Laurie Godfrey, Gina Semprebon,and the Associate Editor for their suggested improvements to the paper.This research was supported by a Research Team Grant, a ResearchProfessional Enhancement Grant, and a Tech Fee Grant from the VicePresident for Research, Georgia State University.

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