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Journal of Human Evolution 62 (2012) 165e168

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Journal of Human Evolution

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Microwear, mechanics and the feeding adaptations of Australopithecus africanus

David S. Strait a,*, Gerhard W. Weber b, Paul Constantino c, Peter W. Lucas d, Brian G. Richmond e,f,Mark A. Spencer g, Paul C. Dechowh, Callum F. Ross i, Ian R. Grosse j, Barth W. Wright k,Bernard A. Wood e,f, Qian Wang l, Craig Byronm, Dennis E. Slice n

aDepartment of Anthropology, University at Albany, 1400 Washington Avenue, Albany, NY 12222, USAbDepartment of Anthropology, University of Vienna, Althanstrasse 14, A-1090 Vienna, AustriacDepartment of Biological Sciences, Marshall University, 1 John Marshall Drive, Huntington, WV 25755, USAdDepartment of Bioclinical Sciences, Faculty of Dentistry, Kuwait University, P.O. Box 29423, Safat 11310, KuwaiteCenter for the Advanced Study of Hominid Paleobiology, Department of Anthropology, The George Washington University, 2110 G St. NW, Washington D. C. 20052, USAfHuman Origins Program, National Museum of Natural History, Smithsonian Institution, Washington D. C. 20560, USAg School of Human Evolution and Social Change, Institute of Human Origins, Arizona State University, Tempe, AZ 85287-4104, United StateshDepartment of Biomedical Sciences, Texas A&M Health Science Center, Baylor College of Dentistry, 3302 Gaston Avenue, Dallas, TX 75246, USAiDepartment of Organismal Biology & Anatomy, University of Chicago, 1027 East 57th Street, Chicago, IL 60637, USAjDepartment of Mechanical & Industrial Engineering, University of Massachusetts, 160 Governor’s Drive, Amherst, MA 01003-2210, USAkDepartment of Anatomy, Kansas City University of Medicine and Biosciences, 1750 Independence Avenue, Kansas City, MO 64106-1453, USAlDivision of Basic Medical Sciences, Mercer University School of Medicine, 1550 College Street, Macon, GA 31207, USAmDepartment of Biology, Mercer University, 1400 Coleman Avenue, Macon, GA 31207, USAn School of Computational Science & Department of Biological Science, Florida State University, Dirac Science Library, Tallahassee, FL 32306-4120, USA

a r t i c l e i n f o

Article history:Received 3 July 2011Accepted 12 October 2011

Keywords:AustralopithecusFeeding mechanicsDietMicrowearFinite element analysis

* Corresponding author.E-mail address: dstrait@albany.edu (D.S. Strait).

0047-2484/$ e see front matter � 2011 Elsevier Ltd.doi:10.1016/j.jhevol.2011.10.006

a b s t r a c t

Recent studies of dental microwear and craniofacial mechanics have yielded contradictory interpreta-tions regarding the feeding ecology and adaptations of Australopithecus africanus. As part of this debate,the methods used in the mechanical studies have been criticized. In particular, it has been claimed thatfinite element analysis has been poorly applied to this research question. This paper responds to some ofthese mechanical criticisms, highlights limitations of dental microwear analysis, and identifies avenuesof future research.

� 2011 Elsevier Ltd. All rights reserved.

Introduction

Grine et al. (2010) recently contributed a critique of ourmethodsand interpretations concerning the feeding mechanics and dietaryecology of Australopithecus africanus (Strait et al., 2009). Wedemonstrated that feeding mechanics in this species are consistentwith Rak’s (1983) biomechanical hypothesis explaining the evolu-tion of certain derived australopith facial features, and wehypothesized that such traits may be evolutionary adaptations foringesting large, hard objects. Here, we respond to some of thecriticisms of Grine et al. (2010) and suggest a way to move thedebate forward.

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Dental microwear

We hypothesized that hard foods were selectively importantcomponents of the diet of A. africanus that could have been eitherpreferred or fallback foods, whereas Grine et al. (2010) state thatthere is no microwear-based evidence of meaningful hard objectfeeding in this species, and that fallback foods in this species weremore likely to have been tough than hard (Scott et al., 2005).However, many of the same authors (Ungar et al., 2010) recentlyconcluded that A. africanus consumed hard objects at a frequencysignificantly greater than that of Australopithecus afarensis but lessthan that of Paranthropus robustus, and that such objects repre-sented an increasing component of the A. africanus diet. Thisinterpretation is consistent with our adaptive hypothesis.

Grine et al. (2010) also assert that the comparative basis of dentalmicrowear research is so well established that it is unreasonable tosuggest (as we have) that interpretations of microwear can be

Table 1Ratios of maximum shear strain between working - side (W), balancing side (B) and midline cranial regions.

Ratio Value observed in macaqueFEA from Strait et al. (2005)

Experiment fromHylander et al. (1991)

Experimentalmean (s.d.)

Experimentaldispersiona

Dorsal interorbital/W Dorsal orbital 0.8 5A 1.7 (0.2) 1.3e2.16 2.3 (0.5) 1.3e2.3

Dorsal interorbital/B Dorsal orbital 0.9 5A 1.8 (0.2) 1.4e2.26 1.8 (0.3) 1.2e2.4

Dorsal interorbital/W Mid-zygomatic 6.8 2A 5.0 (0.9) 3.2e6.82B 6.8 (0.9) 5.0e8.65B 2.2 (0.4) 1.4e3.0

Dorsal interorbital/B Mid-zygomatic 2.6 2A 2.7 (0.8) 1.1e4.3W Infraorbital/Dorsal interorbital 4.9 5C 2.6 (0.2) 2.2e3.0B Infraorbital/Dorsal interorbital 1.9 5C 1.4 (0.3) 0.8e2.0W Infraorbital/W Dorsal orbital 3.7 C 4.0 (1.1) 1.8e6.2B Infraorbital/B Dorsal orbital 1.7 C 2.5 (0.3) 1.9e3.1

a Defined by the range equal to the mean � two standard deviations.

D.S. Strait et al. / Journal of Human Evolution 62 (2012) 165e168166

ambiguous. Yet, in the data presented by Ungar et al. (2010), Pongoexhibits less absolute variation in texture complexity thanPandespitethe presence of very hard objects in the diet of the former (e.g., Vogelet al., 2008).Moreover, Lophocebus andCebusapellahavebeenused inpriormicrowearanalyses asexamplesofhardobject feedingprimates(e.g., Scott et al., 2005), but Lophocebus and Gorilla appear to overlapextensively with each other with respect to complexity and anisot-ropy, as do C. apella and Papio cynocephalus. Neither Gorilla norP. cynocephalus are thought to be hard object feeders, so it is unclearwhat precisely these data are revealing about diet.

Grine et al. (2010) also indicate that existing experimentalevidence (e.g., Teaford andOyen,1989) falsifies our suggestion (Straitet al., 2009) that large, hard objects might not produce microwear.Yet, those experiments involvedmasticatingmonkey chow, which isnot a hard food, being orders of magnitude less stiff than true hardfoods (Lucas, 2004; Williams et al., 2005). Moreover, becausemonkey chow is a composite of many small particles, themicroweargenerated bymasticating it is consistentwith our prediction that it isprimarily small objects that create surface yielding on enamel.

Lastly, the premise of Grine et al’s. (2010) argument is that theabsence of a hard object microwear signal falsifies a hypothesis thathard foods were a selective agent driving evolutionary adaptationin A. africanus. Yet, Ungar et al. (2010) state that because microwearis ephemeral and only preserves information about foods eaten justbefore death, it cannot falsify the possibility of rare hard objectfeeding. Insofar as fallback foods may have been consumed rarely,microwear cannot falsify a hypothesis that hard items were selec-tively important fallback foods.

The points described above limit the manner in which one caninterpret the premolar microwear data presented by Grine et al.(2010). Those data falsify our hypothesis that functional differ-ences in how the premolars and molars were being used mightmanifest themselves in microwear, but they do not falsify ourhypothesis that some derived facial features in A. africanus areadaptations for ingesting large hard foods.

Table 2Maximum shear strain recorded at the working side anterior and posterior zygo-matic arch locations, in microstrain.

Source Mean max. shearstrain � 2 s.d.at the anterior

zyg. arch

Mean max. shearstrain � 2 s.d.at the posterior

zyg. arch

Mean ratio of max.shear strain � 2 s.d.(anterior/posterior)

FEAa 1106 430 2.6Macaque 2b 964 � 398 316 � 104 3.1 � 0.34Macaque 5b 1143 � 262 354 � 56 3.2 � 0.54Macaque 7b 439 � 256 357 � 176 1.2 � 0.62Macaque 9b 628 � 154 273 � 46 2.3 � 0.44

a Strait et al. (2005).b Hylander and Johnson (1997 Table 2), apple with skin.

Enamel chipping

Grine et al. (2010) interpret the relative frequencyof enamel chipson premolars versus molars as being incompatible with ourhypothesis that premolarswereused to ingest large, hardobjects, buttheir chip data merely falsify the microwear-based inference (Scottet al., 2005) that A. africanus did not consume hard foods on itsmolars. Moreover, a recent analysis of enamel chip mechanicsdemonstrates that A. africanus and other australopiths generatedhigh bite forces on their teeth (Constantino et al., 2010), a result thatis compatiblewithouradaptivehypothesis. Finally, Grineet al. (2010)observe enamel chips on 10.8% of all complete postcanine crowns in

A. africanus, whereas Constantino et al. (2010) observed chips onfewer than1%of teeth in several primate species, includingsome thatare seed-predators. Although more work is needed to ensure thatchips are being recorded in a consistent fashion, we predict thatfuture studieswill establish that chip frequency ishigh inA. africanus.Grine et al. (2010) concede that chips are caused by hard foods.

Validation

Grine et al. (2010) claim that our model is unrealistic regardingratios of maximum shear strain magnitudes between differentcranial regions. However, our model is broadly realistic except thatstrain magnitudes are too low in one area, the dorsal interorbitalregion (Table 1). They also assert that our model is unrealisticregarding the orientation of maximum principal strain and theanteroposterior gradient of maximum shear strain in the zygomaticarch. In fact, our model is realistic in both respects (Table 2; Figures.1 and 2), although a computational error (since corrected; Rosset al., 2011) led us to report (Strait et al., 2005) that orientationsin the arch were unrealistic.

Modeling assumptions

Grine et al. (2010) question our modeling assumptions.However, contra their assertions, a) modeling the periodontalligament does not profoundly affect cranial strain away from thealveolus (Wood et al., 2011), b) craniofacial sutures do notprofoundly affect strains across the face (e.g., Wang et al., 2010), c)altering material properties in our models does not change our keyresults (Strait et al., 2009; 2010; see also; Strait et al., 2005), d) theteeth used in our A. africanus model should have no substantiveeffect on our results because their spatial relationships are con-strained by the alveoli preserved in Sts 5, and e) our results arerobust to variation in muscle forces, as revealed by three sets ofmodeling experiments (Strait et al., 2009; 2010).

Figure 1. Vector map illustrating the orientation of maximum principal strain in the Macaca fascicularis finite element model at the zygomatic arch. ‘Warm’ colors indicate highstrain magnitudes and ‘cool’ colors indicate low strain magnitudes. The gray insert depicts the portion of the model that is highlighted. The arch exhibits a gradient that matchesin vivo data in which orientation changes from being anterorsuperiorly directed to posterosuperiorly directed as one moves posteriorly on the arch.

D.S. Strait et al. / Journal of Human Evolution 62 (2012) 165e168 167

Moving forward

None of the points made by Grine et al. (2010) undermine theconclusions of Strait et al. (2009) regarding feeding mechanics andadaptations in A. africanus. The first step in testing this hypothesis is

Figure 2. Maximum shear strain in the zygomatic arch of the Macaca fascicularis finite elemthe anterior, middle and posterior zygomatic arch locations that correspond to strain gage siand lowest posteriorly, as in in vivo data (Hylander and Johnson, 1997).

to collect comprehensive information about enamel chip size andfrequency in A. africanus, other hominins and primates.

Researchers should also seek to elucidate the fundamentalmechanical principles governing microwear formation. Recentmechanical studies (e.g., Lucas et al., 2008; Lawn and Lee, 2009)

ent model. Black circles indicate the position of nodes representing (from left to right)tes in Hylander and Johnson (1997). Note how strain magnitudes are highest anteriorly

D.S. Strait et al. / Journal of Human Evolution 62 (2012) 165e168168

suggest that it is not food tissues per se that produce microwear butrather very small, hard particles (including grit and plant-generatedsilicates) that may be introduced into the oral cavity as the tissuesare ingested. Such particles create microwear because the contactbetween the particle and the tooth surface is so small that evenmodest loads generate high stresses, thereby inducing surfaceyielding explained by the deformation transition threshold (Lucaset al., 2008). Yet, the precise manner in which jaw kinematics,occlusal relief, food material properties and particle size and hard-ness interact to create microwear remains largely unexplored.

Finally, we note that there need not necessarily be a precisecorrespondence between dietary behavior and dietary adaptationin all populations of a given taxon (e.g., Mihlbachler et al., 2011),and the methods useful for examining one phenomenon may notbe equally useful for exploring the other. This topic warrantsfurther consideration.

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