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Comparative forefoot trabecular bone architecture in extant hominids

Nicole L. Griffin a,*, Kristiaan D’Août b,c, Timothy M. Ryan d, Brian G. Richmond e,f,Richard A. Ketchamg, Andrei Postnov h,i

aDepartment of Evolutionary Anthropology, Duke University, P.O. Box 90383 Science Drive Durham, NC, USAbDepartment of Biology, University of Antwerp, Antwerp, BelgiumcCentre for Research and Conservation, Royal Zoological Society of Antwerp, Antwerp, BelgiumdDepartment of Anthropology, Pennsylvania State University, Pennsylvania, USAeCenter for the Advanced Study of Hominid Paleobiology, The George Washington University, Washington, DC, USAfHuman Origins Program, Smithsonian Institution, Washington, USAgDepartment of Geological Sciences, University of Texas at Austin, Austin, TX, USAhDepartment of Biomedical Sciences, University of Antwerp, Antwerp, Belgiumi Lebedev Physical Institute, Moscow, Russia

a r t i c l e i n f o

Article history:Received 22 February 2010Accepted 3 June 2010

Keywords:AnisotropyBone volume fractionHalluxMetatarsalProximal phalanx

a b s t r a c t

The appearance of a forefoot push-off mechanism in the hominin lineage has been difficult to identify,partially because researchers disagree over the use of the external skeletal morphology to differentiatemetatarsophalangeal joint functional differences in extant great apes and humans. In this study, weapproach the problem by quantifying properties of internal bone architecture that may reflect differentloading patterns in metatarsophalangeal joints in humans and great apes. High-resolution x-raycomputed tomography data were collected for first and second metatarsal heads of Homo sapiens(n ¼ 26), Pan paniscus (n ¼ 17), Pan troglodytes (n ¼ 19), Gorilla gorilla (n ¼ 16), and Pongo pygmaeus(n ¼ 20). Trabecular bone fabric structure was analyzed in three regions of each metatarsal head. Whilebone volume fraction did not significantly differentiate human and great ape trabecular bone structure,human metatarsal heads generally show significantly more anisotropic trabecular bone architectures,especially in the dorsal regions compared to the corresponding areas of the great ape metatarsal heads.The differences in anisotropy between humans and great apes support the hypothesis that trabeculararchitecture in the dorsal regions of the human metatarsals are indicative of a forefoot habitually used forpropulsion during gait. This study provides a potential route for predicting forefoot function and gait infossil hominins from metatarsal head trabecular bone architecture.

� 2010 Elsevier Ltd. All rights reserved.

Introduction

Although all extant hominoids are capable of walking bipedally, itis well accepted that only modern humans dorsiflex their meta-tarsophalangeal joints to form a stiff propulsive lever during theterminal stance phase (Elftman and Manter, 1935; Morton, 1964;Robinson, 1972; Susman, 1983; Vereecke et al., 2003; Griffin et al.,in press). In the field of paleoanthropology, the question of whena modern human-like metatarsi-fulcrimating forefoot appeared inthe fossil record has inspired a longstanding debate (e.g., Latimer,1991; Stern and Susman, 1991; Stern, 2000; Bennett et al., 2009).

This lack of consensus has mainly centered on the oldest, mostcomplete set of metatarsophalangeal foot bones, A.L. 333-15 whichhas been attributed to Australopithecus afarensis (Latimer et al., 1982).Au. afarensismetatarsals and pedal phalanges have been described asshowing a mosaic of derived and primitive external characteristicsthat have suggested to some researchers that Au. afarensis forefootfunction was not completely modern human-like, but adapted foramixed locomotor repertoire (Stern and Susman,1983; Susmanet al.,1984). Other researchers argue thatprimitive traits have little value inmaking inferences about function, and these researchers advocatea modern human-like forefoot function in Au. afarensis (Latimer andLovejoy, 1990; Latimer, 1991). The goal of the current study is to testthe potential of an alternative method, the study of trabecular bone,and to resolve current debates surrounding early hominin forefootfunction.

Several in vivo studies have shown that trabecular struts andplates respond to the direction and magnitude of local loading by

Abbreviations: MTPJ, metatarsophalangeal joint; MT, metatarsal; BV/TV, bonevolume fraction; DA, degree of anisotropy; VOI, volume of interest; HRXCT, High-Resolution X-ray Computed Tomography Facility.* Corresponding author.

E-mail address: [email protected] (N.L. Griffin).

Contents lists available at ScienceDirect

Journal of Human Evolution

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0047-2484/$ e see front matter � 2010 Elsevier Ltd. All rights reserved.doi:10.1016/j.jhevol.2010.06.006

Journal of Human Evolution 59 (2010) 202e213


aligning themselves in the direction of stress and increasing indensity (e.g., Lanyon, 1974; Goldstein et al., 1991; Pontzer et al.,2006; van der Meulen et al., 2006) and therefore offer a newapproach to test hypotheses that have long remained unresolvedabout joint function in fossils. In addition, high-resolution X-raycomputed tomography has allowed researchers to show significantdifferences in trabecular bone properties between primate loco-motor categories (Fajardo and Müller, 2001; MacLatchy and Müller,2002; Ryan and Ketcham, 2002a,b, 2005). However, it must benoted that some studies have provided contradictory evidencesuggesting that trabecular bone is not always a reliable indicator ofmechanical demand, and properties of trabecular bone do notalways clearly distinguish locomotor categories (e.g., Fajardo et al.,2007; Carlson et al., 2008; Ryan et al., 2010).

Relevant to foot function, Maga et al. (2006) investigated therelationship between the trabecular architecture of the calcaneusand locomotor regime in extant hominids. Though the analysis waspreliminary as a result of small sample size, the authors found thatmodern human calcanei show greater values of anisotropy (i.e., thestrength of orientation in one or more directions) than those of thegreat apes. This supports the hypothesis that taxa with morediverse locomotor repertoires (e.g., a mix of climbing and quad-rupedalism) exhibit a less stereotypical pattern of trabecular fabricstructure in the posterior region of the calcaneus. Therefore,studying the relationship between trabecular architecture of thefoot and locomotor type has shown promise as an indicator ofdifferences in positional behavior in living and extinct hominids.

The current study focuses on the trabecular architectural prop-erties of the first and secondmetatarsal heads. The two properties ofprimary interest are trabecular bone volume fraction (i.e., bonevolume/total volumeor BV/TV) anddegree of anisotropy (DA). BV/TVhas been found to be correlated with Young’s modulus, a measure ofbone stiffness (Hodgskinson and Currey, 1990; Kabel et al., 1999;Ulrich et al., 1999; Ding et al., 2002) and DA indicates the degree towhich bone is aligned in a preferred orientation or orientations (i.e.,trabeculae adapted for stereotypical loading along one or more axeswill show greater DA values than trabeculae adapted for multi-directional loading) (Ryan and Ketcham, 2002a,b).

Specific predictions about trabecular bone differences in theheads of modern human and great ape metatarsals can be based onexisting studies of modern human forefoot bone properties and thequantified in vivo functional differences of the forefoot in modernhumans and Pan paniscus (bonobos). Each metatarsal head repre-sents the male mating joint surface of a metatarsophalangeal joint(MTPJ) which becomes part of the weight-bearing fulcrum of theforefoot in modern humans at push-off during the stance phase(Hicks, 1954; Bojsen-Møller and Lamoreux, 1979; Erdemir et al.,2004; Griffin, 2009). Push-off occurs after the body weight istransferred to the anterior part of the foot and each phalanx movesonto the dorsum of its respective metatarsal head. As noted for theMTPJ 1, elevated joint compression occurs then (Hetherington et al.,1989; Muehleman et al., 1999). As the MTPJ 1 becomes maximallycongruent in dorsiflexion, and the collateral ligaments around theMTPJ tighten to provide stability, the MTPJ inhabits a positionknown as close-packing (Susman and Brain, 1988; Susman and deRuiter, 2004). This in vivo function corresponds well with theregional differences in bone density found in the modern humanforefoot. The dorsal region of the first metatarsal head showsgreater bone mineral density compared to the more plantarportions of the head (Muehleman et al., 1999). The same pattern isreflected in the trabecular architecture of the second proximalphalanx. The BV/TV and DA of the second proximal phalanx tend todecrease from the dorsal to plantar regions of the bone (Griffin,2008), and this suggests that the MTPJ 2 also experiences dorsalcompression during push-off.

When specific aspects of in vivo function of the modern humanforefoot are comparedwith Pan paniscus, the key role of themodernhuman forefoot during push-off is highlighted (Vereecke et al.,2003; Griffin, 2009; Griffin et al., in press). On average, themodern human MTPJ 1 experiences more dorsal excursion frommidstance to toe-off during walking than the average bonobo(either during quadrupedal or bipedal walking), and at the point ofmaximum MTPJ 1 dorsiflexion, the human hallux experiencesa loading spike (as measured by plantar pressure) compared to thelateral forefoot. This pattern is not apparent in the pressure profile ofthe bonobo hallux (Vereecke et al., 2003; Griffin, 2009; Griffin et al.,in press). Together, the comparative in vivo evidence and propertiesof bone that reflect the specific modern human meta-tarsophalangeal joint function encourage the investigation ofwhether or not the modern human pattern of trabecular architec-ture is also unique among extant hominoids, and thus diagnostic ofa metatarsi-fulcrimating foot.

This study tests two main hypotheses. The first prediction is thatmodern humans will show relatively greater enhancement in BV/TVin the dorsal region relative to the more plantar regions of the MThead than theothergreat apes.Dorsalexcursion in thebonoboMTPJ isusually less than that of modern humans (Griffin et al., in press), andgreat ape metatarsophalangeal joints do not close-pack in extensionand therefore may not provide sufficient stability in dorsiflexion forbearingweight (Susman and deRuiter, 2004). Secondly, it is expectedthat the modern human metatarsal heads will show greater anisot-ropy than those of the great apes, especially in the dorsal region of thehead because modern humans are habitual bipeds, and they exhibitamore consistentpatternof forefoot postureduringgait (ElftmanandManter, 1935; Susman, 1983; Vereecke et al., 2003; Griffin, 2009).Great apes exhibit a more diverse positional behavior than modernhumans (Tuttle, 1970; Doran, 1996), and therefore it is predicted thata behavioral repertoire (e.g., climbing, suspension, quadrupedalism)with less stereotypical loading in theMTPJ 1 andMTPJ 2will result inless trabecular anisotropy compared with the condition in modernhumanmetatarsals.

Materials

The sample consists of modern human and extant great ape firstand secondmetatarsals. Themodern human sample is composed ofmales and females from the Libben Collection (n ¼ 11); theseindividuals represent a minimally shod group. The Libben Collec-tion is a well-preserved Native American skeletal assemblage fromthe Late Woodland Period (800e1100 AD) (Lovejoy et al., 1977).These individuals likely went unshod (Trinkaus, 1975), and iffootwear (i.e., moccasins and sandals) was used, it would have beensoft and conformed to the substrate (Trinkaus, 1975; Trinkaus andHilton, 1996). Three other modern human specimens come fromThe Huntington Collection which consists of 19the20th centuryindividuals who died in the United States of America. It is assumedthese individuals went habitually shod. This collection is housed atthe National Museum of Natural History (NMNH), SmithsonianInstitution in Washington, DC. Most of the wild-collected great apesample comes from the NMNH. The sample includes males andfemales belonging to Pongo pygmaeus (n ¼ 10), Gorilla gorilla(n ¼ 8), and Pan troglodytes (n ¼ 10). The Pan paniscus sample(n ¼ 9) comes from the Royal Museum for Central Africa in Ter-vuren, Belgium, with the exception of one male individual whowasnot wild-collected. This male individual was born in the wild andbrought into captivity at the age of 2. He died at around age 30 inthe Animal Park Planckendael in Muizen, Belgium.

For each sample, only adults were included, and when age wasnot available specimens were chosen based on epiphyseal fusion ofthe long bones of the fore- and hindlimb. Also, when the optionwas

N.L. Griffin et al. / Journal of Human Evolution 59 (2010) 202e213 203


available, right elements were selected and both the first andsecond metatarsals were chosen from the same individual.

Methods

Defining anatomical orientation

Before scanning, each bone was prepared with three markers torecord the anatomical orientation. It was necessary to establishanatomical orientation because only themetatarsal head and a smallpart of the diaphysis of each bonewere scanned. By designating axesusing a marker system, anatomical orientation could be easilyestablished during analysis. Garnet stones (less than 1 mm)embedded inwaxwereusedas theanatomicalmarkers. Beloware thedescriptions of the marker placements for the first and secondmetatarsal heads:

MT1 (Fig. 1a) The bone was placed on a graph paper supportwith its long axis positioned along one line on the paper. Theintersesamoidal ridge of the metatarsal head rested on the line, andthe medial and plantar tubercles rested in the same plane. In mostcases, clay was used to secure this position. The first marker wasthen placed at the maximummedial extension of the dorsal edge ofthe head’s articular surface. Using a ruler and referring to the graphpaper support, the lateral marker was placed at the most lateralextension of the head on the dorsal edge of the articular surface atthe same height as the medial marker and on the coordinate so thatalong with the dorsal marker and the medial marker it formeda line perpendicular to the longitudinal axis of the bone. The thirdmarker, used to designate the transverse plane, was placed on thedorsal surface midway between the first and second markers.

MT 2 (Fig. 1b) The bone was placed on the graph paper support,fixing the midpoint of the most inferior edge of the proximalarticular surface on one line marked on the paper. Then thelongitudinal axis of the bone was set along this line. The medialmarker was placed at the maximum medial extension of the headon the dorsal edge of the articular surface. Using a ruler andreferring to the graph support, the lateral marker was placed at themost lateral extension of the head on the dorsal edge of the artic-ular surface at the same height as the medial marker to designate

the medio-lateral axis perpendicular to the bone’s longitudinalaxis. The third marker, used to designate the transverse plane, wasplaced on the dorsal surface midway between the first and secondmarkers.

Scanning procedures

All specimens except the wild-caught sample of bonobos werescanned at the High-Resolution X-ray Computed TomographyFacility (HRXCT) at the University of Texas at Austin (www.ctlab.geo.utexas.edu). Metatarsals were mounted in a vertical positionand elements from the same individual were scanned together asa set. Only the distal ends of the metatarsals (i.e., each head anda small portion of the shaft) were scanned. MT sets were scannedwith a source energy ranging from 180 to 200 kV, at a current of0.11mA, andwith serial cross-sectional slice resolution and spacingof 0.049 mm. Scans were collected with 1400 projections, two0.067s frames per projection, and 25 slices per rotation. The field ofview was 46mm. Data files were produced as 1024 � 1024 16-bitTIFF files, and were subsequently converted to 8-bit TIFF files withno impact on resolution. Conversions were completed using a code(written by RK) in the Interactive Data Language (IDL) 7.0 (ResearchSystems, Inc.). Since specimens were scanned in sets, each bonewas cropped in ImageJ (http://rsb.info.nih.gov/ij/download.html).

The bonobo sample from the Royal Museum for Central Africacould not be shipped to HRXCT facility for scanning, and thereforescanning was completed locally at the University of Antwerp’sMicro CT Research Group Facility (http://webh01.ua.ac.be/mct/index.htm). Each specimen was placed in a horizontal position onthe object bed. Specimens were scanned individually, and witha source energy of 100 kV and a serial cross-sectional slice reso-lution and spacing of 0.035 mm. Consistent with the scanningprocedure at HRXCT, only the metatarsal head and part of shaftwere scanned. Data files were provided in 1024�1024 8-bit bitmapformat and were then converted to 8-bit TIFFs using ImageJ.

It was possible to scan the captive bonobo’s secondmetatarsal atHRXCT and using the Skyscan machine. The HRXCT and Skyscanscanners have different configurations, and scanning the samebone using both machines provided the opportunity to make thePan paniscus sample more comparable with the rest of the samplefor analysis.

Trabecular bone analyses

The program Quant3D (Ketcham and Ryan, 2004) was used toreconstruct the three-dimensional structure of each metatarsalhead region and serve as a platform for measuring magnitude,directionality, and bone volume fraction of trabeculae. Each speci-men’s 8-bit TIFF stack of scan slices was opened directly intoQuant3D. The coordinates of each of the three garnet stonesmarkers were used to adjust the anatomical axes provided in theprogram to anatomical markers indicating orientation for eachspecimen.

For the purpose of studying the regional variation withina metatarsal head, three volumes of interest (VOI) were chosen torepresent the dorsal, central, and plantar regions. The three VOIswere arranged along the midline of the long axis of the jointsurface (Fig. 2). The Dorsal VOI was placed in an area just distal tothe articular margin of the joint on the dorsum of the head. Fora few great ape specimens, the dorsal region was especially smalland mediolaterally constricted, therefore the VOI was positionedto encompass part of the area past the joint surface on the dorsumof the head. The Central VOI was placed at the most central part ofthe joint facet and as close to the distal end as possible withoutpicking up cortex. In many of the great ape specimens, the

Figure 1. Chimpanzee (A) first metatarsal and (B) second metatarsal with garnet stonemarkers to define anatomical orientation. In each case, the longitudinal axis of themetatarsal was placed along the line defined by the number 1 on the graph paper. Thelongitudinal axis of the MT 1 was set along the line with reference to its head, whilethe longitudinal axis of the MT 2 was set on the line with reference to its base (see textfor more details). Medial and lateral garnet stone markers were placed at coordinatesthat formed a line perpendicular to the longitudinal axis of the bone. The middlemarker was placed at the midpoint of the line formed by the medial and lateralmarkers. The lateral marker in (B) is not in view due to the torsion of the metatarsalhead relative to the base.

N.L. Griffin et al. / Journal of Human Evolution 59 (2010) 202e213204


trabeculae were very dense in the center of the joint and thecortical-cancellous boundary was difficult to distinguish. Asa result, some Central VOIs were positioned slightly further backproximally to ensure that only trabecular bone was selected. ThePlantar VOI was placed in the area distal to the edge where thearticular surface ends on the plantar aspect of the bone. In attemptto select homologous VOIs in specimens of varying metatarsaljoint sizes, the first and second metatarsal VOIs were each scaledby a measurement of size of the distal joint. This size variableconsisted of two measurements using digital calipers taken in theanatomical orientation set by the garnet stone markers (Fig. 1).The dorsoplantar (DP) height was obtained by setting one tip ofthe caliper along the most dorsal margin of the metatarsal headjoint surface and the other tip along the most plantar margin ofthe metatarsal joint surface. The mediolateral (ML) breadth wasmeasured as the length between the most medial and the mostlateral projection of the head. VOI radii (voxels) of MT 1 and MT 2were determined by the following equations:

x ¼ ½ML breadthðmmÞ þ DP heightðmmÞ�=2scaled VOI radiusðvoxelsÞ ¼ x=3

First, the two joint measurements are averaged. Then theaverage is divided by three, an arbitrary number chosen aftersurveying the smallest and largest metatarsal heads in the entiresample. The survey indicated that this scaling measure allowed forthree VOIs to fit within ametatarsal headwithout excessive overlap.It must be noted that the scaling described above is based on theHRXCT sample. Since the bonobo sample was scanned at a differentresolution than the HRXCT sample (0.035 mm vs. 0.049 mm), anextra step was taken to scale each bonobo specimen. After aver-aging, the scaled bonobo VOI was then multiplied by the resolutionratio (0.049 mm/0.035 mm) for the final scaled VOI. The followingequation determined the scaled VOI for a bonobo specimen:

Scaled VOI radius in voxelsðPan paniscus sample scanned with SkyscanÞ¼ ½ðML breadthðmmÞ þ DP heightðmmÞÞ=6�

� ½0:049 mm=0:035 mm�:

The VOI radii (voxels) are reported as VOI diameters (mm) inTable 1. The MT 1 VOI diameters range from 2.9 mm (Pongo pyg-maeus) to 7.8 mm (Homo sapiens), while the MT 2 VOI diameters

Figure 2. The three VOIs (D, Dorsal; C, Central; P, Plantar) are illustrated for (A) the first metatarsal head (frontal and lateral views) and (B) second metatarsal head region (lateralregion not shown here). Often, the VOIs showed some degree of overlap and are much larger than they appear in the illustration. VOIs were arranged along the long axis of the jointsurface which for first metatarsal, usually coincided with the dorsoplantar axis set by the anatomical markers (see Fig. 1). Since the anatomical axes of the second metatarsal wereset in accordance with the proximal joint and for most of the great ape sample, the heads were twisted relative to the proximal joint surface (Fig. 1); the VOIs did not follow the pre-determined dorsoplantar axis as for MT 1.



range from 3.4 mm (Pan troglodytes) to 6.3 mm (Pongo pygmaeus).Several VOI diameters were reduced in order to avoid the selectionof cortical bone in the dorsal or central region (Table 1). It should benoted that the smaller MT 1 VOIs which belong to Pongo pygmaeusdo not capturemore than 3 trabecular struts within the central sliceof the VOI (Fig. 3). Therefore, it is possible that the continuumassumption of bone which posits that material properties arecontinuously distributed without discrete local variations at thesub-structural level (Hoffler et al., 2000) has been violated. Onestandard is that the minimum dimension of the specimen (e.g., theVOI) be significantly larger than the dimension of its structuralsubunits (e.g., the individual plates or rods of trabecular bone) (An,2000). Harrigan et al. (1988) study suggests that the VOI should belarge enough to encompass more than five trabeculae, or thecontinuum assumption may not be upheld. While this serves asa caveat, the VOIs were not made larger for two reasons. First andforemost, the Pongo MT 1s exhibit a thick cortex across the dorsalregion (Fig. 3). This limits the size of the VOI that can fit in thedorsal region of the head. Originally, the specimen with thesmallest VOI of 2.9 mm (Table 3) was calculated to have a VOI of3.2 mm. If 3.2 mm had been used, cortical bone would have thenbeen included in the VOI. The next three specimens with VOIs of

3.3, 3.4, and 3.5 mm also contain fewer than four struts in theirDorsal VOIs, but the next smallest VOIs of 3.8 mm contains five inits Dorsal VOI. For the MT 2, Homo sapiens had the smallest VOIs,but even with the smallest VOI of 3.5 mm, more than 5 trabecularstruts were present in the Dorsal VOI.

Each HRXCT VOI was separately thresholded using an iterativesegmentation algorithm (Ridler and Calvard, 1978; Trussell, 1979).In order to make the Skyscan scan sample more comparable withthe HRXCT sample, a different method of thresholding was used.The iterative segmentation algorithm procedure presumes thatthere are two components in the image, each fully represented inthe image histogram as a roughly normal (bell-shaped) distributionof gray values. The Skyscan scans were reconstructed using defaultssuch that much of the air had negative values, which were thenraised to zero due to the limitations of the graphics file format inwhich they were stored (unsigned 16-bit TIFF). This results ina “clean”, flat-looking background, and seemingly crisper edges forsolid objects, but corrupts the data with respect to the thresholdingalgorithm. Rather than being normal, the distribution of air valuesis truncated, and the mean value of air is effectively raised due tothe increments added to all negative voxels. This in turn leads theiterative algorithm to select a threshold value that is arbitrarilyhigher than it would have been had the air not been truncated, inturn artificially lowering the BV/TV. To avoid this, a single thresholdwas used for the entire Skyscan dataset based on the MT 2 of thecaptive Pan paniscus that had been scanned by both machines. Firstthe HRXCT dataset of the captive specimen was imported intoQuant3D. The largest possible Central VOI was selected, the itera-tive segmentation method was selected, a threshold value wasselected and the generated BV/TV (0.51) was recorded. Then theSkyscan dataset of the same specimen was imported, the scaled“largest possible Central VOI” was selected and a threshold waschosen to result in a BV/TV of 0.51, making it more compatible withthe HRXCT dataset. The resulting threshold was recorded and usedfor the rest of the Pan paniscus sample, which we judged acceptablebecause of the similar sizes of the specimens and consistent graylevels for cortical bone.

For the entire sample, trabecular bone properties were quanti-fied using the star volume distribution method (SVD) (Cruz-Oriveet al., 1992; Karlsson and Cruz-Orive, 1993; Ketcham and Ryan,2004; Ryan and Krovitz, 2006). Each SVD calculation was pro-grammed to run with 2,049 uniformly distributed orientations at8,000 random points placed within the bone phase. From eachpoint, the SVD calculation extends very minute cones in various

Table 1Volume of Interest (VOI) Size Distributions.

Taxon Scaled VOI (millimeters)

MT 1 MT 2

Mean Range Stdev Mean Range Stdev

Homo sapiens 6.8a 5.8e7.8 0.58 4.3 3.5e4.8 0.36Pan troglodytes 5.0 4.6e5.4 0.27 4.3c 3.4e4.7 0.41Pan paniscus 4.6 4.2e4.9 0.30 4.2d 3.8e4.5 0.23Gorilla gorilla 5.9 5.0e6.7 0.68 5.2e 4.0e5.9 0.66Pongo pygmaeus 3.9b 2.9e4.7 0.55 5.3 4.2e6.3 0.63

a One specimen’s Plantar VOI was reduced from 5.9 to 4.9 to avoid the selection ofcortical bone. This reduced VOI value was not included in the generation of thesummary statistics above.

b One specimen’s Plantar VOI was reduced from 4.7 to 4.1 to avoid the selection ofcortical bone. This reduced VOI value was not included in the generation of thesummary statistics above.

c Three separate specimens VOIs (3.8, 4.2, 4.6) were reduced (3.4, 3.9, 4.4) to avoidthe selection of cortical bone.

d Six specimens’ VOIs (5.9, 5.5, 6.2, 6.1, 6.3, 6.1) were reduced (5.7, 5.4, 5.7, 5.9, 6.0,6.0) to avoid the selection of cortical bone.

e One specimen’s VOIs were reduced from 6.3 to 5.9 to avoid the selection ofcortical bone.

Figure 3. Two views (left, frontal; right, sagittal) of a scan slice at the center of the Dorsal VOI (shown here as a circle). Originally, the VOI of this orangutan MT 1 was scaled to be3.2 mm, but due the large amount of cortical bone in the dorsal region of the head (A), the VOI was reduced to 2.9 mm. Note that only 1e2 struts are present per view.



directions within the bone until a bone-marrow interface isreached. The vertex of each cone originates from each point. Thevolumes of the cones are then used to reconstruct the magnitudes(eigenvalues) and principal component directions (eigenvectors) ofeach VOI. Properties of trabecular bone fabric structure weregenerated from the eigenvalues ðbs1;bs2;bs3Þ. This study focuses onthe variable DA, which is equal to ðbs1=bs3Þ. Finally, eigenvectors (û1,û2, û3) were used to generate stereographic projections, whichillustrate the trabecular bone fabric structure of the VOI in refer-ence to established anatomical axes (x, mediolateral; y, dorso-plantar; z, proximodistal).

Statistical procedures

Before exploring interspecific differences for each metatarsal,comparisons of trabecular bone properties were made betweenhabitually shod (Huntington Collection) and minimally shod (Lib-ben Collection) modern human samples. Mann-Whitney U testswere run to test for differences in BV/TV and DA, between thesehuman samples. Also, the values of the captive bonobo werechecked for overlap with the wild sample of Pan paniscus.

Taxonomic differences in absolute values for bone volumefraction and degree of anisotropy were tested using the Mann-

Table 2MT 1 summary statistics.

VOI Taxon N Bone Volume Fraction (BV/TV) Degree of Anisotropy (DA)

Mean Min Max SD Mean Min Max SD

Dorsal Homo sapiens (7,6) 13 0.42 0.37 0.47 0.038 6.9 3.7 10.7 2.5Habitually shod (2,1) 3 0.42 0.38 0.46 0.044 5.8 3.9 9.5 3.2Minimally shod (5,5) 10 0.42 0.37 0.47 0.038 7.3 3.7 10.7 2.4Pan troglodytes (3,6) 9 0.50 0.41 0.61 0.067 3.6 1.7 5.2 1.1Pan paniscus (3,5) 8 0.51 0.43 0.65 0.06 3.8 2.2 5.9 1.2Gorilla gorilla (5,3) 8 0.44 0.37 0.50 0.05 4.1 1.7 6.9 1.8Pongo pygmaeus (5,5) 10 0.39 0.28 0.49 0.06 3.5 2.0 11.3 2.8

Central Homo sapiens (7,6) 13 0.38 0.30 0.45 0.04 5.6 2.6 11.2 2.6Habitually shod (2,1) 3 0.40 0.37 0.43 0.03 7.8 5.3 11.2 3.1Minimally shod (5,5) 10 0.38 0.30 0.45 0.05 5.0 2.6 8.8 2.2Pan troglodytes (3,6) 9 0.51 0.42 0.58 0.05 2.6 1.7 3.7 0.7Pan paniscus (3,5) 8 0.51 0.43 0.69 0.08 3.8 2.2 7.2 1.6Gorilla gorilla (5,3) 8 0.49 0.42 0.57 0.05 3.8 2.0 6.5 1.6Pongo pygmaeus (5,5) 10 0.47 0.40 0.53 0.05 2.0 1.4 2.4 0.4

Plantar Homo sapiens (7,6) 13 0.30 0.23 0.39 0.04 4.3 1.7 11.0 2.5Habitually shod (2,1) 3 0.30 0.27 0.32 0.03 7.3 3.9 11.0 3.6Minimally shod (5,5) 10 0.31 0.23 0.39 0.05 3.4 1.7 5.7 1.4Pan troglodytes (3,6) 9 0.46 0.41 0.51 0.03 2.3 1.7 3.7 0.6Pan paniscus (3,5) 8 0.45 0.37 0.61 0.07 3.9 2.0 5.5 1.2Gorilla gorilla (5,3) 8 0.41 0.35 0.49 0.046 3.5 2.4 6.0 1.1Pongo pygmaeus (5,5) 10 0.41 0.32 0.52 0.057 2.6 1.3 6.5 1.5

Numbers of males and females in parentheses.SD ¼ Standard Deviation.

Table 3MT 2 summary statistics.

VOI Taxon N Bone Volume Fraction (BV/TV) Degree of Anisotropy (DA)

Mean Min Max SD Mean Min Max SD

Dorsal Homo sapiens (7,6) 13 0.36 0.29 0.45 0.038 8.4 4.4 16.0 3.3Habitually shod (2,1) 3 0.37 0.35 0.39 0.019 11.0 7.8 16.0 4.4Minimally shod (5,5) 10 0.36 0.29 0.45 0.042 7.6 4.4 13.0 2.8Pan troglodytes (4,6) 10 0.46 0.42 0.54 0.037 2.2 1.5 4.1 0.8Pan paniscus (4,5) 9 0.44 0.35 0.52 0.05 2.2 1.7 2.8 0.36Gorilla gorilla (5,3) 8 0.42 0.35 0.51 0.05 2.9 1.6 4.1 1.00Pongo pygmaeus (5,5) 10 0.30 0.24 0.41 0.05 2.7 1.9 5.5 1.05

Central Homo sapiens (7,6) 13 0.35 0.28 0.40 0.05 6.7 3.0 14.2 3.10Habitually shod (2,1) 3 0.31 0.28 0.36 0.05 10.3 7.7 14.2 3.39Minimally shod (5,5) 10 0.36 0.28 0.40 0.04 5.6 3.0 9.3 2.15Pan troglodytes (4,6) 10 0.46 0.42 0.51 0.03 2.1 1.3 3.7 0.65Pan paniscus (4,5) 9 0.49 0.39 0.59 0.06 2.4 2.0 3.3 0.38Gorilla gorilla (5,3) 8 0.46 0.38 0.58 0.07 2.6 1.8 4.3 0.84Pongo pygmaeus (5,5) 10 0.45 0.39 0.50 0.03 2.5 1.5 3.1 0.47

Plantar Homo sapiens (7,6) 13 0.28 0.23 0.35 0.04 4.5 2.9 8.5 1.85Habitually shod (2,1) 3 0.29 0.26 0.32 0.03 3.5 2.9 4.3 0.76Minimally shod (5,5) 10 0.28 0.23 0.35 0.04 4.8 3.2 8.5 2.00Pan troglodytes (4,6) 10 0.41 0.38 0.46 0.03 2.5 1.5 3.6 0.56Pan paniscus (4,5) 9 0.38 0.35 0.44 0.02 2.6 1.8 3.5 0.49Gorilla gorilla (5,3) 8 0.35 0.24 0.50 0.086 2.3 1.7 2.7 0.30Pongo pygmaeus (5,5) 10 0.35 0.28 0.40 0.047 2.7 1.6 5.0 1.0

Numbers of males and females in parentheses.SD ¼ Standard Deviation.



Whitney U test, with a p-value of 0.05 taken as a measure ofsignificance. There were several comparisons made betweenhumans and each great ape taxon, (i.e., at least 8 tests for each MTVOI), therefore the Dunn-�Sidák method (Sokal and Rohlf, 1995) wasused to reduce the probability of making a type 1 error. The DorsalVOI comparisons between humans and all the great apes were notsubject to this correction because they directly test the mainhypothesis. Box plots were generated to compare the pattern ofaverages for a given value (i.e., BV/TV or DA) for the three VOIs pertaxon to explore regional differences within a metatarsal head.Wilcoxon Matched Pairs tests were run to assess regional differ-ences (Dorsal vs. Plantar VOI per taxon). Only the Dorsal and PlantarVOIs were compared because in many cases either or both theDorsal and Plantar VOI overlapped in varying degrees with theCentral VOI.

Results

As predicted, in modern human MT heads, the highest meanbone volume fraction values occur in the dorsal region; the modernhuman metatarsal heads tend to be generally more anisotropicthan those of the great apes (Tables 2 and 3).

The habitually shod and minimally shod samples correspondwell with each other, and only one significant difference was foundbetween the two groups (Table 4). The habitually shod sample hasa significantly larger DA for the MT 2 Central VOI (p-value ¼ 0.028).Because there was only one significant difference out of twelvecomparisons, these two samples were pooled together to form onesample for the interspecific comparisons.

Regarding the captive and wild bonobo comparisons, all of thecaptive bonobos’ trabecular bone property values overlapped withranges of values for the wild-caught bonobos (Table 5). Therefore,the captive bonobowas included as part of the wild-caught bonobosample for all the following interspecific comparisons.

Overall, the Mann-Whitney U-tests indicate that for thecomparisons between modern humans and each great ape taxon,modern humans usually have less bone volume fraction and moreanisotropy for each VOI type (Table 6). Significant differences in MT1 BV/TV are found for taxonomic comparisons under all VOIs,especially MT 1 Central and Plantar VOIs. Regarding DA, modernhuman VOIs usually have larger values than corresponding greatape VOIs, but this is only significant for most of the Dorsal VOI andtwo Central VOI comparisons. It should be noted that the specimenwith the largest MT 1 DA for the Dorsal VOI is not a modern humanspecimen, but an orangutan specimen (Table 2). This specimen alsohas the smallest BV/TV. It is likely that, as a consequence of

capturing an exceptionally small amount of trabecular bone ina VOI, if two or three struts are present and show a similar pref-erence in orientation, an unusually high DA value will be obtained.For both BV/TV and DA, the specimen’s value is outside the 95%confidence interval of the mean for orangutans.

As found for the first metatarsal, most taxonomic comparisonsreveal that modern human second metatarsal VOIs have signifi-cantly lower BV/TV values than great ape VOIs (Table 6). For all MT2 comparisons, modern humans have significantly greater DA thanall the great apes, (Table 6). In sum, not only do modern humanshave Dorsal VOIs that are on average more anisotropic thanhominid Dorsal VOIs, modern human Central and Plantar VOIs alsotend to be more anisotropic as well, with the exception of the MT 1Plantar VOI comparison between humans and bonobos.

Modern humans are distinct from all the great apes exceptbonobos in regional differences in trabecular architecture for theMT 1 except the Dorsal VOI has a significantly greater bone volume

Table 4Mann-Whitney U Test p-values for habitually shod human and habitually unshodhuman comparisons.

Trabecular BoneProperty

Metatarsal One Metatarsal Two

Dorsal Central Plantar Dorsal Central Plantar

Bone Volume Fraction (BV/TV) 1.00 0.94 0.81 0.47 0.16 0.57Anisotropy (DA) 0.37 0.22 0.077 0.16 0.028 0.16

Table 5Trabecular bone property values of the captive and wild-caught Pan paniscus MT 2s.

Sample Dorsal VOI Central VOI Plantar VOI

BV/TV DA BV/TV DA BV/TV DA

Captive Pan paniscus (n ¼ 1) 0.48 2.2 0.53 2.6 0.39 2.9

Wild caught Pan paniscus value range (n ¼ 8) (0.35e0.52) (1.75e2.85) (0.39e0.58) (1.97e3.28) (0.35e0.44) (1.8e3.5)

Table 6Mann-Whitney U Test p-values for taxon comparisons.

Metatarsal One

Dorsal VOI BV/TV DA

Homo sapiens vs. Hominids L0.05 0.000026Homo sapiens vs. Pan troglodytes L0.0026 0.0014Homo sapiens vs. Pan paniscus L0.00066 0.0025Homo sapiens vs. Gorilla gorilla �0.37 0.020Homo sapiens vs. Pongo pygmaeus 0.34 0.00064

Central VOIHomo sapiens vs. Pan troglodytes L0.000016 0.00039Homo sapiens vs. Pan paniscus L0.000039 0.089Homo sapiens vs. Gorilla gorilla L0.000069 0.076Homo sapiens vs. Pongo pygmaeus L0.000079 0.0000020

Plantar VOIHomo sapiens vs. Pan troglodytes L0.0000040 0.017Homo sapiens vs. Pan paniscus L0.000020 �0.97Homo sapiens vs. Gorilla gorilla L0.00030 0.75Homo sapiens vs. Pongo pygmaeus L0.00017 0.036

Metatarsal TwoDorsal VOIHomo sapiens vs. Hominids L0.040 3.9E-11Homo sapiens vs. Pan troglodytes L0.000021 0.0000020Homo sapiens vs. Pan paniscus L0.0019 0.00000040Homo sapiens vs. Gorilla gorilla L0.020 0.000010Homo sapiens vs. Pongo pygmaeus 0.0041 0.000012

Central VOIHomo sapiens vs. Pan troglodytes L0.0000020 0.000012Homo sapiens vs. Pan paniscus L0.000028 0.000016Homo sapiens vs. Gorilla gorilla L0.00030 0.00012Homo sapiens vs. Pongo pygmaeus L0.000012 0.0000035

Plantar VOIHomo sapiens vs. Pan troglodytes L0.0000020 0.00017Homo sapiens vs. Pan paniscus L0.0000040 0.000076Homo sapiens vs. Gorilla gorilla �0.53 0.00000983Homo sapiens vs. Pongo pygmaeus L0.0050 0.00086

A negative p-value indicates that the second sample in the comparison has greatervalues.Significant p-values are in bold type. The Dunn-�Sidák method was used to makeadjustments for multiple comparisons (see text for description).



fraction than the Plantar VOI (Table 7, Fig. 4a). If the completeregional pattern, including the Central VOI is considered, modernhuman MT1s are differentiated from chimpanzees, gorillas, andorangutans (Fig. 4). While the modern human pattern showsa decrease in the mean value of BV/TV from the dorsal to plantarregion, the three great ape taxa show an increase in mean BV/TV

from the Dorsal VOI to the Central VOI and then a decrease in meanBV/TV from the Central VOI to the Plantar VOI. The mean values ofthe Dorsal and Central VOIs are the same for the bonobos. Orang-utans show a unique pattern in that the Plantar VOI has a slightlylarger mean than the Dorsal VOI.

In modern humans, the degree of anisotropy in the first meta-tarsal follows the same regional pattern as bone volume fraction,with a significant decrease from the dorsal to plantar region (p-value ¼ 0.015, Table 7, Fig. 4b). Chimpanzees are the only othertaxon that shows a significant difference between the Dorsal andPlantar VOIs (p-value ¼ 0.028, Table 7). Gorillas show the samepattern, but the difference between the Dorsal and Plantar VOI isnot significant. Orangutans show a unique pattern in which DAdecreases from the Dorsal VOI to Central VOI, and the Plantar VOIhas a larger mean DA value than that for the Central VOI.

The modern human MT 2 pattern is the same pattern as the MT1, with significantly lower BV/TV values than the apes in mostcomparisons (Table 6) and a significant decrease in BV/TV from thedorsal to plantar regions of the head (p-value ¼ 0.0015, Tables 7,Fig. 4c). All African great apes show the same statistically significantpattern as modern humans, but the orangutan Dorsal VOI showsthe opposite pattern and only approaches significance. Bonobos,gorillas, and orangutans are each distinct from modern humans inthat their Central VOIs have the largest mean values of BV/TVcompared to their respective Dorsal and Plantar VOIs. Orangutansagain show a unique pattern in that the Plantar VOI has a largermean than the Dorsal VOI.

Table 7Wilcoxon Matched Pairs Test p-values of Dorsal and Plantar VOI comparisons.

Taxon MT 1 Dorsal VOIvs. Plantar VOI

MT 2 Dorsal VOIvs. Plantar VOI

Homo sapiensBV/TV 0.0015 0.0015DA 0.016 0.011

Pan troglodytesBV/TV 0.110 0.017DA 0.028 0.24

Pan paniscusBV/TV 0.012 0.011DA 0.57 0.086

Gorilla gorillaBV/TV 0.069 0.036DA 0.48 0.16

Pongo pygmaeusBV/TV 0.39 �0.059DA 0.093 0.72

A negative p-value indicates that the Plantar VOI has a larger value.

Figure 4. Each boxplot shows the mean (closed square, Dorsal VOI; open circle, Central VOI; closed triangle, Plantar VOI) and the whiskers represent the standard deviation values.Dotted lines connect the mean values of the VOIs for each taxon in order to show patterns more clearly. (A) The modern human BV/TV decreases smoothly from the Dorsal to PlantarVOI. In contrast, the bonobo mean Dorsal and Central VOIs are the same, and the chimpanzees, gorillas, and orangutans show an increase in BV/TV from the Dorsal to Central VOIand then a decrease from the Central to Plantar VOI. Both the modern human and bonobo Dorsal VOIs have significantly larger BV/TV values than the corresponding Plantar VOIs.(B) All taxa show a decline in DA from the Dorsal to Plantar VOIs, however, this decline is only significant in modern humans and chimpanzees. (C) Modern humans show the uniquepattern of BV/TV decline from the dorsal to central then plantar region, while for the other great apes, the BV/TV mean value of the Central VOI tends to be larger than either of theDorsal or Plantar VOIs. When the Dorsal and Plantar VOIs are compared, all taxa, except orangutans show a significant difference. (D) Consistent with the variation shown by the MT2 BV/TV and also with the MT 1 BV/TV and DA, the human MT 2 DA shows a smooth decline from the dorsal region of the head to the plantar region. Gorillas follow a similar pattern,but modern humans are the only taxon that has significantly larger values of DA for the Dorsal VOIs than the Plantar VOIs. Note that for both chimpanzees and bonobos, DA showsa slight increase in mean DA from the Dorsal to Plantar VOI.



The measurement of the degree of anisotropy in the secondmetatarsal also distinguishes the modern humans from the greatapes (Table 7, Fig. 4d). To the exclusion of the great apes, the dorsalregion of the modern human metatarsal head shows significantlymore organization than the more plantar regions. Gorillas are theonly great ape taxon that hints at a similar pattern of regionalanisotropy, but for this taxon, the Dorsal and Plantar VOIs are notsignificantly different from each other (Fig. 4d). Chimpanzees andbonobos show a slight, but insignificant, increase in DA from theDorsal to Plantar VOI. From the Dorsal VOI to the Central VOI inorangutans, the mean DA value decreases from the Dorsal toCentral VOI and then for the Plantar VOI, it reaches a comparablemean value to that of the Dorsal VOI.

Regional patterns within a MT head partially support the firsthypothesis that modern human VOIs have greater relative BV/TV inthe dorsal region. Modern humans show this pattern but so doother hominid taxa. There is more support for our secondhypothesis. The modern human sample shows the greatest abso-lute DA, especially in the dorsal region of either the MT 1 or MT 2head, but only the modern human MT 2 is unique from the greatapes in having a Dorsal VOI that has significantly greater DA thanthe respective Plantar VOI.

Overall, the results of the absolute and regional differences of BV/TV andDAofMT1 andMT2drawattention to a pattern that requiresfurther investigation. Modern human MT VOIs tend to have lesstrabecular bone per unit volume and this trabecular bone is stronglydirected along one or more axes, while great apes tend to show theopposite pattern. If BV/TV and DA are correlated with each other itwould be difficult to attributeDA to function if BV/TV is an influentialfactor or conversely, a BV/TV to function, if DA is an influential factor.To test for a correlation, the Spearman Rank Correlation Coefficientwas considered for each VOI separately. BV/TV and DA values of allspecimens were included in each test. In four out of six cases, DA isnegatively correlated with BV/TV (Fig. 5). However, when themodern human sample is removed and for each MT VOI, no corre-lation is found in any case. Also, when the human sample is analyzedalone no correlation is found in any case. This evidence suggests thatthe trabecular bone structure of modern human metatarsals is nota related to a difference in relative bone mass.

Discussion

The first hypothesis, that modern human metatarsal heads areunique among the great apes by exhibiting relatively greater bonevolume fraction in the dorsal region of the head relative to themoreplantar region, receives no support. For both MT 1 and MT 2, themodern human Dorsal VOI has significantly a greater BV/TV valuethan its respective Plantar VOI (Table 7); however, this is also truefor the bonobo sample for MT 1, and for all taxa except orangutansfor MT 2.

The second hypothesis is more fully supported. Modern humansare not the only taxon that tends to have significantly moreanisotropic Dorsal VOIs compared to Plantar VOIs for the firstmetatarsal because chimpanzees also show this pattern. However,modern human MT 2 heads uniquely show significantly moreanisotropy in the dorsal region compared to the plantar region.Also, both modern human metatarsals generally present greateranisotropy compared to all the great ape taxa, as illustrated by theresults of the Mann-Whitney U tests (Table 6). Regarding DorsalVOI, modern human MTs have significantly higher DA than thegreat apes.

Though it is possible that greater BV/TV, especially in the centraland plantar regions of the great ape metatarsal heads, may be anindicator of greater overall loading at these joints, it may also reflectsystemic differences present in both the cortical bone and

trabecular bone of modern humans and great apes. Ruff (1987)found that modern humans tend to have relatively more slenderfemora and tibiae than modern non-human primates. The presentstudy could not test this finding statistically, although great apevalues of trabecular BV/TV in the posterior region of the calcaneuswere found to be larger than those of modern humans (Maga et al.,2006). A possible cause for these differences may lie in the trend ofan overall increase in gracilization of Homo from the Pleistocene tomodern times (Frayer, 1984; Ruff et al., 1993; Ruff, 2002; Walker,2009). Therefore, examining BV/TV differences in other anatom-ical regions will reveal whether or not this difference is systemic.Also, testing changes through ontogeny in great apes and modernhuman metatarsals, as well as sampling MTs from archaic Homo,Neandertals, and early modern humans may help explain differ-ences in trabecular bone volume fraction in extant humans andgreat apes. In sum, the current comparisons of the modern humansand great ape samples suggest that, compared to BV/TV, DA appearsto be more sensitive for distinguishing hominids that engage inhabitual metatarsi-fulcrimating bipedal walking from those that donot use the metatarsophalangeal joint for propulsion. This may alsocorrelatewith amore diverse locomotor regime among non-bipeds.

It remains possible that similarities between humans and apesin bone volume fraction regional variation may be a consequence ofinteractions between trabecular and cortical bone during growth.For example, if the dorsal region of the cortex thickens in responseto the habitual loading during push-off in modern humans, thiswould relax the need for the trabecular bone volume to changedramatically in the dorsal region. This hypothesis is supported byMuehleman et al. (1999) study showing that the dorsal region ofthe modern human first metatarsal head shows greater bonemineral density compared to themore plantar portions of the head.As encouraged by Egi et al. (2005), who investigated the regionaldistribution of both cancellous and cortical bone in the humeri ofnon-human primates, it may be necessary to combine the analysesof cortical and trabecular bone morphology of the metatarsal headto fully understand why BV/TV is not a clear indicator of differencesin loading patterns between modern humans and the great apes.

Indications of modern human and great ape forefoot function

Despite the fact that other hominids share a similar pattern tomodern humans with a decrease in bone volume fraction from thedorsal to plantar regions of the metatarsal head, humans differfrom the great apes in the degree of anisotropy, especially in thedorsal region. In addition, the human second metatarsal is distinctfrom all the great ape metatarsals in that the Dorsal VOI hassignificantlymore anisotropy than the Plantar VOI, a pattern similarto the base of the human second proximal phalanx (Griffin, 2008).

Principal axes of trabecular fabric structure are currently lessinformative in distinguishing humans from great apes based onforefoot function. The primary direction of trabecular bone orien-tation follows the longitudinal axis of the bone in both humans andgreat apes (Griffin, 2009). Between rays, the direction of thetrabecular fabric structure in the human second metatarsal showsa greater dorsoplantar component of the primary eigenvector thanthe first metatarsal, and this is true for the other great apes too,except orangutans (Griffin, 2009). The slight difference in directionof the first principal axis between the rays is most likely a result ofdifferences in how anatomical orientation was determined for thefirst and second metatarsals. The MT 1s were set with reference totheir heads, while MT 2s were set with reference to their bases. TheMT 2 heads, especially those of the great apes are often twistedrelative their bases (Lewis, 1989) (Fig. 1), and therefore, trabeculaerunning proximodistally may not be align with the longitudinalaxis set by the base of the metatarsal.



The concentration of trabecular bone in the center of the joint ofboth metatarsals as reflected by the larger mean value in theCentral VOI compared to the Dorsal VOI represents one of the mostnotable regional patterns in the great ape sample (Fig. 4). For bothmetatarsals, orangutans separate from the rest of the great apesbecause the plantar BV/TVmean value exceeds the Dorsal VOI’s BV/TV mean value, though this is not significant in either case.

Predictions for fossil hominin forefoot function

Given a first or second metatarsal, what results from a trabecularbone analysis would make a convincing argument that its ownerwould have exhibited a modern human-like forefoot function?Because the samples overlap in both absolute DAvalues and regional

differences in DA, it will be difficult to make predictions abouta single specimen if its values consistently fall within the range ofoverlap betweenmodern humans and great apes. Clearly, a DA valuethat is within the upper range of the values for the modern humansample would provide the strongest signal in the case of a fossil.Moreover, the following complex of characteristics would also alignthe fossil with the modern human sample: (1) greater overallanisotropy in the metatarsal head compared to the great apes, (2)a gradual decline in DA from the dorsal to plantar region, and (3)a gradual decline in BV/TV with the absence of greater density in thecentral region of the joint. Based on the results of this study, it maybe easier to identify amodern human-like functioningMT 2 thanMT1 because the differences between modern humans and great apesfor MT 2 DA are more pronounced (Fig. 4).

Figure 5. Absolute comparisons and differences in regional variation in VOIs illustrate that modern humans tend to have greater DA but lower BV/TV when compared to the greatapes. To test for a correlation between DA and BV/TV, Spearman Rank Coefficients were generated for all VOIs separately and with all specimens included in each case. Thescatterplots of the first and second metatarsals are shown here along with their Spearman r values and p-values. Four out of the six tests result in significant p-values. Modernhumans, closed squares; chimpanzees, open triangles; bonobos, open circles; gorillas, crosses; orangutans, closed diamonds.



Conclusion

This study of the comparative trabecular architecture of theheads of first and second metatarsals in extant hominoids supportsin vivo functional differences in the modern human and great apeforefoot. In addition to having greater anisotropy and relative bonevolume in the dorsal region of both metatarsal heads, the sharedpatterns of regional bone volume and anisotropy in the first andsecond metatarsals reinforce the shared-role of the two rays atpush-off (Bojsen-Møller, 1979).

Bone volume fraction value did not serve to distinguish modernhumans fully from the great apes. However, the differences indegree of anisotropy, especially in the dorsal region of the first andsecond metatarsals of modern human and great apes, are consis-tent with functional differences. This, in turn, encourages theinvestigation of early hominin foot bones to help reconstructforefoot loading patterns and gait.

Acknowledgements

We are grateful to Linda Gordon and Dr. Dave Hunt (NMNH), Dr.Emmanuel Gilissen (Museum for Central Africa), Dr. Owen Lovejoy(Libben Collection) for access to the collections used in this studyand their assistance during data collection. Special thanks to Dr.Jessie Maisano at the HRXCT lab for all of her help, Dr. Nora DeClerkfor permitting NG and KD to work in her microCT lab facility, andDr. Christine Wall for providing NG a computer to run part of theanalysis. We also extend our appreciation to Dr. Masato Nakatsu-kasa and Dr. Bernard Wood for reviewing earlier versions of thismanuscript. NGwould also wish to acknowledge Dr. Daniel Schmittfor his continuous support and guidance. Funding has beenprovided by the GWU Cotlow Field Research Fund, Sigma Xi Grant-in-Aid of Research, L.S.B. Leakey Foundation, the National ScienceFoundation: BCS-0726124, NSF IGERT DGE-9987590 and DGE-0801634, the GWU Selective Excellence Fellowship for HominidPaleobiology, and Duke University.

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