Dietary Proclivities of Paranthropus Robustus from Swartkrans, South Africa

Dietary proclivities of Paranthropus robustus Frank L’Engle Williams

Anthropological Review • Vol. 78 (1), 1–19 (2015)

ANTHROPOLOGICAL REVIEW Available online at: www.degruyter.com Journal homepage: www.ptantropologiczne.pl

Dietary proclivities of Paranthropus robustus from Swartkrans, South Africa

Frank L’Engle Williams

Department of Anthropology, College of Arts and Sciences, Georgia State University, Atlanta, Georgia, United States of America

Abstract: Pleistocene Paranthropus robustus fossils from Swartkrans have yielded stable isotope values suggesting some foraging on C4 plants possibly including underground storage organs. Dental microwear texture analysis on P. robustus (SK 6, SK 34 and SK 47) from Swartkrans Member 1 is performed to examine whether tooth surface damage from mastication agrees with prior dietary inferences from carbon isotopes. There is considerable variation in textural characteristics among the P. robustus specimens. Specifically, adult SK 34 stands apart from the two subadult specimens, SK 6 and SK 47, suggesting life history could be reflected in patterns of dental microwear texture characteristics, although seasonality and availability of fallback foods may also explain the variation observed in P. robustus. The fossils all exhibit elevated surface texture complexity, resembling the values for Lophocebus albigena and Cebus apella, and to a lesser extent, Pan troglodytes. Paranthropus robustus is dissimilar to primary folivores, such as Trachypithecus cristatus or folivore-frugivores such as Alouatta palliata suggesting leaves comprised very little of its diet. The textural fill volume of P. robustus differs from that observed in extant primates from tropical forests indicating extreme durophagy, perhaps a function of differences in habitat. Ingestion of extraneous grit on the underground parts of plants and from terrestrial resources, perhaps as fallback foods or as dietary staples, may account for these enamel textural properties and may help explain the mixed C3/C4 isotopic signal in P. robustus.

Key words: Australopithecus, underground storage organs, dental microwear, grit, Pleistocene

Introduction has yielded by far the greatest number of specimens attributed to P. robustus (Brain Paranthropus (or Australopithecus) robus- 1981; de Ruiter et al. 2008). Paranthropus tus was endemic to southern Africa and robustus was reconstructed as a dedicated existed between circa 1.9 million years biped and exhibits flat bulbous cusps on ago (Ma) to approximately 0.7 Ma (Vrba relatively large molars, molariform pre- 1995; Wood and Strait 2004). The Hang- molars, small incisors and short blunt ing Remnant of Swartkrans Member 1 canines (Robinson 1954). This suite of

Original Article: Received: September 16, 2014; Accepted for publication: January 8, 2015 DOI: 10.1515/anre-2015-0001 © 2015 Polish Anthropological Society 2 Frank L’Engle Williams dental features has been attributed to the Prior dietary reconstructions excessive grinding of hard objects (Rob- inson 1954). The purpose of this study is In his dietary hypothesis, Robinson to investigate three specimens of P. robus- (1954) posited P. robustus as a consum- tus (SK 6, SK 34 and SK 47) which have er of tough vegetation as opposed to A. not been previously examined (Scott et africanus which was described as more al. 2005). The fossils are compared to ex- omnivorous. Robinson (1954) arrived tant primate taxa using dental microwear at this conclusion by observing the ex- texture analysis to address how this tensive wear on P. robustus molars and suite of enamel characteristics evolved in premolars, enamel chipping of the pos- southern Africa during the early Pleisto- terior teeth, buccolingual scratches on cene. the postcanine dentition, the massive bone accumulation around the roots of Paleoecological setting the molars and premolars, and extreme craniofacial superstructures. He attribut- It has long been assumed that P. robustus ed the enamel chipping to the ingestion lived in an open grassland environment of the gritty underground parts of plants given the larger number of grazers com- as observed in chacma baboons (Papio ur- pared to browsing ungulates preserved sinus) which consume rhizomes, bulbs, at Swartkrans (Vrba 1985), along with corms and roots, particularly in the aus- grazing primates such as Theropithecus tral winter. These could have been fall- oswaldi (Elton 2007). The paleoecology back foods for P. robustus in these season- of Swartkrans has been reconstructed al environments. as a relatively open habitat with some Jolly (1970) suggested P. robustus, like edaphic grasslands and a permanent earlier Australopithecus was a seed pred- water source in the region (Brain 1981; ator capable of utilizing a side-to-side 2004; Delson 1984; Vrba 1985; 1995; grinding action of the teeth. The relatively Reed 1997; Avery 2001; Reed and Rec- small anterior dentition, similar to gram- tor 2006). However, as the number of nivores such as Theropithecus, seemed to bovid grazers increased, the number of corroborate seed predation in P. robustus. P. robustus in the fossil assemblages de- Further dietary implications arose from creased. This inverse relationship sug- investigation of incisor microwear in P. gested P. robustus may have preferred robustus which exhibits a smaller density riverine woodlands compared to open of features compared to A. africanus, sug- areas (de Ruiter et al. 2008). The micro- gesting less food preparation occurred mammalian community recovered from with the anterior dentition (Ungar and Swartkrans Member 1 indicated both Grine 1991), perhaps replaced with the moist and arid grassland taxa were pres- use of stone and bone tools (Wood and ent (Avery 2001). Swartkrans deposits Strait 2004). The mesiodistally narrow may have been interred during inter- incisors of P. robustus, intermediate be- glacial intervals (Brain 1981), and may tween Homo erectus and modern H. sapi- have exhibited lower annual rainfall and ens, also signaled a limited degree of food higher mean temperatures compared to processing and paramastication using the the current climatic conditions (Avery anterior teeth (Ungar and Grine 1991). 2001). These dimensions differed from those Dietary proclivities of Paranthropus robustus 3

characterizing Pliocene australopiths sumed a considerable amount of C4 re- which had much wider incisors, although sources which comprised 25–30% of its not as wide relative to reconstructed body diet (Lee-Thorp et al. 1994). Such isotop- size as those of the great apes (Teaford ic variation may be indicative of a habitat and Ungar 2000). The small incisors of P. generalist and could have resulted from robustus suggested large food items were the consumption of sedges, termites, avoided unless they were prepared us- grasses, the underground storage organs ing technology (Wood and Strait 2004). (USOs) of C4 plants (de Ruiter et al. Its flattened molars and lack of shearing 2008), and/or animal protein from graz- crests indicated a lack of folivory (Teaford ers (Lee-Thorp et al. 1994). Seasonality and Ungar 2000). probably affected the diet of P. robustus Paranthropus robustus also exhibited as preferred foods may have been availa- a greater incidence of pitting than did A. ble only during part of the year. Further- africanus suggesting greater hard-object more, Swartkrans bordered moist and feeding in the former (Grine 1986). The arid biomes, presenting a wide array of massive mandibular corpus of P. robust- habitats potentially exploitable by P. ro - us signaled an adaptation to durophagy bustus (Avery 2001). with jaws capable of withstanding sig- Ratios of Sr/Ca for P. robustus suggest- nificant functional demands related to ed omnivory, perhaps with some animal wish-boning or torsion when hard-ob- protein in the diet like fossil carnivores jects were consumed (Teaford and Ungar preserved at Swartkrans Member 1 (Sil- 2000). Furthermore, P. robustus may have len 1992; Sillen et al. 1995). Inter-sea- consumed grit laden foods or masticated sonal and inter-annual isotopic variation opal phytoliths in plants (Grine 1981). in the diet of P. robustus was identified Paranthropus robustus was found to exhib- using perykymata (Sponheimer et al. it greater enamel surface complexity and 2006b). The buttressed face, postcanine less patterning of dental microwear tex- megadonty and thick enamel cap of P. ro- tures than Australopithecus africanus (Scott bustus may also be indicative of a broad et al. 2005), and to exhibit greater tex- dietary niche that included fallback foods tural complexity than early Homo (Ungar (Wood and Strait 2004). and Scott 2009; Ungar et al. 2010). Australopiths from the South Africa Inferring diet and paleoecology caves were associated with a diet distinct from that sampled from the great apes The aim of this study is to infer the diet (Sponheimer and Lee-Thorp 2003; Spon- of P. robustus and to substantiate (or heimer et al. 2006b). The isotopic signal not) prior dietary reconstructions. It is of P. robustus samples showed a mixed C3/ expected that if bipedal P. robustus were

C4 signal, suggesting the consumption of consuming terrestrial foods, it should be forest resources was substantial (Lee- similar to semi-terrestrial African apes. Thorp et al. 1994; 2007; Sponheimer et Given its lack of shearing crests and al. 2006a,b). In fact most living primates broad, flat molars, it is predicted that P. heavily utilize forest foods even in dry robustus will differ from folivorous and fo- areas where these resources are limited livorous-frugivorous monkeys. Since the (Sponheimer et al. 2006a; Elton 2008). grit load of foods in savannas would be Nevertheless, P. robustus must have con- expected to exceed that found in tropical 4 Frank L’Engle Williams forests (Galbany et al. 2009), P. robustus 2001). Herries et al. (2009) suggested is predicted to differ considerably from the Swartkrans Member 1 deposits are primates from closed habitats. older – 2.1 to 1.9 Ma. The three fossils which preserve Materials and methods dental microwear include SK 6, a left hemi-mandible with a partial ascending The P. robustus sample from Swartkrans ramus from a young subadult. The left included SK 6, SK 34 and SK 47 (To- M2 is recently erupted along with P3 and bias et al. 1977) (Fig. 1). The fossils P4, and all three lack substantial attri- all derived from the Hanging Remnant tion, although microwear is noticeably of Swartkrans Member 1 (Brain 1981; present. The first mandibular molar also 1985), dated to circa 1.8 Ma (Brain shows attrition. Within the internal ra- 2004) or 1.6 Ma using biostratigraphy mus surface, a developing unerupted and

(de Ruiter 2003), corroborated by a date complete M3 crown can be observed (Fig. of 1.63 Ma using ESR on one P. robus- 1). SK 6 is the holotype of Paranthropus tus specimen, SKW 11 (Curnoe et al. crassidens (Brain 1981).

Fig. 1. Occlusal views of (a) SK 6 – a left partial mandible from a subadult showing P4 to unerupted M3, and (b) SK 47 – a nearly intact subadult basicranium, showing right P4 to M2. The approximate areas scanned on mandibular (SK 6) and maxillary (SK 47) specimens are marked by a white square with 2 a black outline on M2 of (a) and M of (b) Dietary proclivities of Paranthropus robustus 5

Also included is SK 34, which con- The parameters that justified the tains (a) right and (b) left parts, con- inclusion of SK 6, SK 34 and SK 47 in sisting of unequal hemi-mandibles of this study were (1) presence of scratch- a young adult. The cusp morphology of es consistent with extant primate ana- the molars and premolars exhibits sub- logues with known diets; (2) absence of stantial attrition but the dentine is not extreme differences in surface relief; (3) exposed, although the incisal edges and lack of preparation or casting defects; canine tips do show exposures of dentine. and (4) absence of a pockmarked surface. The dentition is not extensively worn al- All specimens were first examined under though all teeth reach the same occlusal 40× and 100× to accept or reject the sur- plane. The mandibular third molar still face before scanning. preserves some of its original occlusal morphology. The left, SK 34b, is better Dental microwear analysis preserved and subsequently molded. SK47 is a well preserved juvenile/sub- Three P. robustus specimens (SK 6, SK 34 adult basicranium including the palate and SK 47) were molded at the Transvaal and maxillary alveolus. Both right and Museum (currently the Ditsong Nation- left M2 are in situ and were only recently al Museum of Natural History), Pretoria, erupted at time of death as evidenced by South Africa using Regular Body Pres- the lack of heavy attrition on the occlu- ident Jet Plus 4605 (polyvinylsiloxine) sal facets, although microwear is clearly from Coltène-Whaledent. Regular body evident. A late juvenile/early subadult was chosen because of its high repro- age is further corroborated by the right ducibility of the original enamel surface P4 which is only one-third erupted, an (Galbany et al. 2004; 2006). The fossil unossified premaxillary suture, and an teeth were first cleaned with shellac re- unfused spheno-occipital synchondrosis. mover and isopropyl alcohol prior to the As in SK 6, the M1of SK 47 is well worn, application of molding material. Positive although SK 6 is suggested to be slightly replicas (dental casts) from the negative older in age at death than SK 47 (Brain impressions (dental molds) were pre- 1981). Like other P. robustus maxillae, SK pared using a 1:5 mix of hardener and 47 exhibits a Carabelli “furrow” on the epoxy resin (Buehler). The hardener was lingual wall of the protocone of RM1 and poured first, followed by epoxy resin into RM2 (Schwartz et al. 1998). a graduated cylinder and agitated by vig- From an examination of hundreds of orous stirring before being emptied into Plio-Pleistocene hominin fossil molars, plastic tubes and centrifuged for one Grine (1986) found only nine P. robustus minute. The resulting casting mixture appropriate for analysis, suggesting the was then poured into the dental molds vast majority exhibited postmortem or which were a priori nestled into putty cra- preparation artifacts (Grine 1986). There dles affixed beforehand with putty hard- may be other specimens with well-pre- ener (Buehler). The dental casts were served dental microwear that were pre- allowed to dry for 24 hours at room tem- viously overlooked or rejected by Grine perature before they were extracted from (1986). The new material recovered the molds. more recently (e.g., Grine 1989) was not Textural properties of the compara- available. tive taxa were obtained from Ungar et 6 Frank L’Engle Williams al. (2008) and have been featured else- consumes primarily leaves, but occasion- where (Scott et al. 2005; 2006; 2012). ally eats fruit, and at times, soil and sand The same instruments and procedures (Brotoisworo and Dirgayusa 1991). utilized to collect data for the compar- Scanning was performed using ative sample were also utilized for the a white-light confocal microscope (Sen- P. robustus sample. The comparative sofar Plμ) at 100× magnification coupled taxa included mantled howler monkeys, with an optical imaging system (Solarius Alouatta palliata (n =11), tufted capuchin Development Inc.). Scanning occurred monkeys, Cebus apella (n = 13), western on the enamel surface on facet 9 of the lowland gorillas, Gorilla gorilla gorilla (n protocone of the second maxillary mo- = 9), grey-cheeked mangabeys, Lophoce- lar for SK 47 and on the hypoconid of bus albigena (n = 15), common chimpan- the second mandibular molars for SK 6 zees, Pan troglodytes troglodytes (n = 17) and SK 34 (Fig. 1). Facet 9 is a “Phase and silvered langurs, Trachypithecus crista- II” facet which functions as a grinding tus (n = 12). surface (Kay and Hiiemae 1977; Gor- The diets of the comparative taxa don 1982; Krueger et al. 2008). Four differ considerably. Whereas A. palliata adjoining scans for the three specimens is often described as a folivore, its diet (Fig. 2) were captured from a 138 × comprises substantial amounts of fruit 102 µm viewing field derived from a to- (Estrada 1984; Chamberlain et al. 1993). tal sampled area comprising 276 × 204 Cebus apella also consumes notable quan- μm (Scott et al. 2006). Digital elevation tities of fruit as well as bromeliads, in- maps were created to depict textural sects, and often engages in extractive complexity and distinctions in enam- foraging (Jack 2011). Fruit pursuers in- el surface elevation (Fig. 3). After the clude G. gorilla which additionally eats scans were leveled in the program So- leaves, herbs, bark, pith and insects larMap Universal, scale-sensitive fractal (Doran-Sheehy et al. 2009), as well as analysis was performed to extract data L. albigena which consumes ripe, unripe from the point cloud using Toothfrax to and rotten fruit, insects, bark and hard calculate complexity (Asfc), scale of max- seeds (Lambert et al. 2004), and P. troglo- imum complexity (Smc) and anisotropy dytes which, in addition to fruit, has been (epLsar), and SFrax (Surfract.com) to es- observed eating leaves, insects and pith timate textural fill volume Tfv( ) (Scott et (Head et al. 2011). In contrast, T. cristatus al. 2006).

Fig. 2. Reconstructed enamel surface scans for P. robustus showing (a) SK 6, (b) SK 34 and (c) SK 47 Dietary proclivities of Paranthropus robustus 7

Fig. 3. Surface relief reconstructions for SK 47 provide examples of textural complexity characterizing P. robustus, cf. (a) and (b)

Microwear texture An additional indicator of enamel sur- characteristics face roughness, scale of maximum complexity (Smc), derives from the range Surface roughness is contingent on the of slope values from which Asfc is ob- scale of observation such that a surface tained (Scott et al. 2006; 2012; Ungar may appear smooth at a lower magni- et al. 2010). These two measures, scale fication but uneven at a higher reso- of maximum complexity (Smc) and com- lution. Area-scale fractal complexity plexity (Asfc), demonstrate the degree (Asfc) compares differences in the tex- to which hard and brittle food items are tural complexity of a surface from 7200 masticated. For example, hard-object μm2 to 0.02 μm2. Complexity (Asfc) is consumers such as L. albigena exhibits estimated as the steepest point slope of elevated Smc and Asfc, whereas C. apella a log-log comparison of relative length shows high values only for Asfc (Scott et area compared to scale of observation. al. 2006; 2012). 8 Frank L’Engle Williams

Anisotropy (epLsar) describes the pat- ellipses around group centroids; confirm- terning of enamel surface relief such that atory jack-knifed classification rates were a distinct orientation of microwear tex- also examined. Mahalanobis distances ture can be observed. Anisotropy (epL- (D2) and post-hoc probabilities of group sar), or the “exact proportion of Length- membership were included to address scale anisotropy of relief” (Scott et al. how well the P. robustus specimens corre- 2006) is a proxy for the amount of tough sponded to the centroid of each taxon and foods, such as leaves and stems, are con- the degree to which the fossils conformed sumed (Scott et al. 2009). to the P. robustus grouping. A cluster anal- Textural fill volume Tfv( ) is calculat- ysis was incorporated, using the means of ed from an algorithm which compares the dental microwear textures for the ex- the volume of the scanned surface us- tant taxa and including all three P. robustus ing square cuboids with different facet specimens separately, to provide a multi- lengths (10 μm and 2 μm) to estimate variate proxy of diet. the degree of surface dental microwear compared to facet curvature (Scott et al. Results 2006), and serves to separate hard-object consumers and extractive foragers such The taxa exhibit profound differences as C. apella with high values from foliv- (Table 1), including P. robustus, which orous A. palliata with much lower values shows moderate values for complexi- (Scott et al. 2009; 2012). ty (Asfc) and the highest value for scale of maximum complexity (Smc); SK 34 Statistical methods shows an extremely elevated value compared to SK 6 and SK 47. For anisotropy Median values were utilized to limit (epLsar) SK 47 exhibits a much lower val- a positive skewing of the central tendency ue than do SK 6 and SK 34. For textural (Scott et al. 2006) and were rank-trans- fill volumeTfv ( ) SK 6 and SK 47 show formed so that parametric statistics could the highest value; SK 34 stands apart be applied (Conover and Inman 1981). An from the other fossils with a lower value. F test was conducted to test the null hypothesis of equality of variance between Bivariate analyses P. troglodytes (n = 17) and P. robustus (n = 3). Since the critical f-value was larger Several pairwise comparisons of dental than the observed f values, standard be- microwear texture characteristics are sig- tween-group tests of significance could nificant. The relationship between scale not be conducted. Linear regression be- of maximum complexity (Smc) and com- tween all possible pair-wise comparisons plexity (Asfc) shown in Figure 4a is sig- of dental microwear texture characteris- nificant P( = 0.001; r = 0.359). Similarly, tics was performed, and significantly -re a linear regression of textural fill volume lated textures (P < 0.05) were plotted as (Tfv) and complexity (Asfc) shown in bivariate graphs shown with 95% confi- Figure 4b, exhibits a highly significant P dence ellipses around group centroids for value (P < 0.001; r = 0.373). Anisotro- the extant species. Discriminant Function py (epLsar) is significantly relatedP ( < Analysis provided canonical scores axes 0.001) to both scale of maximum com- which were plotted with 95% confidence plexity (Smc) and complexity (Asfc). Dietary proclivities of Paranthropus robustus 9

Table 1. Descriptive statistics for complexity (Asfc), scale of maximum complexity (Smc), anisotropy (epL- sar) and textural fill volume Tfv( ) Genus/Specimen N Asfc Smc epLsar Tfv A. palliata 11 Mean 0.360 –0.188 6.0 × 10–3 2610.909 SD 0.183 1.050 2.1 × 10–3 3225.700 C. apella 13 Mean 5.466 –0.178 4.0 × 10–3 9674.846 SD 6.304 1.101 1.9 × 10–3 4931.705 G. gorilla 9 Mean 1.597 –0.384 4.0 × 10–3 8099.714 SD 1.012 0.567 1.8 × 10–3 5702.802 L. albigena 15 Mean 1.769 0.623 4.0 × 10–3 11388.333 SD 1.740 1.064 2.0 × 10–3 3389.758 P. troglodytes 17 Mean 2.246 –0.497 3.0 × 10–3 9344.529 SD 1.523 0.520 1.0 × 10–3 5476.855 T. cristatus 12 Mean 0.734 –0.365 5.0 × 10–3 9532.250 SD 0.660 0.547 2.6 × 10–3 5687.205 P. robustus 3 Mean 2.167 1.320 3.0 × 10–3 15776.443 SD 0.958 1.744 1.0 × 10–3 12656.741 SK 6 1 1.430 0.420 3.1 × 10–3 25865.010 SK 34 1 1.820 3.330 3.2 × 10–3 1574.720 SK 47 1 3.250 0.210 1.7 × 10–3 19889.600 Note. N = number of individuals, SD = standard deviation.

Figure 4a shows fundamental distinc- C. apella and P. troglodytes with relatively tions exist between A. palliata, and to high values for complexity (Asfc). Lopho- a lesser extent T. cristatus, with relative- cebus albigena and G. gorilla exhibit mod- ly low values contrasting with those of erately elevated values for complexity.

Fig. 4. Bivariate comparison of (a) scale of maximum complexity (Smc) and complexity (Asfc) and (b) textural fill volume Tfv( ) and complexity (Asfc) are shown with 95% confidence ellipses around group centroids 10 Frank L’Engle Williams

All three P. robustus specimens show high na. Paranthropus robustus specimen SK 47 values for complexity (Asfc) and scale of is strongly positive on Canonical Scores maximum complexity (Smc). However, Axis 1 and is most closely approximated SK 34 shows the highest value for scale by one C. apella outlier. One P. troglodytes of maximum complexity (Smc) and SK 47 falls close to SK 6 and two P. troglodytes exhibits the highest value for complex- individuals approximate SK 34. Canoni- ity (Asfc). Meanwhile, SK 6 falls within cal discriminant functions standardized the 95% confidence ellipse for the group by within variances show that anisotro- centroid of L. albigena, and is approximat- py (epLsar) loads negatively on Canoni- ed by outliers from L. albigena and one P. cal Scores Axis 1 whereas complexity troglodytes (Fig. 4a). (Asfc) loads highly positively, indicating Figure 4b shows differences exist in P. robustus exhibits a combination of low textural fill volumeTfv ( ) between SK 6 anisotropy (epLsar) and high complexity and SK 47 with high values, and A. pal- (Asfc) values (Table 2). liata and SK 34 with low values. Four P. The second canonical scores axis, troglodytes individuals and G. gorilla, C. accounting for 18.3% of the variance, apella, L. albigena and T. cristatus outliers serves to contrast T. cristatus, L. albigena approximate P. robustus by exhibiting and P. robustus with negative values from both high textural fill volume Tfv( ) and P. troglodytes, G. gorilla and C. apella with high complexity (Asfc) values. The 95% positive ones (Fig. 5). On the second confidence ellipses for the extant taxa do axis, SK 6, followed by SK 47, shows not overlap with the fossils. Specimen greater negative scores whereas SK 34 SK 34 overlaps the value for one G. gorilla is much less negative and consequently and secondarily resembles P. troglodytes, more difficult to classify. The elevated C. apella and G. gorilla outliers (Fig. 4b). loadings for scale of maximum complexity (Smc) and textural fill value (Tfv) on Canonical scores axes canonical discriminant functions, standardized by within variances, explain the Discriminant function analysis was uti- negative projection of T. cristatus, L. al- lized to ascertain the degree to which individuals correspond to their group, the distribution of groups and which dental microwear textures separated individuals across canonical scores axes. On Canonical Scores Axis 1, representing 71.5% of the variance, A. palliata and T. cristatus are separated from P. robustus, L. albigena and C. apella (Fig. 5). Specimens SK 34 and SK 6 resemble each other in positive values for Canonical Scores Axis 1, although SK 34 falls on the margin of the 95% confidence ellipse around the group centroid for C. apella, whereas SK Fig. 5. Canonical Scores Axis 1 (71.5%) and Axis 2 6 falls close to the 95% confidence ellipse (18.3%) are shown with 95% confidence ellip- around the group centroid for L. albige- ses around group centroids Dietary proclivities of Paranthropus robustus 11

Table 2. Canonical discriminant functions standardized by within-variances for Canonical Scores axes Textural property CS Axis 1 CS Axis 2 Complexity (Asfc) 0.928 0.633 Scale of maximum complexity (Smc) 0.758 –0.643 Anisotropy (epLsar) –0.248 0.359 Textural fill volume Tfv( ) 0.273 –0.555 Note. CS = canonical scores. bigena and P. robustus on Canonical Scores posterior probability of SK 34 is elevat- Axis 2 (Table 2). ed in comparison to that for SK 6. Paran- thropus robustus specimen SK 47 exhibits Jack-knifed classification rates the lowest D2 value (1.8) and the highest posterior probability of group member- Jack-knifed classification rates are high- ship (0.84) (Table 3). est for A. palliata (71%) and lowest for G. gorilla (21%) whereas the classification Cluster analysis rate for P. robustus is 67%. One P. robustus specimen, SK 6, is misclassified as L. A cluster analysis shows that SK 34 is albigena. One L. albigena and one C. apella distinct from the other taxa, followed are misclassified asP. robustus. by SK 47 and A. palliata (Fig. 6). The remaining extant taxa, particularly L. albige- Mahalanobis distances na, cluster with SK 6 but by a relatively long branch length. Taxa deriving from The Mahalanobis distances (D2) for P. ro - tropical forests, with the exception of A. bustus individuals to the group centroid palliata, exhibit relatively short branch are relatively small (Table 3). Howev- lengths, particularly those separating C. er, SK 6 is slightly more similar to the apella, P. troglodytes and G. gorilla (Fig. 6). group centroid for L. albigena (2.1) than the corresponding value for the P. robust- Discussion and conclusion us group centroid (2.4). The D2 value for SK 34 to the P. robustus category is much Scott et al. (2005) suggest that A. afri- higher (5.3) than those characterizing canus and P. robustus differ from A. pallia- the other fossil specimens. However, the ta which has a diet primarily of leaves,

Table 3. Mahalanobis distances of P. robustus to the group centroids of the comparative taxa (with post-hoc probabilities of group membership) Taxon SK 6 SK 34 SK 47 Average D2 A. palliata 18 (0.00) 18.5 (0.00) 28.4 (0.00) 21.633 C. apella 5.8 (0.07) 7.1 (0.22) 8.4 (0.03) 7.1 G. gorilla 8.0 (0.02) 10.1 (0.05) 13.2 (0.00) 10.433 L. albigena 2.1 (0.46) 7.9 (0.15) 5.7 (0.12) 5.233 P. robustus 2.4 (0.39) 5.3 (0.54) 1.8 (0.84) 3.166 P. troglodytes 6.9 (0.04) 11.2 (0.03) 10.5 (0.01) 9.533 T. cristatus 8.4 (0.02) 17.6 (0.00) 17.2 (0.00) 14.4 Note. D2= Mahalanobis distance. 12 Frank L’Engle Williams

adults, SK 6 and SK 47, differ from adult specimen SK 34 in scale of maximum complexity (Smc) and textural fill volume (Tfv) (Table 1; Fig. 7). The Sr/Ca ratio of juvenile SK 54 was substantial- ly higher than adults from Swartkrans Member 1 and more like that of Papio robinsoni than the fossil carnivore taxa. These differences may suggest P. robustus juveniles consumed USOs which exhibit elevated Sr/Ca ratios (Sillen 1992). Corroborating these observa- Fig. 6. A cluster analysis shows SK 34 is distinct, tions, juvenile P. robustus exhibits sub- followed by SK 47 and A. palliata, while SK 6 stantial dentine exposure suggesting an groups with the remaining extant taxa albeit abrasive diet in nonadults, early wean- with a relatively long branch length ing, or both (Aiello et al. 1991). The scratch marks on the Swartkrans bone stems and fruit, and Cebus which con- tools from the Lower Bank of Member sumes greater amounts of fruit and 1, which is believed to be contempo- exhibits considerable durophagy and raneous with the Hanging Remnant extractive foraging. Higher values for remains, may have resulted from dig- anisotropy (epLsar) in A. africanus and ging USOs (Brain 1985; 2004). Perhaps complexity (Asfc) in P. robustus are in- subadults were less able to effectively terpreted as evidence of different fall- utilize the tools or techniques to re- back foods. Scott et al. (2005) examine move the extraneous grit on terrestrial nine specimens attributed to P. robustus resources or USOs in contrast to adults, including eight from Swartkrans. The accounting for the elevated textural fill means and standard deviations from volume (Tfv) in SK 6 and SK 47. Juve- Scott et al. (2005) are reported in Ung- nile and subadult chimpanzees are not ar et al. (2012), and these are compared as well versed in utilizing termite sticks to the results obtained here (Fig. 7). and in nut-cracking activities as adults Specimen SK 47 is similar to the tex- (McGrew 1992). A subadult sample of tural properties recorded in Ungar et al. Papio exhibits a significantly greater de- (2012) with the exception of textural gree of pitting than do adults, perhaps fill volume Tfv( ) (Fig. 7). The values for also reflecting differences in diet or SK 6 resemble those from Ungar et al. food preparation (Nystrom et al. 2004). (2012) for scale of maximum complexity Furthermore, Neandertal subadults are (Smc) and anisotropy (epLsar). However, noted to have a significantly greater SK 34 falls outside the range of values density of striations compared to adults reported by Ungar et al. (2012), increas- (Pinilla Pérez et al. 2011), although ing the variation in textural properties young and older adult Amerindians associated with P. robustus (Fig. 7). were not significantly different in - pat Some of the variation observed could terns of dental microwear suggesting be attributable to life history differenc- a leveling of age differences in diet after es, and may explain why P. robustus sub- maturation (Schmidt 2010). However, Dietary proclivities of Paranthropus robustus 13

Fig. 7. A comparison of the 95% confidence intervals for the nine P. robustus specimens reported in Ungar et al. (2012) and the three P. robustus fossils examined in this study

given the variation in P. robustus (Fig. 7), Dietary reconstruction idiosyncratic factors related to seasonal of P. robustus diets typical of temperate latitude fauna, and the availability of fallback foods Direct evidence of dietary consump- may also account for the differences tion in Paranthropus has been explored within these specimens. by a number of researchers (Robinson 14 Frank L’Engle Williams

1954; Kay 1985; Grine 1986; Scott et tural fill volume (Tfv). Elevated textural al. 2005; Constantino et al. 2010). Kay fill volume (Tfv) may derive from con- (1985) suggests that the exceptionally suming hard and brittle foods (Merceron thick enamel of P. robustus (and A. afri- et al. 2009) or is possibly the result of canus) could have been an adaptation to the consumption of soil and sand such as the consumption of at least three possi- in T. cristatus (Brotoisworo and Dirgayusa ble foods, such as seeds, metapodials of 1991), or when grit inadvertently adheres ungulates and the underground parts of to meat (Romero et al. 2012). Grit may plants. However, thick enamel cannot be be the primary factor in the production used as evidence for terrestrial foraging of dental microwear (Sanson et al. 2007; since it has also evolved in arboreal pri- Lucas et al. 2013). Experimental studies mates that specialize on hard foods such have shown that microwear forms when as Cebus and Lophocebus. Rather, it ap- siliceous grit comes into contact with the pears to be a consequence of consuming teeth (Romero et al., 2012). In addition, a great variety of different foods, some of Galbany et al. (2014) and Romero et al. which are hard and brittle (Kay 1985). (2012) proposed that the production of Paranthropus robustus has been de- enamel microwear is dependent on par- scribed as exhibiting low anisotropy with ticle size. For example, large particles are respect to A. africanus (Scott et al. 2005; more likely to fracture the enamel sur- Ungar et al. 2010) and early Homo (Un- face, whereas small particles produce in- gar and Scott 2009). Highly folivorous dentations. The terrestrial foraging of P. primates such as A. palliata and T. crista- robustus in mixed C4 habitats would likely tus exhibited elevated anisotropy (epLsar) deliver a heavier grit load than observed (Scott et al. 2006). This may indicate in tropical forests. This would be particu- a lack of leaves in the diet of P. robust- larly evident in relatively arid habitats us or suggest that leaves were not a pri- where a layer of grit covers food items mary food source. The low crests on the (Sanson et al. 2007; Galbany et al. 2009; molars also point to a diet low in fibrous Dumont et al. 2011). Grit adheres to leaves (Kay 1985). hypogeous organs (Daegling and Grine Similar to L. albigena, P. robustus exhib- 1999) and can be inadvertently ingested its elevated values for scale of maximum when bulbs or corms have outer skins complexity (Smc) suggesting hard and that are not easily removed or cleaned brittle foods may have been consumed. with the mouth or hands. The consumption of hard and brittle Underground storage organs could foods including seeds and bark neces- have been a reliable source of energy-rich sitates thick enamel to prevent enamel carbohydrates for Australopithecus and chipping, such as is found in L. albigena early Homo (Hatley and Kappelman 1980; (Lambert et al. 2004) and C. apella (Jack Wrangham et al. 1999; Conklin-Brittain 2011). Enamel chipping must have been et al. 2002; Laden and Wrangham 2005). generated by an extreme bite force in P. ro - Some have suggested the possibility that bustus (Constantino et al. 2010), also not- USOs were preferred foods rather than ed for its thick enamel (Robinson 1954; fallback resources explaining the simi- Wallace 1973; Grine 1981; Schwartz et larity in the postcanine dentition of pigs, al. 1998). Paranthropus robustus resembles bears, and australopiths (Hatley and Kap- C. apella and L. albigena in its elevated tex- pelman 1980). Savanna environments Dietary proclivities of Paranthropus robustus 15 yield a more abundant and diverse USO extremely hard and brittle shells, insects distribution than is found in rain forests. and fruit found on ground-level (Lambert Furthermore, 65% of USOs in savannas et al. 2004). Paranthropus robustus shows can be eaten raw compared to only 9.1% a pattern of textural characteristics that from rain forests (Laden and Wrangham resembles in part that of L. albigena and to 2005). Judging from the relatively large a lesser extent, C. apella. In this way, the palate in P. robustus compared to the thick enamel and enamel textural prop- great apes, there was a capacious cavity erties of P. robustus could be reflecting an to allow a thorough processing of starchy adaptation to the mechanical properties foods with salivary amylase which en- of foods, as in L. albigena and C. apella. hances digestion (Conklin-Brittain et al. Paranthropus robustus is distinct from ar- 2002). These resources could have been boreal primates that consume substan- heavily utilized during seasonal dietary tial quantities of leaves such as T. cristatus deficits or during drying episodes typical and A. palliata corroborating the lack of of early Pleistocene southern Africa. folivory inferred from the broad flat mo- It is worth noting that P. troglodytes, lars. The elevated values for complexity C. apella and L. albigena all consume sub- (Asfc) and textural fill volume Tfv( ) in P. stantial quantities of insects and all ex- robustus may derive from the consump- hibit elevated complexity (Asfc) values. tion of hard seeds and/or insects; howev- The consumption of insect cuticle may er, given its isotopic signal, grit particles explain evidence of hard-object foraging associated with terrestrial foraging and in the Muridae, small primates and some the exploitation of USOs derived from C4 bats (Strait 1993; Rodrigues et al. 2009). plants may better account for these den- Although the external shell of insects tal microwear texture properties. lack mineral supports, the cuticle can be extremely stiff (Dirks and Taylor 2012; Disclosure statement Vincent and Wegst 2004). The somewhat elevated value for complexity (Asfc) in P. The Paranthropus robustus fossils utilized robustus could originate from terrestrial in this study have not been reported grit from USOs and meat as well as from upon by the author previously and there hard seeds and/or insects, or a mix of are no conflicts of interest to declare. these resources (Backwell and d’Errico 2001; Peters and Vogel 2005). Acknowledgements The isotopic values of P. robustus suggest the consumption of some C4 grass- This research was funded by a Research land resources, either in the form of Team Grant and a Research Program meat from C4 grazers or C4 plant roots Enhancement Grant from the Vice Pres-

(Lee-Thorp et al. 1994); C4 grass blades ident for Research at Georgia State Uni- would have resulted in elevated values of versity. The author would like to thank anisotropy (epLsar) which is not the case. Francis Thackerey and Stefanie Potze at Ingestion of terrestrial foods should re- the Ditsong National Museum of Natu- sult in greater textural complexity (Asfc), ral History, formerly the Transvaal Mu- scale of maximum complexity (Smc) and seum, Pretoria, South Africa for provid- textural fill volumeTfv ( ) like that seen ing access to the fossil material. Peter on L. albigena which feeds on seeds with Ungar generously granted permission to 16 Frank L’Engle Williams utilize the confocal microscope and an- West Java, Indonesia. In: A Ehara, T Ki- alytical software at the Department of mura, O Takenaka and M Iwamonto, ed- Anthropology, University of Arkansas. itors. Primatology Today. Amsterdam: El- Jessica Scott kindly assisted with data sevier Science. 115–18. Chamberlain J, Nelson G, Milton K. 1993. capture and processing. Brian Carter pro- Fatty acid profiles of major food sources of vided the photographs in Figure 1, and howler monkeys (Alouatta palliata) in the Monique McGee offered assistance with neotropics. Experientia 49:820–24. Figures 4, 5 and 7. Conklin-Brittain NL, Wrangham RW, Smith CC. 2002. A two-stage model of increased Corresponding author dietary quality in early hominid evolution: the role of fiber. In: PS Ungar and MF Tea- Frank L’Engle Williams ford, editors. Human Diet: Its Origin and Department of Anthropology, College of Evolution. London: Bergin and Garvey. 61–76. Arts and Sciences, Georgia State Univer- Conover WJ, Inman RL. 1981. Rank trans- sity, P.O. Box 3998 Atlanta, GA 30303 formation as a bridge between parametric e-mail: [email protected] and nonparametric statistics. Am Statisti- cian 35:124–29. References Constantino PJ, Lee JJW, Chai H, Zipfel B, Ziscovici C, Lawon BR, Lucas PW. 2010. Aiello LC, Montgomery C, Dean C. 1991. The Tooth chipping can reveal the diet and natural history of deciduous tooth attri- bite forces of fossil hominins. Biol Lett tion in hominoids. J Hum Evol 21:397– 6:826–29. 412. Curnoe D, Grun G, Taylor L, Thackeray JF. Avery DM. 2001. The Plio-Pleistocene veg- 2001. Direct ESR dating of a Pliocene etation and climate of Sterkfontein and hominin from Swartkrans. J Hum Evol Swartkrans, South Africa, based on micro- 40:379–91. mammals. J Hum Evol 41:113–32. Daegling DJ, Grine FE. 1999. Terrestrial for- Backwell LR, d’Errico F. 2001. Evidence of ter- aging and dental microwear in Papio ursi- mite foraging by Swartkrans early homi- nus. Primates 40:559–72. nids. Proc Natl Acad Sci USA 98:1358–63. Delson E. 1984. Cercopithecid biochronology Brain CK. 1981. The Hunter or the Hunted? of the African Plio-Pleistocene: correla- An Introduction to African Cave Taphono- tions among eastern and southern hom- my. Chicago: University of Chicago Press. inid-bearing localities. Cour Forsch-Inst Brain CK. 1985. Cultural and taxonomic Senckenberg 69:199–218. comparisons of hominids from Sterkfon- de Ruiter DJ. 2003. Revised faunal lists for tein and Swartkrans. In: E Delson, editor. Members 1–3 of Swartkrans, South Africa. Ancestors: The Hard Evidence. New York: Ann Transvaal Mus 40:29–41. Alan R. Liss. 72–78. de Ruiter DJ, Sponheimer M, Lee-Thorp JA. Brain CK. 2004. Structure and stratigraphy of 2008. Indications of habitat association of the Swartkrans Cave in light of the new Australopithecus robustus in the Bloubank Val- excavations. In: CK Brain, editor. Swart- ley, South Africa. J Hum Evol 55:1015–20. krans: A Cave’s Chronicle of Early Man, Dirks JH, Taylor D. 2012. Fracture tough- 2nd Edition. Pretoria: Transvaal Museum ness of locust cuticle. J Experimental Biol Monograph, No. 8. 7–22. 215:1502–08. Brotoisworo E, Dirgayusa IWA. 1991. Rang- Doran-Sheehy D, Mongo P, Lodwick J, Conk- ing and feeding behavior of Presbytis cris- lin-Brittain NL. 2009. Male and female tata in the Pangandaran nature reserve, western gorilla diet: preferred foods, use of Dietary proclivities of Paranthropus robustus 17

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