AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 000:000000 (2010)

The Importance of Accounting for the Area of the Medullary Cavity in Cross-Sectional Geometry: A Test Based on the Femoral Midshaft
V.S. Sparacello* and O.M. Pearson
Department of Anthropology, University of New Mexico, Albuquerque, NM 87131-0001 KEY WORDS bone mechanical properties; periosteal CSG; external dimensions detect the difference 90% of the time via a t-test. Moreover, endosteal area can be predictedalthough with substantial errorfrom periosteal area. Despite this error, including this relationship in subperiosteally derived estimates of J produces sample mean estimates close to true mean values. Power analyses reveal that when similar samples are used to develop prediction equations, a minimum sample of hundreds or more may be needed to distinguish a predicted mean J from the true mean J. These results further justify the use of regression equations estimating J from periosteal contours when analyzing behaviorally induced changes in bone rigidity in ancient populations, when it is not possible to measure endosteal dimensions. However, in other situations involving comparisons of individual values, growth trends, and senescence, where relative cortical thickness may vary greatly, inclusion of endosteal dimensions is still important. Am J Phys Anthropol 000:000000, 2010. V 2010 Wiley-Liss, Inc.
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ABSTRACT In cross-sectional geometric (CSG) studies, both the subperiosteal and endosteal contours are considered important factors in determining bone bending rigidity. Recently, regression equations predicting CSG properties from a sections external dimensions were developed in a world-wide sample of human long bones. The results showed high correlations between some subperiosteally derived and actual CSG parameters. We present a theoretical model that further explores the inuence of endosteal dimensions on CSG properties. We compare two hypothetical femoral midshaft samples with the same total subperiosteal area but with percentages of cortical bone at the opposite ends of published human variation for population sample means. Even in this relatively uncommon scenario, the difference between the samples in the resultant means for predicted femoral polar second moment of area (J) appears to be modest: power analysis indicates that a minimum sample size of 61 is needed to

The study of long bone robusticity through cross-sectional geometry (CSG) is based on the widely accepted notion that bone tissue responds dynamically to stresses and strains to optimize itself to its mechanical environment. According to what is loosely referred to as Wolff s Law, bone tissue is deposited in the shafts cross section in response to mechanical loads that surpass a specic level of strain, or, if high strains are not encountered, bone is resorbed, until the remaining bone occasionally experiences strain within the acceptable levels (Lovejoy et al., 1976; Lazenby, 1990; Pearson and Lieberman, 2004; Ruff et al., 2006). Although the complexity of the factors inuencing bone robusticity should always be taken into account when interpreting CSG results (Pearson and Lieberman, 2004), it is generally presumed that the form of an adult bones section somehow reects its loading history. Following this rationale, CSG has been used to draw behavioral inferences in human and nonhuman primates (e.g., Marchi, 2005, 2007; Carlson et al., 2008) and to assess diachronic changes in robusticity of the genus Homo (Ruff et al., 1993). The integration of quantitative data derived from CSG with ethnographic and archaeological information has proven to be a powerful tool in reconstructing the physical and behavioral environment of past and recent populations and to make inferences about their subsistence strategies, mobility levels, and other habitual activities (e.g., Bridges, 1985, 1989, 1996; Ruff, 1987, 1999, 2000; Collier, 1989, 1993; Churchill et al., 1996, 2000; Larsen, 1997; Ledger et al., 2000; Stock and Pfeiffer, 2001, 2004;
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Holt, 2003; Marchi et al., 2006; Sladek et al., 2006a,b, 2007; Carlson et al., 2007; Sparacello and Marchi, 2008). Cross-sectional geometry analyzes bone shafts by applying engineering-derived beam theory. Second moments of area (SMA) with respect to various axes and the polar second moment of area are calculated from the distribution of cortical tissue about the shaft sections centroid (Lovejoy et al., 1976; Ruff and Hayes, 1983; Larsen, 1997). The calculation of biomechanical properties traditionally relies upon an accurate determination of periosteal and endosteal contours of the diaphysis (Ruff et al., 1999). To avoid direct sectioning, noninvasive methods are commonly used to reconstruct the cross section, including computed tomography (CT scans) and the latex cast method (LCM), which uses a combination of silicone moulds and biplanar radiographs. This LCM method provides a reliable estimate of cross-section contours to the point that CSG data obtained in this way need not be corrected before comparison with data

*Correspondence to: Vitale Stefano Sparacello, Department of Anthropology, MSC01-1040, 1 University of New Mexico, Albuquerque, NM 87131-0001. E-mail: Vito@unm.edu Received 24 December 2009; accepted 24 May 2010 DOI 10.1002/ajpa.21361 Published online in Wiley InterScience (www.interscience.wiley.com).

WILEY-LISS, INC.

V.S. SPARACELLO AND O.M. PEARSON nutritional factors (Ruff et al., 1993; Mays et al., 2009). Moreover, differences in physical activity may contribute to variation in cortical thickness given the same TA because elevated levels of physical activity may promote medullary stenosis (Ruff et al., 1991, 1994, 2006). The second step assesses the degree of error involved in correcting periosteally derived J using regression equations predicting MA from TA. In research using this method, the regression equation predicting MA from TA would be based on a sample different from the one under analysis. We will therefore test the method using two different regression equations on a control sample composed of direct sectioned bones. One equation is derived from a sample with relative cortical thickness statistically indistinguishable from the control sample; the other is derived from a sample with signicantly different cortical thickness. The degree of error involved in using this method will inform on the importance of using a regression to correct periosteal J from a sample similar to the one under study, rather than from a sample that may be genetically distant, or had different nutritional and health environments. The third step analyzes the effectiveness of using regression equations predicting actual J and the shape index Imax/Imin from their periosteal counterparts in comparisons aimed at the reconstruction of habitual behavior. The reason we introduce in this step an empirical verication of the possibility of estimating the CSG shape is that the applicability of the regression method cannot be theoretically demonstrated for sections departing from circularity, and consequently for the individual SMAs (i.e., Ix, Iy, Imax, Imin, and their ratios). It is expected that the estimates of these properties will be less accurate and systematically biased. We consider two samples that are geographically, temporally, and genetically close and apply regression equations developed on one to estimate SMA in the other. We determine the error this approach entails and assess if using different regression equations (derived from different long bones, the opposite sex, or different time periods) leads to substantially different results.

derived from CT scans (Stock, 2002; ONeill and Ruff, 2004). As noted by Stock and Shaw (2007), several drawbacks restrict the application of noninvasive methods. These include the cost and the occasionally problematic quality of CT and X-rays scans when machines are not well-calibrated or the radiographer has little experience in imaging dry bone. Moreover, in some research locations imaging facilities may be distant from museums, making the transportation of fragile specimens inadvisable. These problems could be circumvented if an accurate reconstruction of the medullary cavity is not necessary to obtain reliable CSG data. Thus, past research explored the relationship between the external dimensions of the diaphysis and CSG properties. Pearson (2000) found a correlation of R2 5 0.898 between predicted J (polar second moment of area, also commonly used as a measure of average bending rigidity) and external diameters at midshaft of 137 human femora (see also Pearson et al., 2006). Regarding the relationship between the CSG shape index (Ix/Iy) and external diameters anteroposterior/ mediolateral (AP/ML), Rockhold (1988) found a relationship of R2 5 0.762, and Wescott (2001) of R2 5 0.829. Stock and Shaw (2007) predicted CSG properties from a sections external dimensions (diameters, circumference, subperiosteal area, and periosteal Imax/Imin and Ix/Iy), in a world-wide sample of human long bones. Their results demonstrated highly predictable relationships between total subperiosteal area (TA) and J in various bones, with R2 values ranging from 0.959 at the subtrochanteric level of the femur to 0.996 in midshaft radius, and R2 5 0.989 at femoral midshaft. Prediction errors fell within the range of error generally accepted in modeling CSG using the LCM method (Stock, 2002; ONeill and Ruff, 2004). Stock and Shaw suggested that when direct sectioning, CT scanning, and radiography are unavailable, an accurate measurement of the TA of the section provides the best externally based method of evaluating J for all bones. These results may have great methodological importance. If the measure of TA obtained through periosteal moulds provides an accurate estimate of bending rigidity, then determining the size of the medullary cavity would become less essential. If so, CSG studies could become faster and less expensive, applicable to more samples, and feasible for more researchers. The purpose of this article is to assess whether an accurate reconstruction of the medullary area (MA) is necessary in a particular kind of CSG study: comparison of sample means as commonly practiced in studies of change in inferred patterns of habitual activity. This study involves three steps, the rst highly idealized and theoretical, the next two increasingly closer to the kind of studies that might benet from the use of regression equations to estimate actual CSG, especially SMA, from periosteal CSG. First, we estimate a maximum error entailed by simply ignoring the effect of normal variation in the size the medullary cavity area when comparing sample means of two simulated populations. Each population is constrained to have the same TA but with cortical thickness at the opposite extremes of variation of published, nonpathological human populations. This provides an initial indication of how important it is to take into account the differences in mean cortical thickness is when comparing populations. Groups may differ in mean cortical thickness due to genetic, health, age-related bone loss, and American Journal of Physical Anthropology

MATERIALS
This analysis focuses on the femoral midshaft, in large part due to the large amount of data we have collected on femoral sections and the substantial amount of comparative data in the literature. In the discussion section, we address whether the results could be extended to other long bones. Data on femoral CSG parameters relevant to this study (percent cortical area, %CA, and average bending rigidity, J) were assembled from relevant studies of Late Pleistocene through Holocene modern humans (Tables 13). Original data derive from a Medieval sample (MED) from Noli (Liguria, Italy) (n 5 21) that was studied via direct sectioning (Sparacello and Marchi, 2008); an Iron Age sample (IRON) from Alfedena (Abruzzo, Italy) (n 5 30) that were sectioned in the past for studies not related to CSG (Macchiarelli, 1988; Sparacello et al., 2009); a Neolithic sample (LIG) from the Finale Ligure area (Liguria, Italy) (n 5 16), studied via the LCM method (Marchi et al., 2006; Marchi, 2008; Sparacello and Marchi, 2008); and femoral data calculated via the LCM method of the Neolithic sample from Catalhoyuk (n 5 17) (Cowgill, personal communication). The CSG data used in this research were obtained using different methods: LCM, CT scans, and direct

CROSS-SECTIONAL GEOMETRY FROM PERIOSTEAL CONTOURS

TABLE 1. Population mean of percent cortical area in the femur, midshaft section Sex Early Upper Paleolithic Europe Late Upper Paleolithic Europe Mesolithic Europe Neolithic Liguria, Italy Neolithic Turkey Iron Age Abruzzo, Italy Medieval Liguria, Italy Sub-Saharan African Zulu Khoisan Afro-American Amerindian Gr. Salt Lake Amerindian Malheur Amerindian Pecos Pueblo Amerindian Stillwater Andaman Islanders Australian hunter-gatherers # $ # $ # $ # $ # $ # $ # $ # $ # $ # $ # $ # $ # $ # $ # $ # $ # $ N 9 4 15 7 29 15 8 8 11 6 20 10 15 6 12 2 25 25 27 20 45 8 8 7 9 14 59 60 11 13 16 15 15 12 Mean %CA 75.84 81.3 81.45 79.72 76.42 79.71 75.9 77.86 77.86 76.22 77.71 71.53 75.45 74.85 77.3 80.2 73.1 68.9 73.6 68.8 72.7 68.3 73.1 69.3 73.1 69 72.0 71.1 68.2 62.5 81.85 80.95 75.4 73.5 SD 5.84 2.53 6.01 8.64 6.01 7.15 5.4 4.43 8.33 7.31 6.47 8.75 4.51 6.96 5.3 6.2 6.8 7.2 11.4 7.7 11.6 4.76 4.16 7.64 5.77 5.9 9.3 5.38 7.62 4.52 3.63 5.9 6.5 Range 67.2781.82 78.3784.54 70.9191.54 69.4093.42 66.1687.73 58.1888.14 6882.79 70.3282.45 62.9386.26 62.6782.86 64.2286.62 60.1781.63 68.7782.04 62.1682.13 68.584.5 78.582 60.884 56.483.3 56.784.1 40.691 55.586.4 50.685.5 Data provenience Holt, 1999a Holt, 1999; Vercellotti, 2005b Holt, 1999 Marchi et al., 2006a Cowgill, Personal dataa Sparacello et al., 2009c Sparacello and Marchi, 2008c Grine et al., 1995b Grine et al., 1995 Grine et al., 1995 Grine et al., 1995 Ruff, 1999b Ruff, 1999 56.382.1 31.083.3

Ruff and Hayes, 1983c; Ruff, personal communication Ruff, 1999 Stock and Pfeiffer, 2001a,b Carlson et al., 2007b

Separated sexes. a Data obtained through LCM method. b Data obtained through CT scans. c Data obtained through direct sectioning.

TABLE 2. Population mean of percent cortical area in the femur, midshaft section N Early Upper Paleolithic Europe Late Upper Paleolithic Europe LSA South Africa Mesolithic Europe Neolithic Liguria, Italy Neolithic Turkey Iron Age Abruzzo, Italy Byzantine Turkey Amerindian Great Basin Amerindian Pecos Pueblo, Georgia Coast, Great plains Andaman Islanders European American Recent Homo sapiens 13 22 37 44 16 16 30 8 62 206 31 40 322 Mean %CA 77.52 80.9 78.26 77.54 76.88 76.93 75.65 74.07 68.7 71.5 81.41 69.1 71.3 SD 5.59 6.79 5.67 6.53 4.88 7.91 7.75 4.09 7.03 7.16 4.07 6.3 7.17 Range 67.2785.54 69.493.42 58.1888.14 6882.79 62.6786.26 60.1786.62 67.8879.52 Data provenience Holt, 1999a Holt, 1999; Vercellotti, 2005b Stock and Pfeiffer, 2001a,b Holt, 1999 Marchi et al., 2006a Cowgill, Personal dataa Sparacello, Personal datac Cowgill, Personal dataa Ruff, 1999b Ruff, 1999b Stock and Pfeiffer, 2001a,b Grine et al., 1995b Ruff et al., 1993b,c

4788

Pooled sexes. a Data obtained through LCM method. b Data obtained through CT scans. c Data obtained through direct sectioning.

sectioning (Tables 13). Although it would be ideal to use a large dataset obtained via a single method (preferably direct sectioning or CT scans), this kind of data is not available at this stage of research. However, crosssectional properties derived from the LCM method can

be compared with CT scan data without prior corrections (Stock, 2002; ONeill and Ruff, 2004), as done in several studies (e.g., Ruff et al., 1993; Trinkaus et al., 1994). For the purpose of this research, we consider the CSG data obtained through the different methods as comparable. American Journal of Physical Anthropology

V.S. SPARACELLO AND O.M. PEARSON

TABLE 3. Mean, standard deviation, and percent standard deviation in femoral unstandardized J Sex N 10 4 16 7 29 15 8 8 20 10 15 6 12 25 25 27 20 119 59 60 22 20 45 8 36 Mean J 72728.40 56462.50 57352.17 38491.14 46562.03 33467.33 45600.10 31227.22 53747.85 39283.08 60561.81 32525.43 46,956 52,802 34,667 35,495 23,247 31,768 37,769 25,531 30,860 15,570 60,367 42,565 45,049 SD 20835.70 12457.62 14278.32 9656.75 13592.28 8454.44 12832.25 7154.71 9015.54 12360.99 11176.57 8793.42 12,247 14,303 8,229 10,879 6,069 8,891 6,643 5,956 7,160 4,670 12,714 7,428 15,348 Mean %SD % SD 28.65 22.06 24.9 25.09 29.19 25.26 28.14 22.91 16.77 31.47 18.45 27.04 26.08 27.09 23.74 30.65 26.11 27.99 17.59 23.33 23.20 29.99 21.06 17.45 34.07 25.13 Data provenience Holt, 1999a Holt, 1999; Vercellotti, 2005b Holt, 1999 Marchi et al., 2006a Sparacello et al., 2009c Sparacello and Marchi, 2008c Grine et al., 1995b Grine et al., 1995 Grine et al., 1995 Ruff, 1984c Ruff and Hayes, 1983c; Ruff, Personal communication Grine et al., 1995 Grine et al., 1995 Ruff, 1984 # $ # $ # $ # $ # $ # $ # # $ # $ #1$ # $ # $ # $ #1$

Early Upper Paleolithic Europe Late Upper Paleolithic Europe Mesolithic Europe Neolithic Liguria, Italy Iron Age Abruzzo, Italy Medieval Liguria, Italy Sub-Saharan African Zulu Khoisan Native American pooled sex Amerindian Pecos Pueblo Japanese Afro-American Autopsy sample
a b c

Data obtained through LCM method. Data obtained through CT scans. Data obtained through direct sectioning.

METHODS
Bone shafts are primarily inuenced by bending rather than by axially compressive and torsional loads (Cowin, 1987; Bertram and Biewener, 1988). We therefore focused our analysis on the CSG variables expressing the resistance of bone shafts to bending loads. The rigidity of a cross section of a beam relative to bending is quantied as its second moment of area (SMA), denoted by the symbol I (J for average bending rigidity) and measured in millimeters to the 4th power (Lovejoy et al., 1976; Ruff and Hayes, 1983). For example, I calculated with respect to the x-axis is: Z Ix
A

circular section, I relative to a bisecting neutral axis is: p I r4 r4 e 4 p 2

where rp is the radius from the centroid to the periosteal surface and re is the radius to the endosteal border. Furthermore, TA pr2 p MA pr2 e 3 4

X dA
2

X
i

Xi2 DAi

1 The formula for I can be written: I TA2 MA2 4p 5

where X is the distance of the unit of area DA to the line parallel to x-axis that passes through the centroid of the section. For perfectly circular sections, SMAs can be easily calculated. The simulation in the rst analysis is based on idealized cross sections of two concentric circles representing the periosteal and endosteal surfaces of the cortex (Cowin, 1984; Lazenby, 1990). An important feature of the SMA formula is that units of bone area situated farther from the neutral axis will contribute more to geometric rigidity than closer units. Therefore, an increase of a given area on the periosteal border will have a greater impact than an increase of the same area on the endosteal border. To quantify this relationship precisely, we express I as a function of TA and MA. For a hollow concentric American Journal of Physical Anthropology

Formula (5) presents an expression of I as a function of TA and the medullary size of the section. This formula will be used in the assessment of the maximum inuence of variation in relative cortical thickness on mechanical rigidity if TA is held constant. %CA TA MA TA 6

This index is the percent of cortical area expressed as a number between 0 and 1. Introducing %CA in the formula (5), we obtain I as a function of TA and %CA:

CROSS-SECTIONAL GEOMETRY FROM PERIOSTEAL CONTOURS I TA 1 1 %CA2 4p

2

J is the average bending rigidity of the bone, which can be calculated as the sum of two perpendicular Is. Thus: J TA2 1 1 %CA2 2p 8

Simulation of the inuence on J of an extreme difference in mean %CA

How much does variation in %CA affect estimates of second moments of area? In particular, how large is the effect of variation in %CA in assessment of the difference between population means in J, a parameter frequently used to make inferences about subsistence-related habitual activity? Tables 1 and 2 show population-level as well as individual-level differences in %CA. The range of variation at the individual level is much higher than at a population level, and therefore the conclusions of this analysis cannot be extended to studies that focus on comparing individuals (see Discussion). To estimate the highest level of error likely to be created by ignoring the variation in %CA, we simulated a comparison between two hypothetical samples with the same TA but values of %CA corresponding to the highest and lowest mean %CA encountered in a variety of previous bioarchaeological studies (Tables 1 and 2). This can be considered a worst-case scenario in behaviorally focused CSG comparisons because actual differences in %CA between most pairs of populations should be lower. We calculated the variation difference in bending rigidity (DJ) due to this extreme difference in %CA using formula (8). Power analysis was used to determine the sample size needed to detect the resulting mean difference in J via a two-sample t-test with a reasonable power of 90%.

P \ 0.00001, Mann-Whitney U test) and is close to the mean %CA reported for Homo erectus (0.837; Ruff et al., 1993). We designated MA* to be the estimates of MA derived from the regression based on the MED sample and MAy the estimates derived from the regression based on the HIGH%CA sample. The estimates of MA derived from the two regressions were then used to obtain estimates of J (J* and Jy, estimated by incorporating MA* and MAy, respectively) through a formula that corrects periosteal CSG data taking into account the inuence of MA. In formula (8), TA2/ 2p is the value of J that is produced in a circular, solid section lacking any medullary cavity. We term this quantity solid J. Formula (8) can therefore be written as:   ! TA MA* 2 J* solid J 1 1 9 TA The differences between the actual J and the two estimates, J* and Jy were assessed calculating mean absolute ([|(estimate 2 true)|/true)] 3 100) and directional ([(estimate-true)/true)] 3 100) percent prediction errors from the true values and regressed estimates. Absolute and directional errors are representative of the random and systematic biases, respectively, of each method. The difference between estimates and actual values was analyzed also through paired t-tests and power analyses (90% power). We utilized the paired t-test instead of the t-test used in step one because the samples compared here are not independent, being composed by the same bones but differently treated (i.e., direct measurement of CSG from sectioned bones or CT scans versus applying regression equations). The null hypothesis of a paired t-test is that the mean difference between paired observations is zero. This hypothesis is mathematically equivalent to the null hypothesis of a t-test (the means of the groups are equal). However, due to the paired design of the data, the paired t-test informs whether a systematic bias in the estimates is present, which is the most relevant to analysis of treatment effects (in this case bias introduced by the regressions). In this setting, the power analysis gives the minimum number of couples with mean difference and standard deviation of the differences as observed necessary to consider signicant the systematic bias. As noted by Stock (2002), the assessment of how much error is acceptable in methods for measurements estimation is generally up the discretion and experience of the individual researcher. For the present study, a regression method correcting periosteal CSG will be considered having an acceptable amount of error (mean absolute and directional percent prediction error, PPE) if it will be comparable of lower than the one produced by the LCM method. This method involving periosteal moulds and biplanar radiographs is currently considered a robust noninvasive means of obtaining cross sections (ONeill and Ruff, 2004).

Correcting periosteal J through the prediction of MA from TA

To reduce the degree of error derived from ignoring the variation in size of the medullary cavity, we considered the possibility that TA can be used to predict MA. We determined the relationship between TA and MA in two samples of femoral cross sections and developed a regression for each (regression equations are based on natural logged data to correct heteroscedasticity). We used the regressions to predict MA in a third sample (n 5 30) of femora from the IRON sample. We used two different samples: a sample with similar mean %CA when compared with the IRON sample and a sample with signicantly different mean %CA. The rst sample is composed from a medieval group (MED) from Noli (n 5 21) (Sparacello and Marchi, 2008); this sample has a mean %CA (0.753) that is not statistically different than the IRON sample one (0.757). The second sample (HIGH%CA) is composed by a selection of Late Pleistocene-Holocene individuals (n 5 48) having values of %CA above 80% (Holt, 1999; Marchi, Sparacello, Vercellotti, personal data). The mean %CA of the HIGH%CA sample (0.835) is signicantly higher when compared with the IRON sample (P \ 0.000000, two sample t-test;

Replicating Stock and Shaws results

The third step involves a realistic scenario where the use of regression equations similar to the ones developed by Stock and Shaw (2007) can be tested: a comparison of CSG parameters aimed at the reconstruction of diachronic changes in habitual behavior. This provides a check on whether Stock and Shaws (2007) results of accurate prediction hold using similar but not identical American Journal of Physical Anthropology

V.S. SPARACELLO AND O.M. PEARSON DJ TA2 0:1077 2p

methods. When applying this method, the researcher would base the regressions on samples that are more likely to be similar to the one under study. We therefore used the humeri, femora, and tibiae of the MED and LIG sample and we created equations predicting J from TA and solid J, and the shape index Imax/Imin from solid Imax/Imin (regression equations are based on logged data to correct heteroscedasticity). The regressions were then applied to the IRON control sample, which dwelled in the same area (the Italian peninsula) of the samples used for the regressions, is temporally intermediate, and shows genetic continuity with Neolithic and early historic samples (Coppa et al., 1998, 2007). The goals of the third step are to: 1) verify whether the strong predictive power of TA and periosteal CSG that Stock and Shaw detected would remain in a smaller sample; 2) assess if, at least in this setting, using different regression equations (by bone, sex, or time period) will lead to noticeably different results; and 3) assess how accurately actual Imax/Imin can be predicted from the periosteal contour. The theoretical explanation based on right-circular concentric sections does not hold for SMAs in sections far from circularity; additional empirical verication is necessary for noncircular geometry. The degree of error derived from the estimation procedure was determined by calculating mean absolute and directional PPEs, and using paired t-tests and power analysis as described in Step 2. A test for homogeneity of slopes was performed to determine if the relationship between predicted CSG and actual CSG was inuenced by three categorical factors: the period the samples came from, the sex of the individuals (estimated in previous researches using standard osteometric correlates), and which long bone (femur, humerus, or tibia) was used in the regression. Cross sections were analyzed with a version of the program SLICE (Nagurka and Hayes, 1980), adapted as a macroroutine for use with Scion Image (freely available at http://www.scioncorp.com/pages/download_now.asp). Statistical analysis was conducted using the PC programs STATISTICA 7 (Statsoft, 2004), Minitab 15 (Minitab Inc., 2006), and the power analysis tool PIFACE 1.70 developed by Russell L. Lenth (available at http:// www.cs.uiowa.edu/$rlenth/Power/).

How many individuals would be needed in each of two samples to detect a difference in J of this magnitude? We used power analysis to determine the necessary size of the two samples to detect this difference with a power of 90%. We set the standard deviation for J to be 20% of the value of J, a conservative value given that the mean standard deviation for published nonstandardized J is 25.13% (Table 3). Another reason to be conservative is the fact that in small samples, such as some of the ones available in Table 3, the standard deviation may be not stable, and therefore averaging over them may not reect the real mean standard deviation of J. However, in Table 3 there is no apparent relationship between sample size and standard deviation. The results indicate that for a difference of this magnitude of J, 61 femora would be needed in each sample to detect a signicant difference (P 0.05) 90% of the time using a t-test with equal variances (the standard deviation of the two samples was averaged). If one sets the mean standard deviation to 25.13%, the sample size rises to 96. If one considers a slightly less exceptional case for differences in mean %CA, and uses the values for population means that fall at the 5th to 95th percentiles of population means, the minimum %CA would be 0.682 and the maximum 0.813. With these parameters, the sample size reaches 168 femora in each sample setting the standard deviation at 20% of J, or 264 in each sample setting the standard deviation at 25.13% of J.

Using TA to predict MA
The above analysis assumes that studying external dimensions (TA), we have no information on the size of the medullary cavity. However, TA can be used to obtain a general estimate of MA. For example, in the femora of the MED sample (n 5 21), TA predicts MA with the following equation: Ln MA 5 22.5527 1 1.1791 3 Ln TA (R2 5 0.524, P 5 0.0002) (see Fig. 1A). In the femora of the HIGH%CA sample the same relationship is: Ln MA 5 22.6285 1 1.1269 3 Ln TA (R2 5 0.437, P 5 0.0000003). We applied each of these regressions to the 30 femora of the IRON sample. Although the relationship between TA and MA is highly signicant in both regressions, the resultant estimates of the medullary cavity area (MA* and MAy) also contain a substantial amount of error. The mean absolute percent prediction errors are 25.35% using the regression derived from the sample (MED) which has a similar mean %CA as the IRON sample and 53.89% using the HIGH%CA sample. Nevertheless, both estimates of MA appear useful when used to correct solid J of the control sample using formula (9) to obtain J* and Jy: the difference in mean and standard deviation between the actual data and the predicted values appears minimal. In Table 4, we report mean absolute and directional PPEs, and the results of the paired t-tests and power analyses. J* values are slightly overestimated (1.08%), but the paired t-test is not signicant, suggesting that the regression based on the MED sample does not produce a systematic bias on the individual estimate. A sample size of 138 bones with the same error mean and SD as observed would be needed for the observed difference to reach signicance 90% of the time.

RESULTS The worst case scenario

The lowest published mean for femoral midshaft %CA in Late Pleistocene-Holocene humans is 0.625 for the female Amerindian sample from Stillwater (Ruff, 1999); the highest is 0.8185 for male Andaman Islanders (Stock and Pfeiffer, 2001) (Tables 1 and 2). The difference in estimated SMAs in two samples which have this extreme difference in %CA with TA and cross-sectional shape held constant was determined via formula (8) in each case. JRCA0;8185 JRCA0;625 TA2 TA2 1 1 0:81852 0:9671 2p 2p TA2 TA2 1 1 0:6252 0:8594 2p 2p

The difference in SMA (DJ) due to the difference in %CA is: American Journal of Physical Anthropology

CROSS-SECTIONAL GEOMETRY FROM PERIOSTEAL CONTOURS

Fig. 1. A: Scatterplot and least squares regression line of Ln MA over Ln TA using the femora of the MED sample (R2 5 0.524). B: Scatterplot and least squares regression lines by bone of Ln J over Ln TA in the humeri, femora, and tibiae of the MED sample (R2 5 0.996). C: Scatterplot and least squares regression lines by bone and period of Ln J over Ln TA in the humeri, femora, and tibiae of the MED and LIG samples pooled (R2 5 0.995). D: Scatterplot and least squares regression lines by bone and period of Ln J over Ln of solid J in the humeri, femora, and tibiae of the MED and LIG samples pooled (R2 5 0.997). See text and Tables 6 and 7 for regression equations.

For the estimate Jy, the paired t-test is highly signicant (P \ 0.0001), and the systematic bias is detectable in small samples (n 5 15). Using a regression based on a sample with substantially different %CA leads to a systematic overestimation of J (directional PPE 5 4.39%; Table 4).

TABLE 4. Power analysis IRON sample femoral J Pooled sexes Mean SD Mean absolute PPEc SD Mean directional PPEd SD %D mean Je Paired t-test Sample size to detect systematic biasf Femoral J Actual data Femoral J*a Femoral Jyb 48926.26 12197.13 49601.5 12993.9 3.48% 3.02 1.08% 4.52 1.36% NS 138 51347.55 13548.92 4.50% 4.29 4.39% 4.41 4.72% P \ 0.0001 15

Replicating Stock and Shaws results

We replicated Stock and Shaws (2007) results using the MED sample, and adding the LIG sample (total n 5 137; Table 5). Even though the sample used to create the regression equations was a smaller sample size than that used by Stock and Shaw (n 5 1431), we still nd regression equations with high predictive strength, as demonstrated by the high R2 and the low %SEE and absolute PPE (Fig. 1B,C; Table 6). In fact, we found higher R2 and lower %SEE and PPE power using solid J as the predictor rather than TA (Fig. 1D; Table 7). Figure 1D suggests that the regression equation is very similar regardless of which long bone or sample is considered because a highly linear relationship exists between solid J and actual J across all the long bones that were included. Tests for homogeneity of slopes and intercept of the categorical predictors sex, period, and bone conrm that, in our samples, these variables

Sample parameters of the actual data, and of the data estimated using formula (9) (see text). a J* estimated from TA using formula (9); MA* predicted from TA using the MED sample. b y J estimated from TA using formula (9); MAy predicted from TA using the HIGH%CA sample. c Absolute PPE 5 (|estimate true|/true) 3 100. Based on back-transformed natural log estimated and natural log true values. d Directional PPE 5 (estimate true/true) 3 100. Based on back-transformed natural log estimated and natural log true values. e %Dmean J 5 (|estimated mean true mean|/true mean) 3 100. Based on back-transformed natural log estimated and natural log true values. f Power analysis, power 5 90%.

American Journal of Physical Anthropology

V.S. SPARACELLO AND O.M. PEARSON shown here). Absolute and directional PPEs have range of 1.5% to 2.42% and 22.27% to 0.2%, respectively. In most cases, regression equations create a systematic bias to the estimate, producing signicant paired t-test.

do not signicantly interact with the regression parameters (Table 8). Table 9 shows the results of different regression equations applied to the IRON femora. We used Stock and Shaws (2007) all-bones equation, the all-bones regression equations based on the MED as well as in the pooled MED and LIG samples (Table 8), and the bonespecic regression equations derived from the same samples (not shown here). Absolute and directional PPEs have range of 3.53% to 4.18%, and 21.50% to 0.57%, respectively. The regression equations do not produce a systematic bias in the estimate (paired t-tests were not signicant). To consider the observed level of bias as signicant, minimum required sample size spans from 136 bones in each sample to 42,300, depending on the equation used. Table 10 shows the results of the estimation of the shape index Imax/Imin. As for J, we used Stock and Shaws (2007) all-bones equation, the all-bones regression equations based on the MED and on the MED and LIG samples pooled (Table 8), and the bone-specic regression equations derived from the same samples (not
TABLE 5. Sample used for the regression equations Period NEOL Sex M F MED M F Bone Humeri Femora Tibiae Humeri Femora Tibiae Humeri Femora Tibiae Humeri Femora Tibiae Total n 14 8 7 16 8 7 25 15 9 17 6 5 137

DISCUSSION
In this article, we address if it is important to accurately measure the area of the medullary cavity when comparing mean J in two bioarchaeological samples. First, we determined the greatest error likely to be produced by ignoring normal, population variation in %CA. We simulated a worst-case scenario: a comparison between two samples having the same TA but relative cortical thickness (%CA) at the opposite ends of variation of samples of Late Pleistocene-Holocene humans. This can be considered a worst-case scenario in behaviorally focused CSG comparisons because actual differences in %CA between most pairs of populations should be lower. This extreme difference in %CA has a modest effect on the difference in J between the two hypothetical samples: power analysis suggests a minimum of 61 bones in each of two samples to detect the resultant level of difference into DJ with 90% power. If one considers a difference between sample means in %CA that is of a magnitude more commonly encountered, the sample size needed to detect the resultant difference reaches the hundreds. The sample size of individuals normally available from CT scans or LCM in most bioarchaeological studies tends to be much smaller (e.g., Tables 13); more numerous samples are usually pooled sex or pooled group samples. Our results imply that for most samples, differences in mean %CA make little impact on analyses of mean J. It should be noted that this effect may not hold when comparing the bending rigidity of two individual bones. Individual variation in %CA is much higher than population level variation, spanning from 31.0% to 93.42% (Tables 1 and 2). Power analysis suggests that, given the

TABLE 6. Parameters of the regression equations predicting actual J from TA Model parameters and coefcients Ln J vs. Ln TA MED sample MED 1 LIG sample
a

Error P 0.0000 0.0000 %SSEb 5.51% 5.99% Mean absolute PPEc 3.91% 4.20% Maxmin PPE 0.04918.22% 0.0917.38%

na 77 137

R2 0.996 0.995

Slope 2.032 2.050

Intercept 22.058 22.152

Pooled bones equation. a Details on size of the sub-samples based on bone, period and sex in Table 5. b %SEE 5 exp (SEE 1 4.6052) 100; based on natural log-transformed data (Ruff, 2003). c Absolute PPE 5 (|estimate true|/true) 3 100. Based on back-transformed natural log estimated and natural log true values.

TABLE 7. Parameters of the regression equations predicting actual J from solid J (TA2/2p) Model parameters and coefcients Ln J vs. Ln solid J MED sample MED 1 LIG sample na 77 137 R2 0.997 0.997 n 77 137 R2 0.992 0.996 Slope 0.998 1.001 b0 1.0203 1.0183 Intercept 20.0555 20.0767 b1 20.008 20.0086 P 0.0000 0.0000 P 0.0000 0.0000 %SEEb 4.32% 4.84% %SEE 2.10% 1.78% Error Mean absolute PPEc 3.03% 2.77% Mean absolute PPE 1.97% 1.91% Maxmin PPE 0.00416.74% 0.0217.07% Maxmin PPE 0.0117.32% 0.0757.23%

Ln Imax/Imin vs. Ln Imax/Imin MED sample MED 1 LIG sample

Pooled bones equation. a Details on size of the sub-samples based on bone, period and sex in Table 5. b %SEE 5 exp (SEE 1 4.6052) 100; based on natural log-transformed data (Ruff, 2003). c Absolute PPE 5 (|estimate true|/true) 3 100. Based on back-transformed natural log estimated and natural log true values.

American Journal of Physical Anthropology

CROSS-SECTIONAL GEOMETRY FROM PERIOSTEAL CONTOURS

TABLE 8. Test for homogeneity of slopes, and interaction effects in the regression equation predicting actual J P-value Intercept Period Sex Bone Ln solid J Period 3 sex Period 3 bone Sex 3 bone Period 3 Ln solid J Sex 3 Ln solid J Bone 3 Ln solid J Period 3 sex 3 bone Period 3 sex 3 Ln solid J Period 3 bone 3 Ln solid J Sex 3 bone 3 Ln solid J Period 3 sex 3 bone 3 Ln solid J 0.173 0.118 0.093 0.757 0.000 0.166 0.604 1 0.121 0.073 0.688 0.750 0.172 0.627 0.987 0.724

Continuous variable: solid J; categorical predictors: bone segment, sex, period.

same TA, the difference in J due to such a level of difference in %CA would be statistically detectable in small samples (Satterthwaite t-test: n 5 6 considering 20% SD for J). Thus, an accurate estimate of the subperiosteal and endosteal contour is paramount when comparing individuals. The same is true for CSG comparisons that analyze the difference in J among samples due to factors such as growth and aging (Ruff et al., 1994; Ruff, 2010), nutrition and health (Mays et al., 2009), and phylogeny (Ruff et al., 1993). Cortical thickness is an essential factor in these studies, and thus in such cases it would not make sense to estimate it or ignore variation in it. Our conclusions apply best for researches comparing estimates of population means drawn from fairly similar skeletal samples to make inferences about the behaviorally determined mechanical environment of past populations. The TA of a section is expected to have some predictive strength for MA due to an optimization trade-off between bone mass and skeletal strength. Many authors suggest that tubular bones can be considered minimum

TABLE 9. Power analysis IRON sample femoral J Mean absolute PPEa 3.61% 3.66% 3.82% 3.62% 3.53% 3.84% 4.00% 3.62% 4.18% Mean directional PPEb 0.26% 0.53% 20.26% 0.48% 0.57% 20.27% 20.78% 0.35% 21.50% Paired t-test NS NS NS NS NS NS NS NS NS Sample size to detect systematic biasd 892 327 42,300 400 366 37,150 1,278 606 136

Mean Actual data Stock & Shaw, all bonese LIG 1 MED sample, all bonesf LIG 1 MED sample, humerusf LIG 1 MED sample, femurf LIG 1 MED sample, tibiaf MED sample, all bonesf MED sample, humerusf MED sample, femurf MED sample, tibiaf 48926.26 49183.40 49372.73 48964.41 49321.55 49331.68 48966.99 48710.52 49243.85 48293.42

SD 12197.13 12886.10 13080.84 12921.24 12980.54 12878.26 12941.06 12841.15 12917.96 12502

SD 2.73 2.78 2.52 2.76 2.82 2.52 2.37 2.72 2.34

SD 4.57 4.62 4.63 4.58 4.53 4.64 4.64 4.57 4.6

%D mean Jc 0.52% 0.9% 0.08% 0.8% 0.8% 0.08% 0.44% 0.64% 1.31%

Sample parameters of the actual data, and of the data estimated using different regression equations. a Absolute PPE 5 (|estimate true|/true) 3 100. Based on back-transformed natural log estimated and natural log true values. b Directional PPE 5 (estimate true/true) 3 100. Based on back-transformed natural log estimated and natural log true values. c %D mean J 5 (|estimated mean true mean|/true mean) 3 100. Based on back-transformed natural log estimated and natural log true values. d Power analysis. Power 5 90%. e Regression equation predicting Ln J from Ln TA. f Regression equation predicting Ln J from Ln solid J.

TABLE 10. Power analysis IRON sample femoral Imax/Imin Mean absolute PPEa 1.94% 1.97% 2.33% 1.8% 1.57% 1.91% 2.42% 1.58% 1.5% Mean directional PPEb 21.66% 21.79% 22.16% 21.41% 0.2% 21.68% 22.27% 20.76% 20.43% %D mean Jc 1.73% 1.73% 2.3% 1.41% 0.15% 1.65% 2.38% 0.78% 0.39% Paired t-test P \ 0.0001 P \ 0.0001 P \ 0.0001 P \ 0.001 NS P \ 0.0001 P \ 0.0001 P \ 0.05 NS Sample size to detect systematic biasd 18 15 13 24 1644 17 12 68 228

Mean Actual data Stock & Shaw, all bonese LIG 1 MED sample, all bonese LIG 1 MED sample, humeruse LIG 1 MED sample, femure LIG 1 MED sample, tibiae MED sample, all bonese MED sample, humeruse MED sample, femure MED sample, tibiae 1.292 1.270 1.27 1.263 1.274 1.295 1.271 1.262 1.282 1.287

SD 0.208 0.198 0.206 0.191 0.201 0.205 0.206 0.191 0.204 0.207

SD 1.8 1.86 2 1.69 1.21 1.82 2.03 1.44 1.39

SD 2.06 2.04 2.19 2.03 2 2.05 2.2 2.01 2.01

Sample parameters of the actual data, and of the data estimated using different regression equations. a Absolute PPE 5 (|estimate true|/true) 3 100. Based on back-transformed natural log estimated and natural log true values. b Directional PPE 5 (estimate true/true) 3 100. Based on back-transformed natural log estimated and natural log true values. c %D mean J 5 (|estimated mean true mean|/true mean) 3 100. Based on back-transformed natural log estimated and natural log true values. d Power analysis. Power 5 90%. e Regression equation predicting Ln Imax/Imin from Ln solid Imax/Imin.

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V.S. SPARACELLO AND O.M. PEARSON in the majority of cases, i.e., when the %CA of the sample used for the regression will be included between the identity with the sample to be regressed and the extremes, the regression method will perform comparably with the LCM method. Although a difference up to 4.5% in robusticity will be biologically and behaviorally signicant in certain research settings, the LCM method is considered a robust noninvasive approach for data collection in CSG, and data obtained through this method do not need correction prior to being compared with CT scan data (ONeill and Ruff, 2004). We suggest that the same conclusions can be applied to the regression method described here. These results suggest that, for the kind of analyses of SMA considered in this article, the contour of the medullary cavity does not need to be known precisely, and that a correction of periosteal CSG through a regression equation based on another, reasonably similar sample is sufcient to obtain a close estimate of mean overall bending strength. Several concomitant factors contribute to the ability of TA and periosteal J to predict actual J in a regression. First, the outermost units of bone contribute exponentially more to bending strength than the same amount of area closer to the centroid. TA or solid J therefore provides most of the information that will determine a bones bending strength. Second, to adapt to different levels of bending strains at the age of peak bone mass, bones will tend to differ in TA rather than in cortical thickness. After skeletal maturation, mechanical effects appear to be most marked on the endosteal rather than subperiosteal surfaces of long bones (Ruff et al., 1991, 1994, 2006). However, for most preindustrial subsistence regimes, we can assume that the workload level typical of the population was attained by the individuals by late adolescence. This would make the TA at the age of peak bone mass informative about the mechanical environment of a pre- and proto-historic population (Pearson and Lieberman, 2004). Which regression equation should be used? A variety of factors are likely to have an inuence in the relative cortical thickness of a bone shaft around the minimum-mass optimum. Various bone segments may be optimized for different kind of loadings, leading to specic optimal TA-%CA relationship (Currey and Alexander, 1985; Lieberman et al., 2003); male and female physiology may dictate variable requirements for calcium storage; genetic factors among populations may lead to variations in cortical thickness; differences in nutritional status and pathogen environment may also lead to variation. Although these factors could potentially inuence the predictive strength of TA over MA, their inuence may be minimal when overall bending strength is predicted. A test for homogeneity of slopes suggests thatwhen regressions are based on samples genetically, temporally, and geographically close to the control sample such as the ones we usedbone segment, period, and sex do not signicantly interact with the continuous predictor solid J. Consequently, even when different regression equations are applied to the same sample, results are very similar. Power analysis suggests that, regardless of the regression equation used, the sample parameters obtained would be distinguishable from the real data only using samples of hundreds or more. The difference in the mean values between regressed data and real data is below 1% for all of the estimates (except the one based on MED tibiae %D mean J 5 1.31%), and absolute and directional PPEs are lower than the ones reported for the LCM method (Stock,

mass solutions adapted to their loading histories (Bouvier, 1985; Frost, 1985; Lanyon, 1987; Rubin and Lanyon, 1987). Alexander (1982), Currey (1982, 1984), and Pauwels (1980) predicted the theoretical optimal hollowness of long bones with respect to ultimate bending; these predictions have been corroborated by empirical observations (Alexander, 1982; Currey, 1982; Currey and Alexander, 1985). Lazenby (1990) notes that the total area of a sectionand the consequent weight-optimized medullary cavityis determined at the age of peak bone mass from the mechanical environment generated by body dimensions (weight plus bone length and curvature) and activity levels. This suggests that, ideally, the relationship between TA and MA may be purely allometric. Currey and Alexander (1985) demonstrated that the cortical thickness with respect to the radius of the section generally conforms to the above theoretical expectations. However, a certain degree of variation in cortical thickness will not affect the minimum-mass optimization (Fig. 2 in Currey and Alexander, 1985). This explains why, in the samples we used, the predictive strength of TA for MA was not great, and the estimates contained substantial error. Individual variability around the theoretical minimum-mass optimum is partially due to activity-related cortical thickening through endosteal bone deposition (Ruff et al., 1991, 1994; Ruff, 2006), but also to the fact that the skeleton does not possess a purely mechanical function but also responds to a variety of physiological needs such as calcium storage (Ruff et al., 2006). However, we demonstrated that when the imprecise estimates of MA are used to correct values of J based in the periosteal contour, the sample parameters obtained are very close to real data, especially when one uses a regression based on a sample with similar %CA. Such cases produce no systematic bias in the estimates, and more than one hundred bones would be needed to distinguish the real and predicted values statistically. Differences between samples requiring hundreds of individuals to be distinguished statistically can be considered of no practical importance in the context of comparisons between archaeological samples for behavioral interpretations because they focus on differences in CSG parameters that are substantial enough to be detected with a few tens of individuals. Moreover, absolute and directional PPEs parameters obtained applying this regression are lower than what has been reported in previous research for the error entailed in the LCM procedure (Stock, 2002; ONeill and Ruff, 2004). For midshaft femoral J, LCM absolute error is 5.6% (SD 5 4.4) against our 3.48% (SD 5 3.02); LCM directional error is 23.4% (SD 5 5.5) against our 1.08% (SD 5 4.52) (Table 3 in ONeill and Ruff, 2004). When regression is based on a sample with a substantially different %CA than to the target sample, a systematic mis-estimation of J is made for each individual, but the mean of the estimate is still close to the real value, absolute PPE is 4.50% (SD 5 4.29) and directional PPE is 4.29 (SD 5 4.41). Thus, the regression method performs slightly worse than the LCM method when the sample used for the regression has an extreme cortical thickness: %CA of the HIGH%CA sample (0.835) is close to the mean %CA reported for Homo erectus (0.837; Ruff et al., 1993). When %CA of the sample used for the regression is indistinguishable from the one shown from the sample to be estimated, the regression method performs better than the LCM method. We can therefore conclude that American Journal of Physical Anthropology

CROSS-SECTIONAL GEOMETRY FROM PERIOSTEAL CONTOURS 2002; ONeill and Ruff, 2004). We therefore suggest that correcting periosteal CSG using regressions is a valid noninvasive method, and when regressions are based on similar samples, as in this case, the use of a single equation for all the long bones usually considered in CSG studies is appropriate to obtain an accurate estimate of J. This is supported also by the fact that the results of the power analysis in our worst-case scenario depend only on the range of variation in %CA and are independent of TA. Therefore, our conclusions are likely valid also for the humerus and tibia, the other bones usually studied in CSG research. A survey of the literature demonstrates that the range of variation of %CA in these bones is similar to that shown by the femur (e.g., Ruff and Jones, 1981; Ruff and Hayes, 1983; Churchill, 1994; Holt, 1999; Ruff, 1999; Stock and Pfeiffer, 2001; Marchi, 2004, 2007; Vercellotti, 2005; Marchi et al., 2006; Carlson et al., 2007; Sparacello and Marchi, 2008). A theoretical justication for ignoring individual variation in the size and shape of the medullary cavity for periosteally derived SMAs such as Ix, Iy, Imax, Imin, or CSG shape is not possible based on right-circular sections for the obvious reason that bone sections usually depart from circularity. Thus, the estimates of these variables will be less accurate and systematically more biased than J when applying the regression method. Accordingly, paired t-test comparing the actual shape index Imax/Imin and its estimates in Table 10 are highly signicant in most cases, and small samples are enough order to detect the bias. Moreover, the accuracy of the estimated mean uctuates based on how similar the shape of the control sample was with respect to the sample used for the regression, and the directional PPE is generally higher than what was detected for J. However, the absolute PPEs are lower than the ones generally shown by J estimates, and the difference in the mean values between regressed data and real data is comprised between 0.15% and 2.38%. Although no PPEs are provided in previous research for shape indices obtained through the LCM method, we can consider these PPEs as having a reasonably low value. Thus, while acknowledging that individual estimates are systematically biased, we suggest that our results support the use of regression equations to predict actual shapes from periosteal shape indices to obtain sample means.

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obtained using the LCM method, and we obtain precise estimates of the actual mean J. We replicated the regression equations obtained in previous research that predict actual CSG from periosteal CSG. Even using a much smaller sample, the results are largely similar. The various regression equations obtained, using all bones or bone-specic samples, produce parameter estimates so close to the real data that samples of hundreds or more would be needed to detect the difference with the actual data. We have empirically shown that a similar result holds for the shape index Imax/Imin. Although individual estimates of Imax/Imin are systematically biased, estimated sample parameters are reasonably close to actual values. Finally, our results suggest thatwhen we base the regression equations on samples that do not greatly differ from the control sample genetically, geographically, and in health and nutritional environmenta general equation can be used for all bones. In fact, categorical factors such as the specic bone used, sex, and the period from which the sample was derived do not interact signicantly with the slope of the regression. It should be noted that estimating the effect of the medullary cavity on CSG properties eliminates the possibility of investigating differences at the individual level or within and between populations due to genetic, ontogenetic, nutritional, and health factors. However, our results support the use of regression equations to estimate average bending rigidity and shape indices from periosteal CSG in the study of behaviorally related changes in robusticity of ancient populations.

ACKNOWLEDGMENTS
We would like to thank Libby W. Cowgill and Christopher B. Ruff for providing their original data. Thanks to Emiliano Bruner, Vincenzo Formicola, Brigitte M. Holt, Ethan Kalosky, Damiano Marchi, and Curtis B. Storlie for useful comments and suggestions during the writing of this article. Thanks to the two anonymous reviewers and the editor of this journal for greatly improving with their comments the earlier version of this manuscript.

LITERATURE CITED
Alexander RMCN. 1982. Optima for animals. London: Edward Arnold. Bertram JEA, Biewener AA. 1988. Bone curvature: sacricing strength for load predictability? J Theor Biol 131:7592. Bouvier M. 1985. Application of in vivo bone strain measurement techniques to problems of skeletal adaptation. Yearb Phys Anthropol 28:237248. Bridges PS. 1985. Changes in long bone structure with the transition to agriculture: implications for prehistoric activities, Ph.D. dissertation. University of Michigan. Bridges PS. 1989. Changes in activities with the shift to agriculture in the southeastern United States. Curr Anthropol 30:385394. Bridges PS. 1996. Skeletal biology and behavior in ancient humans. Evol Anthropol 5:112120. Carlson KJ, Grine FE, Pearson OM. 2007. Robusticity and sexual dimorphism in the postcranium of modern hunter-gatherers from Australia. Am J Phys Anthropol 134:923. Carlson KJ, Sumner DR, Morbeck ME, Nishida T, Yamanaka A, Boesch C. 2008. Role of nonbehavioral factors in adjusting long bone diaphyseal structure in free-ranging Pan troglodytes. Int J Primatol 29:14011420. Churchill SE. 1994. Human upper body evolution in the Eurasian Later Pleistocene, Ph.D. dissertation. University of New Mexico.

CONCLUSIONS
Our results demonstrate that, when comparing two hypothetical samples with the same total area but relative cortical thickness at the opposite ends of human population-level variability, the number of individuals necessary to detect the difference in average bending rigidity would be higher than the sample size usually available in bioarchaological research. As population differences in %CA make little impact on analyses of J, we suggest that, for most samples, the information contained in periosteal contours may be sufcient to characterize trends in average bending rigidity. Given that our theoretical demonstration depends only on the range of population-level variation in cortical thickness and not on the total area of the section, we suggest that the result is likely valid for other long bones such as the humerus and the tibia. Furthermore, if we correct periosteal CSG of a control sample using estimates of MA predicted from periosteal area, individual estimates are comparable with the ones

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Marchi D, Sparacello VS, Holt BM, Formicola V. 2006. Biomechanical approach to the reconstruction of activity patterns in Neolithic Western Liguria. Italy. Am J Phys Anthropol 131:447455. Mays S, Ives R, Brickley M. 2009. The effects of socioeconomic status on endochondral and appositional bone growth, and acquisition of cortical bone in children from 19th century Birmingham. England. Am J Phys Anthropol 140:410416. Nagurka ML, Hayes WC. 1980. An interactive graphics package for calculating cross-sectional properties of complex shapes. J Biomech 13:5964. ONeill MC, Ruff CB. 2004. Estimating human long bone crosssectional geometric properties: a comparison of noninvasive methods. J Hum Evol 47:221235. Pauwels F. 1980. Biomechanics of the locomotor apparatus. Berlin: Springer-Verlag. Pearson OM. 2000. Activity, climate, and postcranial robusticity: implications for modern human origins and scenarios of adaptive change. Curr Anthropol 41:569607. Pearson OM, Cordero RM, Busby AM. 2006. How different were Neanderthals habitual activities? A comparative analysis with diverse groups of recent humans. In: Harvati K, Harrison T, editors. Neanderthals revisited: new approaches and perspectives. New York: Springer. Pearson OM, Lieberman DE. 2004. The aging of Wolff s law: ontogeny and responses to mechanical loading in cortical bone. Yrbk Phys Anthropol 47:6399. Rockhold LA. 1998. Secular change in external femoral measures from 1840 to 1970: a biomechanical interpretation, M.A. thesis. Knoxville: University of Tennessee. Rubin C, Lanyon L. 1987. Osteoregulatory nature of mechanical stimuli: function as a determinant for adaptive remodeling in bone. J Orthop Res 5:300310. Ruff CB. 1984. Allometry between length and cross-sectional dimensions of the femur and tibia in Homo sapiens sapiens. Am J Phys Anthropol 65:347358. Ruff CB. 1987. Sexual dimorphism in human lower limb bone structure: relationship to subsistence strategy and sexual division of labor. J Hum Evol 16:391416. Ruff CB. 1999. Skeletal structure and behavioral patterns of prehistoric Great Basin populations. In: Hemphill BE, Larsen CS, editors. Prehistoric lifeways in the Great Basin wetlands: bioarchaeological reconstruction and interpretation. Salt Lake City: University of Utah Press. p 290320. Ruff CB. 2000. Biomechanical analyses of archaeological human skeletons. In: Katzenberg MA, Saunders SR, editors. Biological anthropology of the human skeleton. New York: Wiley. p 71102. Ruff CB. 2003. Long bone articular and diaphyseal structure in Old World monkeys and apes. II. Estimation of body mass. Am J Phys Anthropol 120:1637. Ruff CB. 2006. Gracilization of the modern human skeleton the latent strength in our slender bones teaches lessons about human lives, current and past. Am Sci 94:508514. Ruff CB. 2010. Structural analyses of postcranial remains. In: Morgan ME, editor. Pecos Pueblo revisited: the biological and social context. Cambridge, MA: Papers of the Peabody Museum of Archeology and Ethnology, Harvard University. Ruff CB, Hayes WC. 1983. Cross-sectional geometry of the Pecos Pueblo femora and tibiae-a biomechanical investigation. I. Methods and general pattern of variation. Am J Phys Anthropol 60:359381. Ruff CB, Holt B, Trinkaus E. 2006. Whos afraid of the big bad Wolff? Wolff s law and bone functional adaptation. Am J Phys Anthropol 129:484498. Ruff CB, Jones HH. 1981. Bilateral asymmetry in cortical bone of the humerus and tibiae-sex and age factors. Hum Biol 53:6986. Ruff CB, McHenry HM, Thackeray JF. 1999. Cross-sectional morphology of the SK 82 and 97 proximal femora. Am J Phys Anthropol 109:509521. Ruff CB, Scott WW, Liu AY-C. 1991. Articular and diaphyseal remodeling of the proximal femur with changes in body mass in adults. Am J Phys Anthropol 86:397413. Ruff CB, Trinkaus E, Walker A, Larsen CS. 1993. Postcranial robusticity in Homo. I. Temporal trends and mechanical interpretation. Am J Phys Anthropol 91:2153.

Churchill SE, Formicola V, Holliday TW, Holt B, Schumann BA. 2000. The Upper Paleolithic population of Europe in an evolutionary perspective. In: Roebroeks W, Mussi M, Svoboda J, Fennema K, editors. Hunters of the golden age-the midupper Palaeolithic of Eurasia 30,00020,000 bp. Leiden: University of Leiden. Churchill SE, Weaver AH, Niewoehner WA. 1996. Late Pleistocene human technological and subsistence behavior: functional interpretations of upper limb morphology. Quaternaria Nova 6:413447. Collier S. 1989. The inuence of economic behaviour and environment upon robusticity of the post-cranial skeleton: a comparison of Australian Aborigines and other populations. Archaeol Oceania 24:1736. Collier S. 1993. Sexual dimorphism in relation to big-game hunting and economy in modern human populations. Am J Phys Anthropol 91:485504. Coppa A, Cucina A, Lucci M, Mancinelli D, Vargiu R. 2007. Origins and spread of agriculture in Italy: a nonmetric dental analysis. Am J Phys Anthropol 133:918930. Coppa A, Cucina A, Mancinelli D, Vargiu R, Calcagno JM. 1998. Dental anthropology of Central-Southern. Iron Age Italy: the evidence of metric versus nonmetric traits. Am J Phys Anthropol 107:371386. Cowin SC. 1984. The mechanical and stress adaptive properties of bone. Ann Biomed Eng 11:263295. Cowin SC. 1987. Bone remodeling of diaphyseal surfaces by torsional loads: theoretical predictions. J Biomech 20:11111120. Currey JD. 1982. Bones as a mechanical structure. In: Huiskes R, Van Campen D, De Wijn J, editors. Biomechanics: principles and applications. The Hague: Nijhoff. p 7585. Currey JD. 1984. The mechanical adaptations of bones. Princeton: Princeton University Press. Currey JD, Alexander RMcN. 1985. The thickness of the walls of tubular bones. J Zool 206:453468. Frost HM. 1985. The new bone: some anthropological potentials. Yearb Phys Anthropol 28:211226. Grine FE, Jungers WL, Tobias PV, Pearson OM. 1995. Fossil Homo from Berg Aukas. Northern Namibia. Am J Phys Anthropol 97:151185. Holt BM. 1999. Biomechanical evidence of decreased mobility in Upper Paleolithic and Mesolithic Europe, Ph.D. dissertation. Missouri: University of Missouri-Columbia. Holt BM. 2003. Mobility in Upper Paleolithic and Mesolithic Europe: evidence from the lower limb. Am J Phys Anthropol 122:200215. Lanyon LE. 1987. Functional strain in bone tissue as an objective, and controlling stimulus for adaptive bone remodeling. J Biomech 20:10831093. Larsen CS. 1997. Bioarchaeology. Cambridge: University Press. Lazenby RA. 1990. Continuing periosteal apposition II: the signicance of peak bone mass, strain equilibrium, and agerelated activity differentials for mechanical compensation in human tubular bones. Am J Phys Anthropol 82:473484. Ledger M, Holtzhausen L, Constant D, Morris A. 2000. Biomechanical beam analysis of long bones from late 18th century slave cemetery in Cape Town, South Africa. Am J Phys Anthropol 112:207216. Lovejoy CO, Burstein H, Heiple K. 1976. The biomechanical analysis of bone strength: a method and its application to Platycnemia. Am J Phys Anthropol 44:489506. Macchiarelli R. 1988. Age-related rates and patterns of cortical bone involution in past human populations: a protohistorical Italian example. Riv Anthropol 66:5576. Marchi D. 2004. Cross-sectional geometry of the limb bones of the Hominoidea: its relationships with locomotion and posture, Ph.D. dissertation. Pisa: University of Pisa. Marchi D. 2005. Cross-sectional geometry of the hand and foot bones of Hominoidea and its relationships with locomotor behavior. J Hum Evol 49:743761. Marchi D. 2007. Relative strength of the tibia and bula and locomotor behavior in hominoids. J Hum Evol 53:647655. Marchi D. 2008. Relationships between lower limb cross-sectional geometry and mobility: the case of a Neolithic sample from Italy. Am J Phys Anthropol 137:188200.

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CROSS-SECTIONAL GEOMETRY FROM PERIOSTEAL CONTOURS

Ruff CB, Walker A, Trinkaus E. 1994. Postcranial robusticity in Homo. III. Ontogeny. Am J Phys Anthropol 93:3554. Sladek V, Berner M, Sailer R. 2006a. Mobility in Central European Late Eneolithic and Early Bronze Age: femoral cross-sectional geometry. Am J Phys Anthropol 130:320332. Sladek V, Berner M, Sailer R. 2006b. Mobility in Central European Late Eneolithic and Early Bronze Age: tibial cross-sectional geometry. J Archaeol Sci 33:470482. Sladek V, Berner M, Sosna D, Sailer R. 2007. Human manipulative behavior in Central European Late Eneolithic and Early Bronze Age: humeral bilateral asymmetry. Am J Phys Anthropol 133:669681. Sparacello VS, Marchi D. 2008. Mobility and subsistence economy: a diachronic comparison between two groups settled in the same geographical area (Liguria, Italy). Am J Phys Anthropol 136:485495. Sparacello VS, Pearson OM, Coppa A. 2009. Cross-sectional geometry of a warlike Samnite sample from the Alfedena necropolis (Italy). Am J Phys Anthropol [Suppl] 48:244. Stock J. 2002. A test of two methods of radiographically deriving long bone cross-sectional properties compared to direct sectioning of the diaphysis. Int J Osteoarch 12:335342.

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Stock J, Pfeiffer S. 2001. Linking structural variability in long bone diaphyses to habitual behaviors: foragers from southern African Later Stone Age and Andaman Islands. Am J Phys Anthropol 115:337348. Stock J, Pfeiffer S. 2004. Long bone robusticity and subsistence behaviour among Later Stone Age foragers of Fynbos biomes of South Africa. J Archaeol Sci 31:9991013. Stock JT, Shaw CN. 2007. Which measures of skeletal robusticity are robust? A comparison of external methods of quantifying diaphyseal strength to cross-sectional geometric properties. Am J Phys Anthropol 134:412423. Trinkaus E, Churchill SE, Ruff CB. 1994. Postcranial robusticity in Homo. II: humeral bilateral asymmetry and bone plasticity. Am J Phys Anthropol 93:134. Vercellotti G. 2005. Lo scheletro Paleolitico di Villabruna 1. Una fonte di dati su biologia e comportamento di un cacciatore di 14.000 anni fa, Thesis dissertation. University of Pisa. Wescott DJ. 2001. Structural variation in the humerus and femur in the American Great Plains and adjacent regions: differences in subsistence strategy and physical terrain, Ph.D. dissertation. Knoxville: University of Tennessee.

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