AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 115:337–348 (2001)
Linking Structural Variability in Long Bone Diaphyses to
Habitual Behaviors: Foragers From the Southern African
Later Stone Age and the Andaman Islands
Jay Stock* and Susan Pfeiffer
Department of Anthropology, University of Toronto, Toronto, Ontario M5S 3G3, Canada
KEY WORDS
cross-sectional geometry; foragers; Later Stone Age; South Africa; Andaman
Islands; biomechanics
ABSTRACT
The cross-sectional distribution of cortical bone in long bone diaphyses is highly responsive to
mechanical loading during life, yet the relationship between systemic and localized influences on skeletal structure remains unclear. This study investigates postcranial
robustness throughout the body among adults from two
groups of foragers with different patterns and modes of
mobility, to determine whether there is evidence for upper
vs. lower body localization of skeletal robustness. The
samples used for this comparison are from the southern
African Later Stone Age (LSA; n ⫽ 65, male ⫽ 33, female ⫽ 28) dating from ca. 10,000 to 2,000 B.P., and 19th
century indigenous Andaman Islanders (AI; n ⫽ 36,
male ⫽ 17, female ⫽ 16). The LSA were highly mobile
foragers who did not exploit offshore marine resources. In
contrast, the AI had tightly constrained terrestrial, but
significant marine, mobility. Geometric properties of cortical bone distribution in the diaphyses of the clavicle,
humerus, femur, tibia, and first metatarsal are compared between the samples, providing a representation
of skeletal robustness throughout the body. Multivariate ANOVA shows the AI to have significantly stronger
clavicles and humeri, while the LSA femora, tibiae, and
first metatarsals are stronger than those of the AI.
These patterns, in which upper and lower limbs show
biomechanical properties that are consistent with habitual behaviors, suggest localized osteogenic response.
Although postcranial robustness appears to be correlated with overall limb function, the results suggest
that more proximal elements within the limb may be
more responsive to mechanical loading. Am J Phys Anthropol 115:337–348, 2001. © 2001 Wiley-Liss, Inc.
Ever since Wolff (1892) proposed his law of bone
remodeling, evidence has accumulated that bone
structure is highly responsive to mechanical loading
during life. While this research suggests that characteristics of bone structure may be used to make
inferences about behavioral patterns and intensity
in past populations, the abundance of nonmechanical factors that influence bone structure complicates
our ability to do so. Regardless of these complications, significant advances have been made in our
ability to recognize patterns and intensity of human
activity from skeletal remains. The application of
beam theory to the study of mechanical characteristics of human long bones has been particularly informative (Ruff and Hayes, 1983; Bridges, 1989;
Ruff et al., 1984, 1993; Trinkaus et al., 1994, 1998a;
Trinkaus, 1997; Trinkaus and Churchill, 1999a).
This method applies mathematical formulae that
are used to predict the mechanical strength of hollow beams to the cross-sectional geometry of long
bone diaphyses, estimating the mechanical competence of a bone diaphysis under various types of
loading. It has been used to illustrate the variability
in long bone cross-sectional properties that is associated with differences in body size (Ruff, 1984; Ruff
et al., 1993), age (Ruff, 1981; Ruff and Hayes, 1982;
Lazenby, 1990; Bouxsein et al., 1994; Feik et al.,
1997), bilateral asymmetry in limb use (Fresia et al.,
1990; Trinkaus et al., 1994), sex (Feik et al., 1996;
Mays, 1999), and physical activity related to subsistence strategy (Bridges, 1989; Ruff et al., 1984). The
results of these studies emphasize the numerous
influences on long bone diaphyseal form, and underscore the complications of behavioral interpretations
based on skeletal morphology. They do suggest however, that correlations between cross-sectional properties of long bone diaphyses and behavioral patterns may be meaningfully interpreted when
confounding influences on skeletal structure are
controlled.
Some of the most intriguing applications of beam
theory in anthropology have addressed the behavioral and taxonomic implications of postcranial robustness among earlier hominins (Ruff et al., 1993;
©
2001 WILEY-LISS, INC.
Grant sponsor: SSHRC Canada.
*Correspondence to: Jay Stock, Department of Anthropology, University of Toronto, 100 St. George Street, Toronto, Ontario M5S 3G3,
Canada. E-mail: jstock@chass.utoronto.ca
Received 18 October 1999; accepted 3 May 2001.
338
J. STOCK AND S. PFEIFFER
Trinkaus, 1997; Trinkaus and Churchill, 1999b;
Trinkaus and Ruff, 1999a,b). The gracilization of
skeletal elements has been documented throughout
the transition to anatomically modern humans (Ruff
et al., 1993; Trinkaus, 1983a), and between Middle
Stone Age and recent populations (Churchill et al.,
1996a; Pearson and Grine, 1997; Pfeiffer and Zehr,
1996). Although the relationship between lifestyle,
climate, and skeletal robustness is not fully understood (Pearson, 2000), the observed differences in
skeletal robustness suggest that knowledge of the
extent to which habitual behavior influences skeletal morphology is necessary to interpret morphological trends in recent human evolution.
Despite well-documented evidence for temporal
changes in robustness, we do not fully understand
differences between systemic and localized effects on
bone structure. Experimental analyses have demonstrated that in the growing skeleton, exercised animals develop thicker cortical bone throughout the
skeleton, including locations such as the cranium
that are not directly loaded during locomotion
(Lieberman, 1996). Although this provides compelling evidence for systemic regulation of bone robustness, there is significant evidence for localized effects of habitual behavior within the skeleton.
Recent research suggests that osteoblastic activity
may be responsive to low-level strains (Rubin et al.,
2001). This implies that the augmentation of bone
mass may respond to loading encountered during
normal patterns of habitual behavior, where strain
magnitude does not exceed previously defined physiological thresholds (Frost, 1987). Two independent
studies have documented significant bi-lateral
asymmetry in the humeri of elite tennis players
(Haapasalo et al., 1996; Ruff, 1992). Significant levels of bilateral asymmetry have also been documented in many prehistoric human populations, the
highest levels of which have been found in Neandertals and Upper Paleolithic groups (Trinkaus et al.,
1994; Churchill et al., 1996b). There also appears to
be evidence for localized differences in upper and
lower limb robustness between hominins of the Near
Eastern Middle Paleolithic (Trinkaus et al., 1998a).
This evidence suggests that differences in upper vs.
lower limb morphology between groups may be correlated with differences in habitual volitional behaviors and terrestrial mobility. Several studies have
demonstrated a correlation between patterns of
lower limb robustness or diaphyseal shape, and
other lines of evidence for terrestrial mobility (Ruff
and Larsen, 1990) or terrain-dictated loading intensity (Ruff, 1987, 1995). The utility of correlating
morphological traits with archaeological or ethnographic evidence for habitual behavior has been
questioned (Jurmain, 1999). However, in lieu of specific experimental testing on humans, ethnographic
and archaeological evidence provides the best opportunity for anthropologists to build corroborative evidence for the relationships between general patterns of behavior and skeletal morphology.
The potential to expand the interpretive resolution of biomechanical analyses of skeletal remains
depends on our ability to correlate morphological
characteristics throughout the body, and to determine the extent to which morphological characteristics are correlated with known patterns of behavior. This study begins to take such an integrative
approach to the examination of the relationship between postcranial morphology and general categories of habitual behavior in human foragers. Holocene foragers are well-suited to anthropologically
relevant investigations of the relationship between
general patterns of habitual behavior and bone
structure for several reasons: it is reasonable to
assume a gender-based division of labor on the basis
of ethnographic and archaeological evidence (Endicott, 1999); there should be less task specialization
between individuals in foraging groups than is
found in agricultural or horticultural societies; and
it can be assumed that all individuals led active
lifestyles during childhood, with some life-long participation in subsistence activities. In many contexts, foraging populations can be considered to
have been long-time inhabitants of their respective
environments, and foraging groups can be viewed as
relatively homogenous, both culturally and genetically. Furthermore, foraging was the dominant subsistence strategy throughout most of the human
past. The study of functionally relevant skeletal
morphology among foragers should provide an understanding of the extent (and limits) to which we
can interpret general patterns of behavior from
hominin skeletal remains. Future interpretations
would be strengthened by evidence for localized differences in robustness between foragers for whom
we have evidence of differences in habitual behavior
and terrestrial mobility.
Anthropological studies of adult human robustness often compare cross-sectional geometry among
past populations, and make post hoc interpretations
of habitual behavior on the basis of observed morphological differences (Ruff et al., 1984; Bridges,
1989; Collier, 1989). These interpretations are justified by clinical evidence for skeletal responses to
mechanical loading. Patterns of skeletal robustness
have been interpreted as evidence for behavioral
differences between Neandertals and the earliest
modern humans (Trinkaus, 1983b), although recent
analyses suggest that much of the observed morphological variability may be explained by eco-geographic patterning in body proportions (Trinkaus et
al., 1998b; Trinkaus and Ruff, 1999a,b; Pearson,
2000). Within the context of climatic adaptation and
mechanical response to loading, skeletal robustness
is still poorly understood. It remains unclear to what
extent morphological patterns of robustness may be
used to interpret habitual behavior. An alternate
approach to the study of human robustness would be
to compare patterns of postcranial robusticity between samples derived from known populations
with well-documented evidence of habitual behav-
339
DIAPHYSEAL STRENGTH OF FORAGERS
1
TABLE 1. Southern African Later Stone Age sample
Male
Site/location
Female
Site/location
Indeterminate
Site/location
ALB 119
ALB 131
NMB MSk 5t
NMB SS3t
NMB 1273
NMB 1437
SAM-AP 34
SAM-AP 1145
SAM-AP 1878a
SAM-AP 1879
SAM-AP 1889
SAM-AP 1893
SAM-AP 4308t
SAM-AP 4720
SAM-AP 4728a
SAM-AP 4728ct
SAM-AP 4734bt
SAM-AP 4834at
SAM-AP 4834bt
SAM-AP 4843
SAM-AP 5075
UCT 107
UCT 199
UCT 204t
UCT 206a
UCT 209t
UCT 212
UCT 214
UCT 347t
UCT 374
UCT 386
UCT 390
UCT 394
Wilton Rock Shelter
Spitzkop
Matjes River
Matjes River
Matjes River
Matjes River
Touws River Mouth
Robberg
Robberg (cave E)
Robberg
Robberg (cave E)
Robberg
Noordhoek
Kommetjie, Camel Rock
Drury’s Cave
Drury’s Cave
Drury’s Cave
Van Bonde’s Cave
Van Bonde’s Cave
Van Bonde’s Cave
Cape Point, Rooikrans
Knysna
Oakhurst
Oakhurst
Oakhurst
Oakhurst
Oakhurst
Oakhurst
Nelson Bay Cave
Elands Bay
Faraoskop
Faraoskop
Faraoskop
ALB 136
ALB 139
ALB 150
NMB MSk 1t
NMB MSk 2t
NMB SS2
NMB 1241at
NMB 1241bt
NMB 1271
NMB 1274
NMB 1342
NMB 1639
NMB 1640
NMB 1704
NMB 1705a
SAM-AP 1871
SAM-AP 1878b
SAM-AP 3021
SAM-AP 4813
SAM-AP 5095
UCT 200
UCT 201
UCT 202
UCT 206b
UCT 211t
UCT 345
UCT 385
UCT 391
Spitzkop
Spitzkop
Kabeljaaus River Cave
Matjes River
Matjes River
Matjes River
Matjes River
Matjes River
Matjes River
Matjes River
Matjes River
Robberg
Robberg
Plettenberg Bay
Plettenberg Bay
Robberg (cave D)
Robberg (cave E)
Robberg
Bokbaai, Darling
Saldahna
Oakhurst
Oakhurst
Oakhurst
Oakhurst
Oakhurst
Nelson Bay Cave
Faraoskop
Faraoskop
NMB 1705b
SAM-AP 4208a
SAM-AP 4208b
UCT 397
Plettenberg Bay
Drury’s Cave
Drury’s Cave
Faraoskop
1
Site/location as listed in (Morris, 1992). t, sex based on nonpelvic indicators.
iors. If we are to use evidence for patterns of skeletal
robustness to interpret behavior among prehistoric
foragers and fossil hominins, we must first be able to
predict variability in patterns of postcranial morphology among foragers of known habitual behaviors. This study follows this approach, exploring
whether we can predict skeletal robusticity of
groups of foragers who have comparable physiques,
but different patterns of subsistence and mobility.
LATER STONE AGE SOUTHERN AFRICAN AND
ANDAMANESE FORAGERS
The two groups compared in this study are prehistoric Later Stone Age (LSA) foragers of the
Southwestern, Southern, and Eastern Capes of
South Africa, and indigenous Andaman Islanders
(AI) of the Bay of Bengal, between Burma and
Sumatra. The AI and LSA populations were both
small in adult stature and had similar levels of
material technology. Both groups relied upon stone
tool technology, lived in warm climates requiring
minimal clothing, were habitually unshod, and had
no access to domesticates or long-term storage of
food surpluses. Geriatric changes in skeletal structure are not a significant factor in either of these
populations, suggesting that life expectancies were
not high and, presumably, all individuals remained
active until death. Although the populations are distant spatially and temporally, the similarities in
subsistence, age distribution, and material technology minimize many of the possible sources of variation in skeletal robustness.
The Later Stone Age sample used in this study is
derived from archaeological contexts from several
coastal or near-coastal sites dating from 11,000 to
2000 BP (Morris, 1992; Sealy et al., 1992; Churchill
and Morris, 1998; Wilson and Lundy, 1994; Sealy
and Pfeiffer, 2000). At ca. 2000 BP there was a
cultural shift from foraging to pastoralism among
some LSA people, with an increased dependence on
plants and domesticated animals (Parkington et al.,
1986) which may coincide with shifts in bone mass
and stature (Smith et al., 1992). By restricting analysis to individuals dated earlier that 2000 BP, complications relating to this dietary and behavioral
shift are minimized. What we know about LSA subsistence behavior prior to 2000 BP is derived from a
relatively rich archaeological record (Sampson,
1974; Deacon, 1984; Deacon and Deacon, 1999). Although the temporal range of skeletal material
spans approximately 8,000 years, this time period is
characterized by general cultural homogeneity (Deacon and Deacon, 1999; Churchill and Morris, 1998).
Later Stone Age subsistence during this period is
characterized by the hunting of small game, terrestrial foraging, and the intensive exploitation of
coastal marine resources (Deacon, 1993). Sealy et al.
(1992) and Sealy (1997) illustrated the importance
340
J. STOCK AND S. PFEIFFER
TABLE 2. Sample sizes for each skeletal component1
Bone
AI
male
AI
female
Clavicle
Humerus
Femur
Tibia
Metatarsal I
15
16
16
15
12
15
15
15
14
13
1
AI
indet.
LSA
male
LSA
female
LSA
indet.
17
22
18
15
12
2
2
3
16
19
19
15
8
2
Total
65
74
72
59
50
AI, Andaman Islanders; LSA, Later Stone Age, South African; indet., indeterminate.
of marine resources prior to 2000 BP, although there
is significant temporal and geographic variability in
the proportions of marine food eaten. Further archaeological evidence illustrates that the LSA diet
also consisted of a mixture of terrestrial plants,
small terrestrial animals, and small to mediumsized grazers (Deacon, 1984). Using evidence for the
exploitation of terrestrial resources, an early model
predicted that the area over which a band would
have hunted may have been as high as 2,000 –3,000
square miles (Clarke, 1959). Recent stable isotope
analyses of LSA people from the Southern Cape
suggests more delimited movement, perhaps even
territoriality (Sealy and Pfeiffer, 2000). It has been
argued that LSA people became less mobile through
time (Hall, 1990; Jerardino Wiesenborn, 1996). All
studies agree, however, that resources were broadly
distributed, and that exploitation, whether terrestrial or marine, was land-based. The terrain of the
region is generally rocky, with considerable vertical
relief. The exploitation of diverse terrestrial and
marine resources throughout this landscape would
require the negotiation of rugged terrain.
The Andaman Island sample is a protohistoric
skeletal collection derived from the time period immediately following the first permanent European
settlement of the islands, in 1858 (Man, 1878, 1883,
1885; Brander, 1880). The material used in this
study is derived from the islands of Great and Little
Andaman. The entire chain of islands covers approximately 4,000 km2, but individual islands seldom
exceed 25 km in breadth. At the time of British
settlement of the Islands, the Andamanese population was estimated to be between 4,800 – 8,000 people (Myka, 1993). As a result of the recent origin of
the AI remains, there is a significant body of ethnographic literature on which to base interpretations
of Andamanese subsistence behavior, combined
with a relatively short period of colonial occupation.
At the time of initial British settlement, government
officials observed that the Andamanese were divided
into numerous tribal groups that exploited both terrestrial and marine resources. Despite tribal divisions, the groups were morphologically homogenous
(Cappieri, 1974). Dietary staples included various
fruits and yams in addition to wild pigs and honey,
while marine hunting provided fish, dugong and sea
turtles (Myka, 1993). Andamanese villages or base
camps consisted of 20 –50 people, who moved between coastal or forest camps depending upon re-
source availability. Large-scale tribal mobility was
restricted within the islands due to conflict and the
defense of tribal territories. Steward (1955) suggested that the average territory for a group was
approximately 40 km2, which was an adequate
hunting area due to the wealth of resources (cited in
Myka, 1993). The Andamanese frequently used the
canoe for transportation and procuring food. In addition, swimming was a common activity among
both sexes. The children learned to swim almost as
soon as they could walk, and all Andamanese, regardless of age or sex, could spend up to several
hours in the water at a time (Man, 1883).
In summary, the Later Stone Age people, before
2000 BP, appear to have had a relatively low population density characterized by high levels of terrestrial mobility over a large and rugged geographic
area, with no evidence for marine mobility. In contrast, the terrestrial mobility of the Andamanese
was tightly constrained by the small geographic
area of tribal territories and the higher population
density; they can be characterized as having high
marine mobility.
PURPOSE OF THIS STUDY
This paper compares the pattern of long bone robustness in the upper and lower limbs between two
groups of Holocene foragers who are known to have
had different patterns of terrestrial and marine mobility. If bone robustness is under systemic regulation, we would predict either no differences in robustness between elements of the upper or lower
limbs, or differences in robustness that are consistently manifest throughout the body. If humans display localization of osteogenic response to mechanical loading between the upper and lower body, then
we would predict specific patterns of robustness
throughout the body. Foragers with high terrestrial
mobility should have greater diaphyseal strength of
the bones of the lower limb, while foragers with
greater marine mobility (swimming, propulsion of
watercraft) would exhibit greater strength of the
upper limb.
MATERIALS AND METHODS
Osteological samples
The Later Stone Age sample used in this study
consists of 65 adults (Table 1), while the Andamanese skeletal sample consists of 39 adults. The
341
DIAPHYSEAL STRENGTH OF FORAGERS
TABLE 3. Variability in osteometric variables used to estimate body proportions
Andamanese
LSA
Linear dimension (mm)
n
Mean
SD
V
n
Mean
SD
V
F1
Clavicle maximum length
Humerus maximum length
Radius maximum length
Femur maximum length
Femoral head diameter
Tibia maximum length
30
31
24
31
31
29
112.73
270.48
217.88
384.84
37.61
324.93
9.43
15.05
12.61
17.02
2.49
14.18
8.37
5.56
5.79
4.42
6.61
4.36
28
42
32
33
36
27
133.25
283.95
217.69
407.06
39.16
342.41
11.66
18.32
12.38
27.46
2.72
23.03
8.75
6.45
5.69
6.75
6.95
6.73
1.09
1.43
1.04
2.35*
1.10
2.58*
1
F value for variance-ratio test between coefficients of variation.
* Significant differences in V between samples at ␣ ⫽ 0.05.
sex of each individual was assessed on the basis of
pelvic morphology. In a few cases where the pelves
were only partially preserved, the individual was
classified on the basis of other morphological characteristics or discriminant functions derived from
metric characteristics of each of the long bones of the
known sample of the same population. Cross-sectional properties of the Andamanese first metatarsals were provided by Rye (1995). They represent
the same skeletal sample and were collected in a
fashion fully consistent with our work.
There are no skeletons in either sample that appear to be over age 60 years, and most died prior to
age 40 years. Not all skeletons are complete, and
thus not all skeletal elements are represented in
each individual. Sample sizes for each skeletal element are presented in Table 2. Sample sizes for each
bone represent the minimum number of bones for
which both cross-sectional properties and the data
necessary for body size standardization exist.
The LSA and AI populations were similar in a
variety of ways that serve to control for several
factors that are believed to influence the robustness
of long bone diaphyses. Both samples represent people who employed a foraging subsistence strategy,
had similar age distributions, and had characteristically small body size, with mean adult statures
under the fifth percentile of the contemporary American population for both males and females (Abraham, 1979). As a result of this similarity in stature,
there is presumably less absolute variability in
adult body mass, which is likely to influence phenotypic morphology of the long bone diaphyses.
Methods of analysis
The comparison of long bone robustness between
groups focuses on femora, tibiae, humeri, clavicles,
and first metatarsals. The combination of robustness measures at these skeletal locations provides a
representation of the mechanical adaptation in both
the upper and lower limbs. If the pattern of robustness is localized to overall limb function, we would
expect the morphology of the clavicle and humerus
to represent functional adaptation to a variety of
volitional upper limb activities, and the structural
characteristics of the femur, tibia, and first metatarsal to reflect adaptive response to ambulatory behavior.
Cross-sectional properties were calculated at the
midshafts of the maximum lengths of all bones, with
the exception of the tibiae, which were taken at the
location of the cnemic foramen. The cross-sectional
dimensions for approximately half of the LSA sample were derived from CT images taken perpendicular to the diaphysis at the section location. CT
images were taken at Groote Schuur Hospital in
Cape Town and Hydromed Hospital in Bloemfontein, using Siemens Somatom DRH scanners with
window and level settings at 4,000 W and 1,500 L, as
described by Pearson and Grine (1996). The remaining cross-sectional dimensions were obtained using
a method that combines information from casts of
the periosteal dimensions and biplanar radiographs
(Trinkaus and Ruff, 1989). Periosteal casts were
taken at each section location, using polysiloxane
impression material (Exaflex威, GC America). The
casts were scanned and enlarged using a flatbed
scanner. Biplanar radiographs were used to measure four cortical thicknesses at the section location
of each bone, in anatomical planes perpendicular to
the diaphyseal long axis. Cortical thicknesses were
corrected for x-ray parallax, scaled, and transcribed
onto the enlarged image of the periosteal cast, and
used to transpose the endosteal boundary of the
cross section in accordance with the periosteal contour of the section. The resulting sections were digitized using a Summagraphics digitizing tablet, and
cross-sectional properties were calculated using a
PC version (Eschman, 1990) of SLICE (Nagurka and
Hayes, 1980).
Cross-sectional properties that were calculated include the total subperiosteal area of the section (TA),
and cortical area (CA), i.e., the proportion of the
section comprised of cortical bone. Cortical area represents the axial compressive and tensile strength of
the section. The percent cortical area (PCA) provides
a representation of the proportion of cortical bone
within the section and is independent of body size.
The most common forms of loading that occur in long
bones during movement are bending and torsion.
The second moment of area represents the bending
strength of the bone in a particular direction. Maximum and minimum second moments of area are
calculated for each section, labeled as Imax and Imin,
respectively. A circularity ratio of Imax/Imin can be
used to determine whether the section is symmetri-
342
J. STOCK AND S. PFEIFFER
TABLE 4. Andamanese vs. Later Stone Age cross-sectional properties1
Andamanese
Bone
Clavicle
AI n ⫽ 31
LSA n ⫽ 32
Humerus
AI n ⫽ 31
LSA n ⫽ 42
Femur
AI n ⫽ 31
LSA n ⫽ 37
Tibia
AI n ⫽ 29
LSA n ⫽ 30
Metatarsal I
AI n ⫽ 25
LSA n ⫽ 20
Property
3
TA/length
CA/length3
Imax/length5.33
Imin/length5.33
J/length5.33
Imax/Imin
PCA
TA/length3
CA/length3
Imax/length5.33
Imin/length5.33
J/length5.33
Imax/Imin
PCA
TA/length ⫻ BM
CA/length ⫻ BM
Imax/length ⫻ BM
Imin/length ⫻ BM
J/length ⫻ BM
Imax/Imin
PCA
TA/length ⫻ BM
CA/length ⫻ BM
Imax/length ⫻ BM
Imin/length ⫻ BM
J/length ⫻ BM
Imax/Imin
PCA
TA/length ⫻ BM
CA/length ⫻ BM
Imax/length ⫻ BM
Imin/length ⫻ BM
J/length ⫻ BM
Imax/Imin
PCA
Later Stone Age
Mean
SD
Mean
SD
Significance
421.26
341.12
428.76
264.10
692.85
1.656
81.02
97.88
75.94
40.16
24.90
65.06
1.656
77.70
190.86
155.35
5,859.09
4,504.28
10,363.38
1.299
81.41
238.16
161.17
9,871.39
3,940.43
13,881.82
2.546
67.74
327.89
187.22
2,061.45
1,583.32
3,644.77
1.316
56.94
96.86
88.60
217.75
126.56
337.82
0.384
7.72
15.36
12.63
11.57
8.22
65.08
0.258
5.94
20.28
18.08
1,291.58
873.39
2,113.97
0.117
4.07
29.54
22.25
2,233.41
934.32
3,000.56
0.397
5.43
41.81
37.09
566.20
400.76
924.94
0.210
7.33
264.38
218.99
197.44
109.21
306.65
1.870
83.34
79.74
62.21
26.81
17.34
44.15
1.563
78.22
210.24
164.17
8,860.28
5,630.76
14,491.05
1.573
78.26
277.04
164.42
14,605.38
5,570.76
20,176.14
2.662
59.96
367.07
190.97
2,402.65
1,993.05
4,395.70
1.213
52.44
54.35
40.48
72.88
45.25
115.29
0.350
7.39
12.77
10.93
8.24
5.26
13.18
0.217
8.13
19.66
16.32
2,062.40
936.21
2,827.56
0.244
5.67
41.28
24.06
4,405.36
1,662.07
5,815.22
0.563
8.330
55.36
22.83
576.26
473.66
1,018.49
0.126
8.308
0.000*
0.000*
0.000*
0.000*
0.000*
0.024*
0.227
0.000*
0.000*
0.000*
0.000*
0.000*
0.098
0.760
0.000*
0.039*
0.000*
0.000*
0.000*
0.000*
0.012*
0.000*
0.592
0.000*
0.000*
0.000*
0.365
0.000*
0.009*
0.689
0.050*
0.003*
0.012*
0.061
0.060
1
AI, Andamanese Islander; LSA, Later Stone Age. Original measurements in mm. TA, total subperiosteal area; CA, cortical area;
PCA, percent cortical area.
* Significant difference based upon ANOVA with ␣ ⫽ 0.05.
cal or asymmetrical in strength characteristics The
sum of any two perpendicular second moments of
area gives the polar second moment of area (J),
which represents the torsional strength of the diaphysis.
There is no current consensus on the most appropriate means of standardizing cross-sectional properties to body size for the bones of the upper body (cf.
Trinkaus et al., 1994; Trinkaus and Churchill,
1999b). The theory behind standardizing properties
to powers of bone lengths has been supported for use
with the humerus (Churchill, 1995). The morphology and loading environment of the clavicle are complicated, and it is not yet apparent how best to
standardize cross-sectional properties of the clavicular diaphysis to body size. In this case, the theoretical foundation for scaling using power formulae is
relevant, although it remains to be seen whether
this is the ideal method for body-size standardizing
cross-sectional properties of the upper limb bones.
Following this reasoning, cross-sectional properties
of the clavicle and humerus were standardized to
bone length3 for total subperiosteal and cortical areas, and length5.33 for second moments of area, using the power equations described by Ruff et al.
(1993).
Various factors have been used to standardize
cross-sectional properties in the lower body, including bone length (Ruff et al., 1993), estimated body
mass (Trinkaus and Ruff, 1999a), and length multiplied by estimated body mass (Trinkaus and Ruff,
1999a; Ruff, 2000). Theoretically, methods that employ an estimate of body mass should be most appropriate when standardizing cross-sectional properties of bones that bear weight during ambulatory
activity, but of lesser utility in long bones of the
upper body which do not regularly support body
mass. As a result, recent research suggests that in
investigations of robustness of the femur and tibia,
cortical areas are best standardized to estimated
body mass with second moments of area standardized to the product of body mass and bone length,
which represents the moment arm length of the limb
segment (Ruff, 2000). Cross-sectional properties of
the femur, tibia, and first metatarsal were standardized to bone length multiplied by estimated body
mass, as estimated by femoral head diameters and
the mean of three regression equations cited in Ruff
et al. (1997).
In order to ensure that the LSA and AI skeletal
samples could be treated as morphologically homogenous populations, coefficients of variation (V) for
DIAPHYSEAL STRENGTH OF FORAGERS
343
Fig. 1. Midshaft polar second moment of area (J) of the clavicle and humerus. Andaman Islander values are significantly
higher than those for the Later Stone Age among both males and
females. Boxes represent the 25th–75th percentile range, with
whiskers extending to the maximum and minimum values within
1.5 box lengths. Outliers are indicated with an X.
osteometric variables related to body size and proportions were compared using the criteria outlined
by Simpson et al. (1960). The ratio method of Lewontin (1966) was used to test the significance of
differences in morphological variability within each
sample.
The significance of differences between the AI and
LSA sample means for cross-sectional properties,
percent cortical areas, and circularity indices was
tested using ANOVA. Differences in these properties between the males and females of each sample
were subsequently contrasted using Scheffé’s post
hoc test, with a significance level of P ⫽ 0.05.
RESULTS
The coefficients of variation (V) for osteometric
variables that represent body size and proportions
Fig. 2. Midshaft polar second moment of area (J) of femur,
tibia, and first metatarsal. Later Stone Age values are significantly higher than those for Andaman Islanders, in femoral and
tibial J values.
344
J. STOCK AND S. PFEIFFER
Fig. 3. Diaphyseal circularity indices of the femoral midshaft.
Later Stone Age femoral diaphyses are less circular than those of
Andaman Islanders.
are presented in Table 3. The observed V values,
which have a mean of 6.37, fall within the range of
4 –10 and satisfy the criteria of Simpson et al. (1960)
for a morphologically homogenous population. Despite this homogeneity, the LSA V values are somewhat higher than those of the Andaman Islanders.
Results of the variance-ratio test (Lewontin, 1966)
between V values indicate that there are no significant differences between the LSA and AI samples in
variability in clavicle, humerus, or radius length. In
contrast, there is significantly greater variability
among the LSA sample in maximum lengths of the
femora and tibiae. The V values indicate, however,
that this trend is the result of greater homogeneity
in femur and tibia lengths among the Andamanese
rather than increased variability in lengths among
the LSA.
Table 4 summarizes the comparisons of sample
means of body-size standardized cross-sectional
properties for the pooled-sex AI and LSA samples.
All bones show significant differences in CA, Imax,
Imin, and J values (Figs. 1, 2) between the groups. An
examination of the distribution of these differences
illustrates that the AI clavicles and humeri are significantly stronger in compressive (CA), bending
(Imax, Imin), and torsional (J) strength (Fig. 1). In
contrast, the LSA femora, tibiae, and first metatarsals are stronger than those of the LSA in bending
(Imax, Imin) and torsional (J) strengths (Fig. 2). The
LSA femora have significantly greater mean cortical
area and total area, illustrating a greater resistance
to compressive loading. The LSA tibiae and first
metatarsals both have significantly higher TA values than the AI, but minimal differences exist in CA.
This illustrates that the amount of cortical bone in
the cross sections is similar between groups, but
among the LSA the cortical bone is situated further
from the section centroid, resulting in a diaphysis
that is more resistant to bending and torsional
stresses.
Despite the many differences in diaphyseal
strength estimates between the LSA and AI, there
are only a few differences in percent cortical area
and diaphyseal circularity. The LSA clavicles are
significantly less circular than the AI clavicles. Although the LSA have proportionally stronger femora
and tibiae, the AI femora and tibiae have a greater
percentage of cortical bone within the section. This
difference results from significantly lower total subperiosteal areas combined with thick cortices and
small medullary cavities within the AI sections. Another significant difference between the groups is in
the circularity of the femur. The LSA femora are
significantly less circular than the AI, a relationship
which is also apparent but not quite significant
among the LSA/AI sex comparisons (Fig. 3).
The results of the comparison between males of
each sample (Table 5) follow a similar pattern to the
results observed among the pooled-sex samples. The
male AI have significantly stronger clavicles and
humeri than the LSA males (Fig. 1), despite the
absence of significant differences in diaphyseal circularity or PCA in either bone. The femora and
tibiae of the male LSA subsample have significantly
stronger Imax, Imin, and J values (Fig. 2) than those
of the AI males. Although the male LSA first metatarsals have larger Imax and J values, these values
do not reach statistical significance. In addition to
the strength differences, circularity indices show
that the male LSA femora and tibiae are less circular than those of the AI males (Fig. 3). The male LSA
tibiae have significantly lower percent cortical areas, but this is combined with significantly higher
TA values, indicating that the cortical bone present
is situated further from the section centroid.
The comparison of the AI and LSA females (Table
6) illustrates a pattern very similar to that of the
males. In this case, the clavicles and humeri of the
Andamanese females are significantly stronger in
compressive, maximum, and minimum bending
strength and torsional strength (Fig. 1). The female
AI clavicles are also significantly more circular than
those of the LSA females. As with the male comparisons, the female LSA femora and tibiae have significantly higher Imax, Imin, and J means (Fig. 2) than
the AI females. The female LSA femora also have
less circular diaphyses and significantly greater total subperiosteal areas than do the AI (Fig. 3), indicating that cortical bone is situated further from the
section centroid. Significantly greater TA values are
also present in the female LSA first metatarsals, a
statistic which is accompanied by larger Imax, Imin,
and J values that do not quite reach significance.
The morphological pattern of robust lower limb
bones among the LSA, and robust upper limb bones
among the AI, is prevalent in all comparisons
whether the sexes are pooled or treated separately.
Differences between the sexes in each sample appear to be manifest only in terms of the overall
345
DIAPHYSEAL STRENGTH OF FORAGERS
1
TABLE 5. Andamanese male vs. LSA male cross-sectional properties
Andamanese males
Bone
Clavicle
AI n ⫽ 15
LSA n ⫽ 16
Humerus
AI n ⫽ 16
LSA n ⫽ 19
Femur
AI n ⫽ 16
LSA n ⫽ 19
Tibia
AI n ⫽ 15
LSA n ⫽ 15
Metatarsal I
AI n ⫽ 12
LSA n ⫽ 8
Property
3
TA/length
CA/length3
Imax/length5.33
Imin/length5.33
J/length5.33
Imax/Imin
PCA
TA/length3
CA/length3
Imax/length5.33
Imin/length5.33
J/length5.33
Imax/Imin
PCA
TA/length ⫻ BM
CA/length ⫻ BM
Imax/length ⫻ BM
Imin/length ⫻ BM
J/length ⫻ BM
Imax/Imin
PCA
TA/length ⫻ BM
CA/length ⫻ BM
Imax/length ⫻ BM
Imin/length ⫻ BM
J/length ⫻ BM
Imax/Imin
PCA
TA/length ⫻ BM
CA/length ⫻ BM
Imax/length ⫻ BM
Imin/length ⫻ BM
J/length ⫻ BM
Imax/Imin
PCA
Later Stone Age males
Mean
SD
Mean
SD
Significance
427.58
347.24
459.03
280.63
739.67
1.634
80.62
102.36
80.29
43.69
27.93
71.63
1.572
78.60
197.71
161.80
6,603.19
4,988.11
11,591.30
1.323
81.85
247.39
171.34
10,999.68
4,531.93
15,531.61
2.458
69.44
338.84
189.27
2,277.57
1,765.45
4,043.02
1.303
55.51
108.11
108.76
262.43
146.22
403.58
0.286
7.93
12.95
10.74
10.76
6.51
16.88
0.167
5.94
18.41
17.34
1,195.95
809.30
1,924.40
0.121
4.52
24.39
16.68
1,407.25
650.89
1,807.60
0.363
5.20
40.34
35.85
515.75
343.94
787.82
0.227
6.16
253.82
213.76
185.65
105.10
290.76
1.819
84.58
84.49
67.21
30.17
20.19
50.36
1.492
79.94
213.53
168.09
9,964.99
5,942.27
15,907.26
1.684
78.79
292.71
175.82
17,697.10
6,287.62
23,984.72
2.914
60.64
362.45
197.64
2,683.78
2,237.83
4,921.62
1.218
55.05
45.87
34.45
60.42
38.07
94.32
0.390
6.05
11.57
8.66
8.33
4.76
12.76
0.179
7.10
16.62
16.10
1,851.61
908.50
2,594.06
0.206
5.38
41.88
25.85
3,732.85
1,882.19
5,307.69
0.599
8.96
38.27
21.78
568.91
575.77
1,097.23
0.159
8.41
0.000*
0.000*
0.000*
0.000*
0.000*
0.591
0.559
0.003*
0.009*
0.001*
0.006*
0.001*
0.776
0.961
0.137
0.738
0.000*
0.012*
0.000*
0.000*
0.374
0.007*
0.950
0.000*
0.002*
0.000*
0.069
0.013*
0.772
0.954
0.446
0.102
0.222
0.793
0.999
1
AI, Andamanese Islander; LSA, Later Stone Age. Original measurements in mm. TA, total subperiosteal area; CA, cortical area;
PCA, percent cortical area.
* Significant difference based upon ANOVA with Scheffé’s post hoc test, ␣ ⫽ 0.05.
strength of individual skeletal elements, rather than
the overall pattern of robustness throughout the
body. The greatest differences in cross-sectional geometry appear to be in the most proximal elements.
This is best illustrated in the diminishing levels of
significance observed among the femora, tibiae, and
first metatarsals.
DISCUSSION
This study was designed to explore systemic and
localized variability in the pattern of long bone robustness throughout the upper and lower limbs, between two groups of foragers who are known to have
had different patterns of terrestrial and marine mobility. Our results illustrate that, despite broad similarities in body size and subsistence strategy between the Andaman Islanders and Later Stone Age
samples, there remain significant differences in the
pattern of long bone robustness throughout the
body. The comparisons of cross-sectional properties
illustrate that in the upper body, AI long bone diaphyses are significantly stronger than those of the
LSA sample. In contrast, in the lower body, the LSA
long bones are significantly more robust than those
of the AI sample. These differences apply to both
sexes. The most significant and consistent differences are in maximum bending and torsional
strengths, which represent a bone’s resistance to
dynamic loading.
When compared to the Andamanese data, the significantly stronger femora, tibiae, and first metatarsals of both the LSA males and females follow the
morphological pattern that we would predict on the
basis of the model of osteogenic response to localized
loading factors, and based on the evidence for behavioral differences between the groups. This relationship is consistent in both sexes, suggesting that the
LSA people were more terrestrially mobile as a
group, with a range and/or intensity of seasonal
transhumance that was significantly greater than
that of the Andamanese. The more circular femoral
diaphyses of the Andamanese contrast with the
more asymmetric diaphyseal strengths among the
LSA, providing support for the correlation between
shaft shape and terrestrial mobility. The rugged
terrain of coastal southern Africa may have influenced the strength properties of the lower limb
among the LSA people, but the comparisons possible
in the current study are insufficient to differentiate
346
J. STOCK AND S. PFEIFFER
TABLE 6. Andamanese female vs. LSA female cross-sectional properties1
Andamanese females
Bone
Clavicle
AI n ⫽ 15
LSA n ⫽ 17
Humerus
AI n ⫽ 15
LSA n ⫽ 22
Femur
AI n ⫽ 15
LSA n ⫽ 18
Tibia
AI n ⫽ 14
LSA n ⫽ 15
Metatarsal I
AI n ⫽ 13
LSA n ⫽ 12
Property
3
TA/length
CA/length3
Imax/length5.33
Imin/length5.33
J/length5.33
Imax/Imin
PCA
TA/length3
CA/length3
Imax/length5.33
Imin/length5.33
J/length5.33
Imax/Imin
PCA
TA/length ⫻ BM
CA/length ⫻ BM
Imax/length ⫻ BM
Imin/length ⫻ BM
J/length ⫻ BM
Imax/Imin
PCA
TA/length ⫻ BM
CA/length ⫻ BM
Imax/length ⫻ BM
Imin/length ⫻ BM
J/length ⫻ BM
Imax/Imin
PCA
TA/length ⫻ BM
CA/length ⫻ BM
Imax/length ⫻ BM
Imin/length ⫻ BM
J/length ⫻ BM
Imax/Imin
PCA
Later Stone Age females
Mean
SD
Mean
SD
Significance
414.51
334.59
396.46
246.46
642.92
1.679
81.45
93.10
71.29
36.39
21.66
58.05
1.746
76.73
183.56
148.48
5,065.39
3,988.20
9,053.59
1.272
80.95
228.27
150.28
8,662.52
3,306.68
11,969.20
2.640
65.93
317.78
185.34
1,861.96
1,415.19
3,277.15
1.328
58.27
86.53
334.59
160.15
103.77
254.67
0.477
7.74
16.69
13.16
11.54
8.81
19.96
0.310
5.98
20.17
16.74
857.00
616.38
1,430.74
0.109
3.63
32.17
22.79
2,359.72
766.61
2,967.14
0.422
5.25
42.11
39.56
554.54
385.98
914.92
0.201
8.29
273.70
223.61
207.84
112.83
320.67
1.915
82.25
76.13
58.46
24.38
15.05
39.43
1.638
77.01
206.77
160.03
7,694.20
5,301.96
12,996.16
1.456
77.69
261.37
153.03
11,513.66
4,853.90
16,367.56
2.410
59.27
369.91
186.87
2,229.65
1,842.41
4,072.06
1.209
54.94
60.71
45.70
82.77
51.66
132.37
0.316
8.43
12.80
11.14
7.20
4.60
11.48
0.221
8.94
22.38
15.95
1,604.22
871.35
2,279.91
0.232
6.05
35.34
15.90
2,404.87
1,038.47
3,285.52
0.402
7.91
65.05
23.32
528.71
340.61
853.66
0.107
8.02
0.000*
0.000*
0.000*
0.000*
0.000*
0.024*
0.227
0.005*
0.010*
0.004*
0.022*
0.006*
0.556
1.000
0.013*
0.271
0.000*
0.000*
0.000*
0.063
0.344
0.090
0.988
0.045*
0.011*
0.018*
0.610
0.104
0.075
1.000
0.400
0.077
0.184
0.459
0.131
1
AI, Andamanese Islander; LSA, Later Stone Age. Original measurements in mm. TA, total subperiosteal area; CA, cortical area;
PCA, percent cortical area.
* Significant difference based upon ANOVA with Scheffé’s post hoc test, ␣ ⫽ 0.05.
between morphological correlates of rugged terrain
vs. long distance terrestrial mobility.
The strong clavicles and humeri of the Andaman
Islanders are consistent with expectations based on
their observed mobility that is based on the offshore
exploitation of food resources. The gathering of marine resources offshore is dependent on either swimming or the use of watercraft, both of which rely
heavily on the strength of the upper body. The localization of diaphyseal strength properties in the upper body within the AI group, and in the lower body
among the LSA, supports the assertion that the
properties and distribution of postcranial bone mass
within the body is related to general levels of activity among foragers.
The comparisons of AI and LSA cross-sectional
properties demonstrate a positive correlation between the localization of postcranial robustness and
both terrestrial and marine mobility. Although sexual dimorphism exists in both population groups,
the patterns of robustness are similar regardless of
sex, in each sample. This homogeneity of results
within samples illustrates that the morphological
patterns of each sample are characteristic of the
group. This suggests that morphological character-
istics of limb bones may reflect overall patterns of
terrestrial mobility and, as such, may be responsive
to low-level strains produced by daily activities
rather than only peak strains endured under unusually high loads. The observation that the most significant differences appear to be in the more proximal elements may illustrate that these bones are
more responsive to habitual loading, while those
further from the trunk may be more tightly constrained by selective and metabolic factors. This relationship needs to be investigated in greater detail.
This study has illustrated the presence of different patterns of upper vs. lower body long bone robustness between two groups of foragers. Specifically, the Andaman Islanders exhibit greater
strength of the upper limbs in comparison with the
Later Stone Age foragers. This pattern of diaphyseal
strength is likely the result of the Andaman Islanders’ heavy dependence on canoes and swimming for
the offshore exploitation of resources. In contrast to
the Andamanese, the Later Stone Age southern Africans have more robust long bones of the lower
limb, which likely corresponds to a subsistence pattern that was dependent on greater terrestrial mobility, including the exploitation of coastal marine
DIAPHYSEAL STRENGTH OF FORAGERS
resources. The morphological differences between
the LSA and AI are consistent and are statistically
significant. Although the observed morphological
differences are likely the result of differences in
habitual loading of the skeleton during growth and
development, continuing into adulthood, it is not
possible on the basis of available evidence to rule out
long-term genetic adaptation as a cause for the observed morphological variability. Regardless of the
source of this variability, the observed morphological differences follow patterns of long bone robustness that would be predicted from known patterns of
behavioral intensity among these foragers, if we accept common assumptions of biomechanical theory.
This suggests that there is potential for cross-sectional geometry, and its patterning through the
body, to be used to infer behavioral patterns of human groups from the past.
ACKNOWLEDGMENTS
The authors thank the curators of the skeletal
collections used in this study, and those who facilitated the production of CT and radiographic images:
Louise Humphrey and Robert Kruszynski of the
British Museum (Natural History), Alan Morris of
the University of Cape Town, Graham Avery of
the South African Museum (Cape Town), Steve
Benningfield (Groote Schuur Hospital, Cape Town),
Johan Binnemann at the Albany Museum (Grahamstown), Basil MacKenzie (Settler’s Hospital, Grahamstown), James Brink at the National Museum of
Bloemfontein, and Drs. Lamprecht and Gouws (Hydromed Hospital, Bloemfontein). Special thanks are
given to Judith Sealy (University of Cape Town) for
guidance on the LSA collections, and to Leslie Aiello
and Phillip Rye (University College London) for providing the Andamanese first metatarsal data. We
also thank Emõke Szathmáry and two anonymous
reviewers for comments that improved this manuscript.
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