Comparative forefoot trabecular bone architecture in extant hominids

Journal of Human Evolution 59 (2010) 202e213

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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. Ketcham g, Andrei Postnov h, i a

Department of Evolutionary Anthropology, Duke University, P.O. Box 90383 Science Drive Durham, NC, USA Department of Biology, University of Antwerp, Antwerp, Belgium c Centre for Research and Conservation, Royal Zoological Society of Antwerp, Antwerp, Belgium d Department of Anthropology, Pennsylvania State University, Pennsylvania, USA e Center for the Advanced Study of Hominid Paleobiology, The George Washington University, Washington, DC, USA f Human Origins Program, Smithsonian Institution, Washington, USA g Department of Geological Sciences, University of Texas at Austin, Austin, TX, USA h Department of Biomedical Sciences, University of Antwerp, Antwerp, Belgium i Lebedev Physical Institute, Moscow, Russia b

a r t i c l e i n f o

a b s t r a c t

Article history: Received 22 February 2010 Accepted 3 June 2010

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 differentiate metatarsophalangeal joint functional differences in extant great apes and humans. In this study, we approach the problem by quantifying properties of internal bone architecture that may reflect different loading patterns in metatarsophalangeal joints in humans and great apes. High-resolution x-ray computed 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. While bone 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 trabecular architecture in the dorsal regions of the human metatarsals are indicative of a forefoot habitually used for propulsion during gait. This study provides a potential route for predicting forefoot function and gait in fossil hominins from metatarsal head trabecular bone architecture. Ó 2010 Elsevier Ltd. All rights reserved.

Keywords: Anisotropy Bone volume fraction Hallux Metatarsal Proximal phalanx

Introduction Although all extant hominoids are capable of walking bipedally, it is well accepted that only modern humans dorsiflex their metatarsophalangeal joints to form a stiff propulsive lever during the terminal 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 when a modern human-like metatarsi-fulcrimating forefoot appeared in the fossil record has inspired a longstanding debate (e.g., Latimer, 1991; Stern and Susman, 1991; Stern, 2000; Bennett et al., 2009).

Abbreviations: MTPJ, metatarsophalangeal joint; MT, metatarsal; BV/TV, bone volume fraction; DA, degree of anisotropy; VOI, volume of interest; HRXCT, HighResolution X-ray Computed Tomography Facility. * Corresponding author. E-mail address: nicole.griffi[email protected] (N.L. Griffin). 0047-2484/$ e see front matter Ó 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.jhevol.2010.06.006

This lack of consensus has mainly centered on the oldest, most complete set of metatarsophalangeal foot bones, A.L. 333-15 which has been attributed to Australopithecus afarensis (Latimer et al., 1982). Au. afarensis metatarsals and pedal phalanges have been described as showing a mosaic of derived and primitive external characteristics that have suggested to some researchers that Au. afarensis forefoot function was not completely modern human-like, but adapted for a mixed locomotor repertoire (Stern and Susman, 1983; Susman et al., 1984). Other researchers argue that primitive traits have little value in making inferences about function, and these researchers advocate a modern human-like forefoot function in Au. afarensis (Latimer and Lovejoy, 1990; Latimer, 1991). The goal of the current study is to test the potential of an alternative method, the study of trabecular bone, and to resolve current debates surrounding early hominin forefoot function. Several in vivo studies have shown that trabecular struts and plates respond to the direction and magnitude of local loading by

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

aligning themselves in the direction of stress and increasing in density (e.g., Lanyon, 1974; Goldstein et al., 1991; Pontzer et al., 2006; van der Meulen et al., 2006) and therefore offer a new approach to test hypotheses that have long remained unresolved about joint function in fossils. In addition, high-resolution X-ray computed tomography has allowed researchers to show significant differences in trabecular bone properties between primate locomotor categories (Fajardo and Müller, 2001; MacLatchy and Müller, 2002; Ryan and Ketcham, 2002a,b, 2005). However, it must be noted that some studies have provided contradictory evidence suggesting that trabecular bone is not always a reliable indicator of mechanical demand, and properties of trabecular bone do not always 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 the relationship between the trabecular architecture of the calcaneus and locomotor regime in extant hominids. Though the analysis was preliminary as a result of small sample size, the authors found that modern human calcanei show greater values of anisotropy (i.e., the strength of orientation in one or more directions) than those of the great apes. This supports the hypothesis that taxa with more diverse locomotor repertoires (e.g., a mix of climbing and quadrupedalism) exhibit a less stereotypical pattern of trabecular fabric structure in the posterior region of the calcaneus. Therefore, studying the relationship between trabecular architecture of the foot and locomotor type has shown promise as an indicator of differences in positional behavior in living and extinct hominids. The current study focuses on the trabecular architectural properties of the first and second metatarsal heads. The two properties of primary interest are trabecular bone volume fraction (i.e., bone volume/total volume or BV/TV) and degree of anisotropy (DA). BV/TV has been found to be correlated with Young’s modulus, a measure of bone stiffness (Hodgskinson and Currey, 1990; Kabel et al., 1999; Ulrich et al., 1999; Ding et al., 2002) and DA indicates the degree to which bone is aligned in a preferred orientation or orientations (i.e., trabeculae adapted for stereotypical loading along one or more axes will show greater DA values than trabeculae adapted for multidirectional loading) (Ryan and Ketcham, 2002a,b). Specific predictions about trabecular bone differences in the heads of modern human and great ape metatarsals can be based on existing studies of modern human forefoot bone properties and the quantified in vivo functional differences of the forefoot in modern humans and Pan paniscus (bonobos). Each metatarsal head represents the male mating joint surface of a metatarsophalangeal joint (MTPJ) which becomes part of the weight-bearing fulcrum of the forefoot 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 is transferred to the anterior part of the foot and each phalanx moves onto the dorsum of its respective metatarsal head. As noted for the MTPJ 1, elevated joint compression occurs then (Hetherington et al., 1989; Muehleman et al., 1999). As the MTPJ 1 becomes maximally congruent in dorsiflexion, and the collateral ligaments around the MTPJ tighten to provide stability, the MTPJ inhabits a position known as close-packing (Susman and Brain, 1988; Susman and de Ruiter, 2004). This in vivo function corresponds well with the regional differences in bone density found in the modern human forefoot. The dorsal region of the first metatarsal head shows greater bone mineral density compared to the more plantar portions of the head (Muehleman et al., 1999). The same pattern is reflected in the trabecular architecture of the second proximal phalanx. The BV/TV and DA of the second proximal phalanx tend to decrease from the dorsal to plantar regions of the bone (Griffin, 2008), and this suggests that the MTPJ 2 also experiences dorsal compression during push-off.

203

When specific aspects of in vivo function of the modern human forefoot are compared with Pan paniscus, the key role of the modern human forefoot during push-off is highlighted (Vereecke et al., 2003; Griffin, 2009; Griffin et al., in press). On average, the modern human MTPJ 1 experiences more dorsal excursion from midstance to toe-off during walking than the average bonobo (either during quadrupedal or bipedal walking), and at the point of maximum MTPJ 1 dorsiflexion, the human hallux experiences a loading spike (as measured by plantar pressure) compared to the lateral forefoot. This pattern is not apparent in the pressure profile of the bonobo hallux (Vereecke et al., 2003; Griffin, 2009; Griffin et al., in press). Together, the comparative in vivo evidence and properties of bone that reflect the specific modern human metatarsophalangeal joint function encourage the investigation of whether or not the modern human pattern of trabecular architecture is also unique among extant hominoids, and thus diagnostic of a metatarsi-fulcrimating foot. This study tests two main hypotheses. The first prediction is that modern humans will show relatively greater enhancement in BV/TV in the dorsal region relative to the more plantar regions of the MT head than the other great apes. Dorsal excursion in the bonobo MTPJ is usually less than that of modern humans (Griffin et al., in press), and great ape metatarsophalangeal joints do not close-pack in extension and therefore may not provide sufficient stability in dorsiflexion for bearing weight (Susman and de Ruiter, 2004). Secondly, it is expected that the modern human metatarsal heads will show greater anisotropy than those of the great apes, especially in the dorsal region of the head because modern humans are habitual bipeds, and they exhibit a more consistent pattern of forefoot posture during gait (Elftman and Manter, 1935; Susman, 1983; Vereecke et al., 2003; Griffin, 2009). Great apes exhibit a more diverse positional behavior than modern humans (Tuttle, 1970; Doran, 1996), and therefore it is predicted that a behavioral repertoire (e.g., climbing, suspension, quadrupedalism) with less stereotypical loading in the MTPJ 1 and MTPJ 2 will result in less trabecular anisotropy compared with the condition in modern human metatarsals. Materials The sample consists of modern human and extant great ape first and second metatarsals. The modern human sample is composed of males and females from the Libben Collection (n ¼ 11); these individuals represent a minimally shod group. The Libben Collection is a well-preserved Native American skeletal assemblage from the Late Woodland Period (800e1100 AD) (Lovejoy et al., 1977). These individuals likely went unshod (Trinkaus, 1975), and if footwear (i.e., moccasins and sandals) was used, it would have been soft and conformed to the substrate (Trinkaus, 1975; Trinkaus and Hilton, 1996). Three other modern human specimens come from The Huntington Collection which consists of 19the20th century individuals who died in the United States of America. It is assumed these individuals went habitually shod. This collection is housed at the National Museum of Natural History (NMNH), Smithsonian Institution in Washington, DC. Most of the wild-collected great ape sample comes from the NMNH. The sample includes males and females 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 Tervuren, Belgium, with the exception of one male individual who was not wild-collected. This male individual was born in the wild and brought into captivity at the age of 2. He died at around age 30 in the Animal Park Planckendael in Muizen, Belgium. For each sample, only adults were included, and when age was not available specimens were chosen based on epiphyseal fusion of the long bones of the fore- and hindlimb. Also, when the option was

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available, right elements were selected and both the first and second metatarsals were chosen from the same individual. Methods Defining anatomical orientation Before scanning, each bone was prepared with three markers to record the anatomical orientation. It was necessary to establish anatomical orientation because only the metatarsal head and a small part of the diaphysis of each bone were scanned. By designating axes using a marker system, anatomical orientation could be easily established during analysis. Garnet stones (less than 1 mm) embedded in wax were used as the anatomical markers. Below are the descriptions of the marker placements for the first and second metatarsal heads: MT1 (Fig. 1a) The bone was placed on a graph paper support with its long axis positioned along one line on the paper. The intersesamoidal ridge of the metatarsal head rested on the line, and the medial and plantar tubercles rested in the same plane. In most cases, clay was used to secure this position. The first marker was then placed at the maximum medial extension of the dorsal edge of the head’s articular surface. Using a ruler and referring to the graph paper support, the lateral marker was placed at the most lateral extension of the head on the dorsal edge of the articular surface at the same height as the medial marker and on the coordinate so that along with the dorsal marker and the medial marker it formed a line perpendicular to the longitudinal axis of the bone. The third marker, used to designate the transverse plane, was placed on the dorsal 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 proximal articular surface on one line marked on the paper. Then the longitudinal axis of the bone was set along this line. The medial marker was placed at the maximum medial extension of the head on the dorsal edge of the articular surface. Using a ruler and referring to the graph support, the lateral marker was placed at the most lateral extension of the head on the dorsal edge of the articular surface at the same height as the medial marker to designate

the medio-lateral axis perpendicular to the bone’s longitudinal axis. The third marker, used to designate the transverse plane, was placed on the dorsal surface midway between the first and second markers. Scanning procedures All specimens except the wild-caught sample of bonobos were scanned at the High-Resolution X-ray Computed Tomography Facility (HRXCT) at the University of Texas at Austin (www.ctlab. geo.utexas.edu). Metatarsals were mounted in a vertical position and elements from the same individual were scanned together as a set. Only the distal ends of the metatarsals (i.e., each head and a small portion of the shaft) were scanned. MT sets were scanned with a source energy ranging from 180 to 200 kV, at a current of 0.11 mA, and with serial cross-sectional slice resolution and spacing of 0.049 mm. Scans were collected with 1400 projections, two 0.067s frames per projection, and 25 slices per rotation. The field of view was 46mm. Data files were produced as 1024  1024 16-bit TIFF files, and were subsequently converted to 8-bit TIFF files with no impact on resolution. Conversions were completed using a code (written by RK) in the Interactive Data Language (IDL) 7.0 (Research Systems, Inc.). Since specimens were scanned in sets, each bone was cropped in ImageJ (http://rsb.info.nih.gov/ij/download.html). The bonobo sample from the Royal Museum for Central Africa could not be shipped to HRXCT facility for scanning, and therefore scanning was completed locally at the University of Antwerp’s Micro CT Research Group Facility (http://webh01.ua.ac.be/mct/ index.htm). Each specimen was placed in a horizontal position on the object bed. Specimens were scanned individually, and with a source energy of 100 kV and a serial cross-sectional slice resolution and spacing of 0.035 mm. Consistent with the scanning procedure at HRXCT, only the metatarsal head and part of shaft were scanned. Data files were provided in 1024  1024 8-bit bitmap format and were then converted to 8-bit TIFFs using ImageJ. It was possible to scan the captive bonobo’s second metatarsal at HRXCT and using the Skyscan machine. The HRXCT and Skyscan scanners have different configurations, and scanning the same bone using both machines provided the opportunity to make the Pan paniscus sample more comparable with the rest of the sample for analysis. Trabecular bone analyses

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

The program Quant3D (Ketcham and Ryan, 2004) was used to reconstruct the three-dimensional structure of each metatarsal head region and serve as a platform for measuring magnitude, directionality, and bone volume fraction of trabeculae. Each specimen’s 8-bit TIFF stack of scan slices was opened directly into Quant3D. The coordinates of each of the three garnet stones markers were used to adjust the anatomical axes provided in the program to anatomical markers indicating orientation for each specimen. For the purpose of studying the regional variation within a metatarsal head, three volumes of interest (VOI) were chosen to represent the dorsal, central, and plantar regions. The three VOIs were arranged along the midline of the long axis of the joint surface (Fig. 2). The Dorsal VOI was placed in an area just distal to the articular margin of the joint on the dorsum of the head. For a few great ape specimens, the dorsal region was especially small and mediolaterally constricted, therefore the VOI was positioned to encompass part of the area past the joint surface on the dorsum of the head. The Central VOI was placed at the most central part of the joint facet and as close to the distal end as possible without picking up cortex. In many of the great ape specimens, the

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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 (lateral region 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 joint surface 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 were set 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 predetermined dorsoplantar axis as for MT 1.

trabeculae were very dense in the center of the joint and the cortical-cancellous boundary was difficult to distinguish. As a result, some Central VOIs were positioned slightly further back proximally to ensure that only trabecular bone was selected. The Plantar VOI was placed in the area distal to the edge where the articular surface ends on the plantar aspect of the bone. In attempt to select homologous VOIs in specimens of varying metatarsal joint sizes, the first and second metatarsal VOIs were each scaled by a measurement of size of the distal joint. This size variable consisted of two measurements using digital calipers taken in the anatomical orientation set by the garnet stone markers (Fig. 1). The dorsoplantar (DP) height was obtained by setting one tip of the caliper along the most dorsal margin of the metatarsal head joint surface and the other tip along the most plantar margin of the metatarsal joint surface. The mediolateral (ML) breadth was measured as the length between the most medial and the most lateral projection of the head. VOI radii (voxels) of MT 1 and MT 2 were determined by the following equations:

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

First, the two joint measurements are averaged. Then the average is divided by three, an arbitrary number chosen after surveying the smallest and largest metatarsal heads in the entire sample. The survey indicated that this scaling measure allowed for three VOIs to fit within a metatarsal head without excessive overlap. It must be noted that the scaling described above is based on the HRXCT sample. Since the bonobo sample was scanned at a different resolution than the HRXCT sample (0.035 mm vs. 0.049 mm), an extra step was taken to scale each bonobo specimen. After averaging, the scaled bonobo VOI was then multiplied by the resolution ratio (0.049 mm/0.035 mm) for the final scaled VOI. The following equation determined the scaled VOI for a bonobo specimen:

Scaled VOI radius in voxelsðPan paniscus sample scanned with SkyscanÞ ¼ ½ðML breadthðmmÞ þ DP heightðmmÞÞ=6  ½0:049 mm=0:035 mm: The VOI radii (voxels) are reported as VOI diameters (mm) in Table 1. The MT 1 VOI diameters range from 2.9 mm (Pongo pygmaeus) to 7.8 mm (Homo sapiens), while the MT 2 VOI diameters

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Table 1 Volume of Interest (VOI) Size Distributions. Taxon

Scaled VOI (millimeters) MT 1

Homo sapiens Pan troglodytes Pan paniscus Gorilla gorilla Pongo pygmaeus

MT 2

Mean

Range

Stdev

Mean

Range

Stdev

6.8a 5.0 4.6 5.9 3.9b

5.8e7.8 4.6e5.4 4.2e4.9 5.0e6.7 2.9e4.7

0.58 0.27 0.30 0.68 0.55

4.3 4.3c 4.2d 5.2e 5.3

3.5e4.8 3.4e4.7 3.8e4.5 4.0e5.9 4.2e6.3

0.36 0.41 0.23 0.66 0.63

a One specimen’s Plantar VOI was reduced from 5.9 to 4.9 to avoid the selection of cortical bone. This reduced VOI value was not included in the generation of the summary statistics above. b One specimen’s Plantar VOI was reduced from 4.7 to 4.1 to avoid the selection of cortical bone. This reduced VOI value was not included in the generation of the summary statistics above. c Three separate specimens VOIs (3.8, 4.2, 4.6) were reduced (3.4, 3.9, 4.4) to avoid the 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 of cortical bone.

range from 3.4 mm (Pan troglodytes) to 6.3 mm (Pongo pygmaeus). Several VOI diameters were reduced in order to avoid the selection of cortical bone in the dorsal or central region (Table 1). It should be noted that the smaller MT 1 VOIs which belong to Pongo pygmaeus do not capture more than 3 trabecular struts within the central slice of the VOI (Fig. 3). Therefore, it is possible that the continuum assumption of bone which posits that material properties are continuously distributed without discrete local variations at the sub-structural level (Hoffler et al., 2000) has been violated. One standard is that the minimum dimension of the specimen (e.g., the VOI) be significantly larger than the dimension of its structural subunits (e.g., the individual plates or rods of trabecular bone) (An, 2000). Harrigan et al. (1988) study suggests that the VOI should be large enough to encompass more than five trabeculae, or the continuum assumption may not be upheld. While this serves as a caveat, the VOIs were not made larger for two reasons. First and foremost, the Pongo MT 1s exhibit a thick cortex across the dorsal region (Fig. 3). This limits the size of the VOI that can fit in the dorsal region of the head. Originally, the specimen with the smallest VOI of 2.9 mm (Table 3) was calculated to have a VOI of 3.2 mm. If 3.2 mm had been used, cortical bone would have then been 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 their Dorsal VOIs, but the next smallest VOIs of 3.8 mm contains five in its 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 trabecular struts were present in the Dorsal VOI. Each HRXCT VOI was separately thresholded using an iterative segmentation algorithm (Ridler and Calvard, 1978; Trussell, 1979). In order to make the Skyscan scan sample more comparable with the HRXCT sample, a different method of thresholding was used. The iterative segmentation algorithm procedure presumes that there are two components in the image, each fully represented in the image histogram as a roughly normal (bell-shaped) distribution of gray values. The Skyscan scans were reconstructed using defaults such that much of the air had negative values, which were then raised to zero due to the limitations of the graphics file format in which they were stored (unsigned 16-bit TIFF). This results in a “clean”, flat-looking background, and seemingly crisper edges for solid objects, but corrupts the data with respect to the thresholding algorithm. Rather than being normal, the distribution of air values is truncated, and the mean value of air is effectively raised due to the increments added to all negative voxels. This in turn leads the iterative algorithm to select a threshold value that is arbitrarily higher than it would have been had the air not been truncated, in turn artificially lowering the BV/TV. To avoid this, a single threshold was used for the entire Skyscan dataset based on the MT 2 of the captive Pan paniscus that had been scanned by both machines. First the HRXCT dataset of the captive specimen was imported into Quant3D. The largest possible Central VOI was selected, the iterative segmentation method was selected, a threshold value was selected and the generated BV/TV (0.51) was recorded. Then the Skyscan dataset of the same specimen was imported, the scaled “largest possible Central VOI” was selected and a threshold was chosen to result in a BV/TV of 0.51, making it more compatible with the HRXCT dataset. The resulting threshold was recorded and used for the rest of the Pan paniscus sample, which we judged acceptable because of the similar sizes of the specimens and consistent gray levels for cortical bone. For the entire sample, trabecular bone properties were quantified using the star volume distribution method (SVD) (Cruz-Orive et al., 1992; Karlsson and Cruz-Orive, 1993; Ketcham and Ryan, 2004; Ryan and Krovitz, 2006). Each SVD calculation was programmed to run with 2,049 uniformly distributed orientations at 8,000 random points placed within the bone phase. From each point, the SVD calculation extends very minute cones in various

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 be 3.2 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.

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Table 2 MT 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) Habitually shod (2,1) Minimally shod (5,5) Pan troglodytes (3,6) Pan paniscus (3,5) Gorilla gorilla (5,3) Pongo pygmaeus (5,5)

13 3 10 9 8 8 10

0.42 0.42 0.42 0.50 0.51 0.44 0.39

0.37 0.38 0.37 0.41 0.43 0.37 0.28

0.47 0.46 0.47 0.61 0.65 0.50 0.49

0.038 0.044 0.038 0.067 0.06 0.05 0.06

6.9 5.8 7.3 3.6 3.8 4.1 3.5

3.7 3.9 3.7 1.7 2.2 1.7 2.0

10.7 9.5 10.7 5.2 5.9 6.9 11.3

2.5 3.2 2.4 1.1 1.2 1.8 2.8

Central

Homo sapiens (7,6) Habitually shod (2,1) Minimally shod (5,5) Pan troglodytes (3,6) Pan paniscus (3,5) Gorilla gorilla (5,3) Pongo pygmaeus (5,5)

13 3 10 9 8 8 10

0.38 0.40 0.38 0.51 0.51 0.49 0.47

0.30 0.37 0.30 0.42 0.43 0.42 0.40

0.45 0.43 0.45 0.58 0.69 0.57 0.53

0.04 0.03 0.05 0.05 0.08 0.05 0.05

5.6 7.8 5.0 2.6 3.8 3.8 2.0

2.6 5.3 2.6 1.7 2.2 2.0 1.4

11.2 11.2 8.8 3.7 7.2 6.5 2.4

2.6 3.1 2.2 0.7 1.6 1.6 0.4

Plantar

Homo sapiens (7,6) Habitually shod (2,1) Minimally shod (5,5) Pan troglodytes (3,6) Pan paniscus (3,5) Gorilla gorilla (5,3) Pongo pygmaeus (5,5)

13 3 10 9 8 8 10

0.30 0.30 0.31 0.46 0.45 0.41 0.41

0.23 0.27 0.23 0.41 0.37 0.35 0.32

0.39 0.32 0.39 0.51 0.61 0.49 0.52

0.04 0.03 0.05 0.03 0.07 0.046 0.057

4.3 7.3 3.4 2.3 3.9 3.5 2.6

1.7 3.9 1.7 1.7 2.0 2.4 1.3

11.0 11.0 5.7 3.7 5.5 6.0 6.5

2.5 3.6 1.4 0.6 1.2 1.1 1.5

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

directions within the bone until a bone-marrow interface is reached. The vertex of each cone originates from each point. The volumes of the cones are then used to reconstruct the magnitudes (eigenvalues) and principal component directions (eigenvectors) of each VOI. Properties of trabecular bone fabric structure were s 1 ; bs 2 ; bs 3 Þ. This study focuses on generated from the eigenvalues ðb s 1 =bs 3 Þ. Finally, eigenvectors (û1, the variable DA, which is equal to ðb û2, û3) were used to generate stereographic projections, which illustrate the trabecular bone fabric structure of the VOI in reference to established anatomical axes (x, mediolateral; y, dorsoplantar; z, proximodistal).

Statistical procedures Before exploring interspecific differences for each metatarsal, comparisons of trabecular bone properties were made between habitually shod (Huntington Collection) and minimally shod (Libben Collection) modern human samples. Mann-Whitney U tests were run to test for differences in BV/TV and DA, between these human samples. Also, the values of the captive bonobo were checked for overlap with the wild sample of Pan paniscus. Taxonomic differences in absolute values for bone volume fraction and degree of anisotropy were tested using the Mann-

Table 3 MT 2 summary statistics. VOI

Taxon

N

Bone Volume Fraction (BV/TV)

Degree of Anisotropy (DA) Mean

Min

Max

SD

Dorsal

Homo sapiens (7,6) Habitually shod (2,1) Minimally shod (5,5) Pan troglodytes (4,6) Pan paniscus (4,5) Gorilla gorilla (5,3) Pongo pygmaeus (5,5)

13 3 10 10 9 8 10

0.36 0.37 0.36 0.46 0.44 0.42 0.30

0.29 0.35 0.29 0.42 0.35 0.35 0.24

0.45 0.39 0.45 0.54 0.52 0.51 0.41

0.038 0.019 0.042 0.037 0.05 0.05 0.05

8.4 11.0 7.6 2.2 2.2 2.9 2.7

4.4 7.8 4.4 1.5 1.7 1.6 1.9

16.0 16.0 13.0 4.1 2.8 4.1 5.5

3.3 4.4 2.8 0.8 0.36 1.00 1.05

Central

Homo sapiens (7,6) Habitually shod (2,1) Minimally shod (5,5) Pan troglodytes (4,6) Pan paniscus (4,5) Gorilla gorilla (5,3) Pongo pygmaeus (5,5)

13 3 10 10 9 8 10

0.35 0.31 0.36 0.46 0.49 0.46 0.45

0.28 0.28 0.28 0.42 0.39 0.38 0.39

0.40 0.36 0.40 0.51 0.59 0.58 0.50

0.05 0.05 0.04 0.03 0.06 0.07 0.03

6.7 10.3 5.6 2.1 2.4 2.6 2.5

3.0 7.7 3.0 1.3 2.0 1.8 1.5

14.2 14.2 9.3 3.7 3.3 4.3 3.1

3.10 3.39 2.15 0.65 0.38 0.84 0.47

Plantar

Homo sapiens (7,6) Habitually shod (2,1) Minimally shod (5,5) Pan troglodytes (4,6) Pan paniscus (4,5) Gorilla gorilla (5,3) Pongo pygmaeus (5,5)

13 3 10 10 9 8 10

0.28 0.29 0.28 0.41 0.38 0.35 0.35

0.23 0.26 0.23 0.38 0.35 0.24 0.28

0.35 0.32 0.35 0.46 0.44 0.50 0.40

0.04 0.03 0.04 0.03 0.02 0.086 0.047

4.5 3.5 4.8 2.5 2.6 2.3 2.7

2.9 2.9 3.2 1.5 1.8 1.7 1.6

8.5 4.3 8.5 3.6 3.5 2.7 5.0

1.85 0.76 2.00 0.56 0.49 0.30 1.0

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

Mean

Min

Max

SD

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Table 4 Mann-Whitney U Test p-values for habitually shod human and habitually unshod human comparisons. Trabecular Bone Property

Metatarsal One

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

Metatarsal Two

Dorsal VOI

Dorsal Central Plantar Dorsal Central Plantar

Bone Volume Fraction (BV/TV) 1.00 Anisotropy (DA) 0.37

0.94 0.22

0.81 0.077

0.47 0.16

0.16 0.028

0.57 0.16

Whitney U test, with a p-value of 0.05 taken as a measure of significance. There were several comparisons made between humans and each great ape taxon, (i.e., at least 8 tests for each MT  VOI), therefore the Dunn-Sidák method (Sokal and Rohlf, 1995) was used to reduce the probability of making a type 1 error. The Dorsal VOI comparisons between humans and all the great apes were not subject to this correction because they directly test the main hypothesis. Box plots were generated to compare the pattern of averages for a given value (i.e., BV/TV or DA) for the three VOIs per taxon to explore regional differences within a metatarsal head. Wilcoxon Matched Pairs tests were run to assess regional differences (Dorsal vs. Plantar VOI per taxon). Only the Dorsal and Plantar VOIs were compared because in many cases either or both the Dorsal and Plantar VOI overlapped in varying degrees with the Central VOI. Results As predicted, in modern human MT heads, the highest mean bone volume fraction values occur in the dorsal region; the modern human metatarsal heads tend to be generally more anisotropic than those of the great apes (Tables 2 and 3). The habitually shod and minimally shod samples correspond well with each other, and only one significant difference was found between the two groups (Table 4). The habitually shod sample has a significantly larger DA for the MT 2 Central VOI (p-value ¼ 0.028). Because there was only one significant difference out of twelve comparisons, these two samples were pooled together to form one sample for the interspecific comparisons. Regarding the captive and wild bonobo comparisons, all of the captive bonobos’ trabecular bone property values overlapped with ranges of values for the wild-caught bonobos (Table 5). Therefore, the captive bonobo was included as part of the wild-caught bonobo sample for all the following interspecific comparisons. Overall, the Mann-Whitney U-tests indicate that for the comparisons between modern humans and each great ape taxon, modern humans usually have less bone volume fraction and more anisotropy for each VOI type (Table 6). Significant differences in MT 1 BV/TV are found for taxonomic comparisons under all VOIs, especially MT 1 Central and Plantar VOIs. Regarding DA, modern human VOIs usually have larger values than corresponding great ape VOIs, but this is only significant for most of the Dorsal VOI and two Central VOI comparisons. It should be noted that the specimen with the largest MT 1 DA for the Dorsal VOI is not a modern human specimen, but an orangutan specimen (Table 2). This specimen also has the smallest BV/TV. It is likely that, as a consequence of

BV/TV

DA

sapiens sapiens sapiens sapiens sapiens

vs. vs. vs. vs. vs.

Hominids Pan troglodytes Pan paniscus Gorilla gorilla Pongo pygmaeus

L0.05 L0.0026 L0.00066 0.37 0.34

0.000026 0.0014 0.0025 0.020 0.00064

Central VOI Homo sapiens Homo sapiens Homo sapiens Homo sapiens

vs. vs. vs. vs.

Pan troglodytes Pan paniscus Gorilla gorilla Pongo pygmaeus

L0.000016 L0.000039 L0.000069 L0.000079

0.00039 0.089 0.076 0.0000020

Plantar VOI Homo sapiens Homo sapiens Homo sapiens Homo sapiens

vs. vs. vs. vs.

Pan troglodytes Pan paniscus Gorilla gorilla Pongo pygmaeus

L0.0000040 L0.000020 L0.00030 L0.00017

Metatarsal Two Dorsal VOI Homo sapiens vs. Homo sapiens vs. Homo sapiens vs. Homo sapiens vs. Homo sapiens vs.

Hominids Pan troglodytes Pan paniscus Gorilla gorilla Pongo pygmaeus

L0.040 L0.000021 L0.0019 L0.020 0.0041

3.9E-11 0.0000020 0.00000040 0.000010 0.000012

Central VOI Homo sapiens Homo sapiens Homo sapiens Homo sapiens

vs. vs. vs. vs.

Pan troglodytes Pan paniscus Gorilla gorilla Pongo pygmaeus

L0.0000020 L0.000028 L0.00030 L0.000012

0.000012 0.000016 0.00012 0.0000035

Plantar VOI Homo sapiens Homo sapiens Homo sapiens Homo sapiens

vs. vs. vs. vs.

Pan troglodytes Pan paniscus Gorilla gorilla Pongo pygmaeus

L0.0000020 L0.0000040 0.53 L0.0050

0.00017 0.000076 0.00000983 0.00086

Homo Homo Homo Homo Homo

0.017 0.97 0.75 0.036

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

capturing an exceptionally small amount of trabecular bone in a VOI, if two or three struts are present and show a similar preference 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 comparisons reveal that modern human second metatarsal VOIs have significantly lower BV/TV values than great ape VOIs (Table 6). For all MT 2 comparisons, modern humans have significantly greater DA than all the great apes, (Table 6). In sum, not only do modern humans have Dorsal VOIs that are on average more anisotropic than hominid Dorsal VOIs, modern human Central and Plantar VOIs also tend to be more anisotropic as well, with the exception of the MT 1 Plantar VOI comparison between humans and bonobos. Modern humans are distinct from all the great apes except bonobos in regional differences in trabecular architecture for the MT 1 except the Dorsal VOI has a significantly greater bone volume

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

Dorsal VOI BV/TV

Captive Pan paniscus (n ¼ 1) Wild caught Pan paniscus value range (n ¼ 8)

0.48 (0.35e0.52)

DA 2.2 (1.75e2.85)

Central VOI BV/TV 0.53 (0.39e0.58)

DA 2.6 (1.97e3.28)

Plantar VOI BV/TV 0.39 (0.35e0.44)

DA 2.9 (1.8e3.5)

N.L. Griffin et al. / Journal of Human Evolution 59 (2010) 202e213 Table 7 Wilcoxon Matched Pairs Test p-values of Dorsal and Plantar VOI comparisons. Taxon

MT 1 Dorsal VOI vs. Plantar VOI

MT 2 Dorsal VOI vs. Plantar VOI

Homo sapiens BV/TV DA

0.0015 0.016

0.0015 0.011

Pan troglodytes BV/TV DA

0.110 0.028

0.017 0.24

Pan paniscus BV/TV DA

0.012 0.57

0.011 0.086

Gorilla gorilla BV/TV DA

0.069 0.48

0.036 0.16

Pongo pygmaeus BV/TV DA

0.39 0.093

0.059 0.72

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

fraction than the Plantar VOI (Table 7, Fig. 4a). If the complete regional pattern, including the Central VOI is considered, modern human MT1s are differentiated from chimpanzees, gorillas, and orangutans (Fig. 4). While the modern human pattern shows a decrease in the mean value of BV/TV from the dorsal to plantar region, the three great ape taxa show an increase in mean BV/TV

209

from the Dorsal VOI to the Central VOI and then a decrease in mean BV/TV from the Central VOI to the Plantar VOI. The mean values of the Dorsal and Central VOIs are the same for the bonobos. Orangutans show a unique pattern in that the Plantar VOI has a slightly larger mean than the Dorsal VOI. In modern humans, the degree of anisotropy in the first metatarsal follows the same regional pattern as bone volume fraction, with a significant decrease from the dorsal to plantar region (pvalue ¼ 0.015, Table 7, Fig. 4b). Chimpanzees are the only other taxon that shows a significant difference between the Dorsal and Plantar VOIs (p-value ¼ 0.028, Table 7). Gorillas show the same pattern, but the difference between the Dorsal and Plantar VOI is not significant. Orangutans show a unique pattern in which DA decreases from the Dorsal VOI to Central VOI, and the Plantar VOI has a larger mean DA value than that for the Central VOI. The modern human MT 2 pattern is the same pattern as the MT 1, with significantly lower BV/TV values than the apes in most comparisons (Table 6) and a significant decrease in BV/TV from the dorsal to plantar regions of the head (p-value ¼ 0.0015, Tables 7, Fig. 4c). All African great apes show the same statistically significant pattern as modern humans, but the orangutan Dorsal VOI shows the opposite pattern and only approaches significance. Bonobos, gorillas, and orangutans are each distinct from modern humans in that their Central VOIs have the largest mean values of BV/TV compared to their respective Dorsal and Plantar VOIs. Orangutans again show a unique pattern in that the Plantar VOI has a larger mean than the Dorsal VOI.

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 Plantar VOI. 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 VOI and 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 unique pattern 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 the Dorsal 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 MT 2 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 shows a slight increase in mean DA from the Dorsal to Plantar VOI.

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The measurement of the degree of anisotropy in the second metatarsal also distinguishes the modern humans from the great apes (Table 7, Fig. 4d). To the exclusion of the great apes, the dorsal region of the modern human metatarsal head shows significantly more organization than the more plantar regions. Gorillas are the only great ape taxon that hints at a similar pattern of regional anisotropy, but for this taxon, the Dorsal and Plantar VOIs are not significantly different from each other (Fig. 4d). Chimpanzees and bonobos show a slight, but insignificant, increase in DA from the Dorsal to Plantar VOI. From the Dorsal VOI to the Central VOI in orangutans, the mean DA value decreases from the Dorsal to Central VOI and then for the Plantar VOI, it reaches a comparable mean value to that of the Dorsal VOI. Regional patterns within a MT head partially support the first hypothesis that modern human VOIs have greater relative BV/TV in the dorsal region. Modern humans show this pattern but so do other hominid taxa. There is more support for our second hypothesis. The modern human sample shows the greatest absolute DA, especially in the dorsal region of either the MT 1 or MT 2 head, but only the modern human MT 2 is unique from the great apes in having a Dorsal VOI that has significantly greater DA than the respective Plantar VOI. Overall, the results of the absolute and regional differences of BV/ TV and DA of MT 1 and MT 2 draw attention to a pattern that requires further investigation. Modern human MT VOIs tend to have less trabecular bone per unit volume and this trabecular bone is strongly directed along one or more axes, while great apes tend to show the opposite pattern. If BV/TV and DA are correlated with each other it would be difficult to attribute DA to function if BV/TV is an influential factor or conversely, a BV/TV to function, if DA is an influential factor. To test for a correlation, the Spearman Rank Correlation Coefficient was considered for each VOI separately. BV/TV and DA values of all specimens were included in each test. In four out of six cases, DA is negatively correlated with BV/TV (Fig. 5). However, when the modern human sample is removed and for each MT VOI, no correlation is found in any case. Also, when the human sample is analyzed alone no correlation is found in any case. This evidence suggests that the trabecular bone structure of modern human metatarsals is not a related to a difference in relative bone mass.

trabecular bone of modern humans and great apes. Ruff (1987) found that modern humans tend to have relatively more slender femora and tibiae than modern non-human primates. The present study could not test this finding statistically, although great ape values of trabecular BV/TV in the posterior region of the calcaneus were found to be larger than those of modern humans (Maga et al., 2006). A possible cause for these differences may lie in the trend of an overall increase in gracilization of Homo from the Pleistocene to modern times (Frayer, 1984; Ruff et al., 1993; Ruff, 2002; Walker, 2009). Therefore, examining BV/TV differences in other anatomical regions will reveal whether or not this difference is systemic. Also, testing changes through ontogeny in great apes and modern human metatarsals, as well as sampling MTs from archaic Homo, Neandertals, and early modern humans may help explain differences in trabecular bone volume fraction in extant humans and great apes. In sum, the current comparisons of the modern humans and great ape samples suggest that, compared to BV/TV, DA appears to be more sensitive for distinguishing hominids that engage in habitual metatarsi-fulcrimating bipedal walking from those that do not use the metatarsophalangeal joint for propulsion. This may also correlate with a more diverse locomotor regime among non-bipeds. It remains possible that similarities between humans and apes in bone volume fraction regional variation may be a consequence of interactions between trabecular and cortical bone during growth. For example, if the dorsal region of the cortex thickens in response to the habitual loading during push-off in modern humans, this would relax the need for the trabecular bone volume to change dramatically in the dorsal region. This hypothesis is supported by Muehleman et al. (1999) study showing that the dorsal region of the modern human first metatarsal head shows greater bone mineral density compared to the more plantar portions of the head. As encouraged by Egi et al. (2005), who investigated the regional distribution of both cancellous and cortical bone in the humeri of non-human primates, it may be necessary to combine the analyses of cortical and trabecular bone morphology of the metatarsal head to fully understand why BV/TV is not a clear indicator of differences in loading patterns between modern humans and the great apes.

Discussion

Despite the fact that other hominids share a similar pattern to modern humans with a decrease in bone volume fraction from the dorsal to plantar regions of the metatarsal head, humans differ from the great apes in the degree of anisotropy, especially in the dorsal region. In addition, the human second metatarsal is distinct from all the great ape metatarsals in that the Dorsal VOI has significantly more anisotropy than the Plantar VOI, a pattern similar to the base of the human second proximal phalanx (Griffin, 2008). Principal axes of trabecular fabric structure are currently less informative in distinguishing humans from great apes based on forefoot function. The primary direction of trabecular bone orientation follows the longitudinal axis of the bone in both humans and great apes (Griffin, 2009). Between rays, the direction of the trabecular fabric structure in the human second metatarsal shows a greater dorsoplantar component of the primary eigenvector than the first metatarsal, and this is true for the other great apes too, except orangutans (Griffin, 2009). The slight difference in direction of the first principal axis between the rays is most likely a result of differences in how anatomical orientation was determined for the first and second metatarsals. The MT 1s were set with reference to their heads, while MT 2s were set with reference to their bases. The MT 2 heads, especially those of the great apes are often twisted relative their bases (Lewis, 1989) (Fig. 1), and therefore, trabeculae running proximodistally may not be align with the longitudinal axis set by the base of the metatarsal.

The first hypothesis, that modern human metatarsal heads are unique among the great apes by exhibiting relatively greater bone volume fraction in the dorsal region of the head relative to the more plantar region, receives no support. For both MT 1 and MT 2, the modern human Dorsal VOI has significantly a greater BV/TV value than its respective Plantar VOI (Table 7); however, this is also true for the bonobo sample for MT 1, and for all taxa except orangutans for MT 2. The second hypothesis is more fully supported. Modern humans are not the only taxon that tends to have significantly more anisotropic Dorsal VOIs compared to Plantar VOIs for the first metatarsal because chimpanzees also show this pattern. However, modern human MT 2 heads uniquely show significantly more anisotropy in the dorsal region compared to the plantar region. Also, both modern human metatarsals generally present greater anisotropy compared to all the great ape taxa, as illustrated by the results of the Mann-Whitney U tests (Table 6). Regarding Dorsal VOI, modern human MTs have significantly higher DA than the great apes. Though it is possible that greater BV/TV, especially in the central and plantar regions of the great ape metatarsal heads, may be an indicator of greater overall loading at these joints, it may also reflect systemic differences present in both the cortical bone and

Indications of modern human and great ape forefoot function

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

211

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 great apes. 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. The scatterplots 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. Modern humans, closed squares; chimpanzees, open triangles; bonobos, open circles; gorillas, crosses; orangutans, closed diamonds.

The concentration of trabecular bone in the center of the joint of both metatarsals as reflected by the larger mean value in the Central VOI compared to the Dorsal VOI represents one of the most notable regional patterns in the great ape sample (Fig. 4). For both metatarsals, orangutans separate from the rest of the great apes because the plantar BV/TV mean 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 trabecular bone analysis would make a convincing argument that its owner would have exhibited a modern human-like forefoot function? Because the samples overlap in both absolute DA values and regional

differences in DA, it will be difficult to make predictions about a single specimen if its values consistently fall within the range of overlap between modern humans and great apes. Clearly, a DA value that is within the upper range of the values for the modern human sample would provide the strongest signal in the case of a fossil. Moreover, the following complex of characteristics would also align the fossil with the modern human sample: (1) greater overall anisotropy 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 the central region of the joint. Based on the results of this study, it may be easier to identify a modern human-like functioning MT 2 than MT 1 because the differences between modern humans and great apes for MT 2 DA are more pronounced (Fig. 4).

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Conclusion This study of the comparative trabecular architecture of the heads of first and second metatarsals in extant hominoids supports in vivo functional differences in the modern human and great ape forefoot. In addition to having greater anisotropy and relative bone volume in the dorsal region of both metatarsal heads, the shared patterns of regional bone volume and anisotropy in the first and second metatarsals reinforce the shared-role of the two rays at push-off (Bojsen-Møller, 1979). Bone volume fraction value did not serve to distinguish modern humans fully from the great apes. However, the differences in degree of anisotropy, especially in the dorsal region of the first and second metatarsals of modern human and great apes, are consistent with functional differences. This, in turn, encourages the investigation of early hominin foot bones to help reconstruct forefoot 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 study and their assistance during data collection. Special thanks to Dr. Jessie Maisano at the HRXCT lab for all of her help, Dr. Nora DeClerk for permitting NG and KD to work in her microCT lab facility, and Dr. Christine Wall for providing NG a computer to run part of the analysis. We also extend our appreciation to Dr. Masato Nakatsukasa and Dr. Bernard Wood for reviewing earlier versions of this manuscript. NG would also wish to acknowledge Dr. Daniel Schmitt for his continuous support and guidance. Funding has been provided by the GWU Cotlow Field Research Fund, Sigma Xi Grantin-Aid of Research, L.S.B. Leakey Foundation, the National Science Foundation: BCS-0726124, NSF IGERT DGE-9987590 and DGE0801634, the GWU Selective Excellence Fellowship for Hominid Paleobiology, and Duke University. References An, Y.H., 2000. Mechanical properties of bone. In: An, Y.H., Draughn, R.A. (Eds.), Mechanical Testing of Bone and the Bone-Implant Interface. CRC Press, Boca Raton, pp. 41e85. Bennett, M.R., Harris, J.W., Richmond, B.G., Braun, D.R., Mbua, E., Kiura, P., Olago, D., Kibunjia, M., Omuombo, C., Behrensmeyer, A.K., Huddart, D., Gonzalez, S., 2009. Early hominin foot morphology based on 1.5-million-year-old footprints from Ileret, Kenya. Science 323, 1197e1201. Bojsen-Møller, F., 1979. Calcaneocuboid joint and stability of the longitudinal arch of the foot at high and low gear push off. J. Anat. 129, 165e176. Bojsen-Møller, F., Lamoreux, L., 1979. Significance of free-dorsiflexion of the toes in walking. Acta Orthop. Scand. 50, 471e479. Carlson, K.J., Lublinsky, S., Judex, S., 2008. Do different locomotor modes during growth modulate trabecular architecture in the murine hind limb? Int. Comp. Biol. 48, 385e393. Cruz-Orive, L.M., Karlsson, L.M., Larsen, S.E., Wainschtein, F., 1992. Characterizing anisotropy: a new concept. Micron. Microsc. Acta 23, 75e76. Ding, M., Odgaard, A., Danielsen, C.C., Hvid, I., 2002. Mutual associations among microstructural, physical and mechanical properties of human cancellous bone. J. Bone Jt. Surg. 84-B, 900e907. Doran, D.M., 1996. Comparative positional behavior of the African apes. In: McGrew, W.C., Marchant, L.F., Nishida, T. (Eds.), Great Ape Societies. Cambridge University Press, Cambridge, pp. 213e224. Egi, N., Nakatsukasa, M., Ogihara, N., 2005. Variation in internal structure of distal humerus among small primates. Am. J. Phys. Anthropol. 40 (Suppl.), 99. Elftman, H., Manter, J., 1935. Chimpanzee and human feet in bipedal walking. Am. J. Phys. Anthropol. 20, 69e79. Erdemir, A., Hamel, A.J., Fauth, A.R., Piazza, S.J., Sharkey, N.A., 2004. Dynamic loading of the plantar aponeurosis in walking. J. Bone Jt. Surg. Am. 86-A, 546e552. Fajardo, R.J., Müller, R., Ketcham, R.A., Colbert, M., 2007. Nonhuman anthropoid primate femoral neck trabecular architecture and its relationship to locomotor mode. Anat. Rec. (Hoboken) 290, 422e436. Fajardo, R.J., Müller, R., 2001. Three-dimensional analysis of nonhuman primate trabecular architecture using micro-computed tomography. Am. J. Phys. Anthropol. 115, 327e336.

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