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Bone strontium in pregnant and lactating females from archaeological samples.

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Bone Strontium in Pregnant and Lactating Females From
Archaeological Samples
Department of Anthropology, Georgia State University, Atlanta, Georgia
Strontiudcalcium ratios, Diet, Prehistoric native
Because plants and animals consume or absorb different
amounts of strontium and calcium, anthropologists are able to use strontium/
calcium (Sr/Ca) ratios from archaeologically recovered human bone to estimate the relative contributions of meat and plants to paleodiets. Often females
exhibit higher Sr/Ca ratios than males, a fact usually attributed to lower meat
intake among women. However, in vivo and in vitro experiments with laboratory animals show that pregnancy and lactation elevate maternal bone
strontium and depress maternal bone calcium because 1) strontium is discriminated against in favor of calcium in the transport of ions to the placenta and
mammary glands and 2) pregnancy and lactation facilitate absorption of
alkaline earth metals from the gut. In this study, bone Sr/Ca ratios and
strontium concentrations were compared between reproductive-age females,
postmenopausal females, and adult males from two late prehistoric Native
American sites in Georgia: the King site (N = 43) and the Etowah site (N = 51).
At the King site, the mean Sr/Ca ratio of females was over 14%greater than
that of males. At Etowah, the mean strontium level of reproductive-age
females exceeded that of postmenopausal females by almost 25%.Most of the
difference, it is argued, is due to pregnancy and lactation. A dietary preference
among pregnant and lactating women for foods high in alkaline earths,
particularly nuts and corn, may also be partially responsible. Until we assess
the influence variables other than nutrition exert on trace element concentrations, our reconstructions of paleodiets will be suspect.
Among the outgrowths from above-ground
tests of nuclear fission in the 1950s and
1960s was concern over the health hazards
posed by radiostrontium ("Sr) in the ecosphere. Radioactive and stable strontium
behave similarly in food chains (Comar,
1963). Most plants indiscriminantly absorb
strontium and other alkaline earth metals
-calcium, barium, and magnesium-from
the soil (Hutchin and Vaughan, 1968; Sanzharova, 1978). Terrestrial vertebrates, on
the other hand, discriminate against strontium in favor of calcium, since the proteins
necessary for the transfer of ions across the
intestinal mucosa have a lower affinity for
strontium than for calcium (Ingersoll and
Wasserman, 1971; Menczel and Mor, 1972).
This may reflect the fact that calcium is a
more essential nutrient in vertbrate metab-
@ 1989 ALAN R. LISS, INC.
olism than strontium (Comar and Wasserman, 1964; Schroeder et al., 1972; Spencer et
al., 19731.l As a consequence, strontium!
calcium (Sr/Ca) ratios decrease as one moves
up the food chain. Herbivores absorb only a
small amount of the strontium available to
them in plants. Carnivores incorporate even
less strontium than herbivores because of
both continued discrimination and reduced
amounts of strontium in their diets. OmniReceived May 4,1988; accepted December 3,1988.
'The essentiality of strontium in vertebrate metabolism is
controversial. Although most investigators contend that strontium has no known independent metabolic function (Rosenthal,
1981; Sillen and Kavanagh,19821, some argue that, like calcium,
it aids in the formation and maintenance of bones, enamel, and
dentin. Strontium deficiencies are reported to result in depressed
growth, impaired mineralization of bones and teeth, and high
incidence of dental caries (Schroeder et al., 1972; Underwood,
R.L. B m L Y
vores, such as humans, exhibit bone strontium levels intermediate to those of herbivores and carnivores, the amount dependent
in part on the proportion of plants and animals consumed (Toots and Voorhies, 1965).
Anthropologists have used this principle
to infer the relative contributions of meat
and plant foods t o paleodiets (see, for example, Brown, 1973; Gilbert, 1975; Schoeninger, 1979, 1982; Sillen, 1981; Price and
Kavanagh, 1982; Katzenberg, 1984; for comprehensive overviews of the uses of strontium in paleodietary research, see Sillen and
Kavanagh, 1982; Price et al., 1985). Some
studies have been hampered by failure to
take fully into account the influence of variables other than diet on Sr/Ca ratios in
human bone. Diagenesis-postdepositional
change in the chemical composition of buried
bone-is one (see Lambert et al., 1979,1982,
1984,1985; Sillen, 1981; Vlasak, 1982; Pate
and Brown, 1985; Klepinger et al., 1986;
Nelson et al., 1986; Byrne and Parris, 1987;
Price, 1988); disease is another (Sillen and
Kavanagh, 1982; Price et al., 1985);the complexities of strontiudcalcium metabolism
are a third (Comar, 1963; Lengemann, 1963;
Thompson, 1963; Lenihan et al., 1967; Spencer et al., 1973; Elias et al., 1982; Sillen and
Kavanagh, 1982; Price et al., 1986).
Because the gastrointestinal tract discriminates against strontium in favor of calcium in the absorption of alkaline earths,
only 2040% of ingested strontium passes
through the intestinal wall, compared with
4040% of ingested calcium (Comar, 1963).
The unabsorbed strontium is excreted in
feces. Of the strontium absorbed through the
intestinal wall, about 99% is stored in the
bone mineral, or hydroxyapatite (Schroeder
et al., 1972).The remainder is housed in soft
tissue, excreted renally, and transferred to
the placenta and mammary glands (Hartsook and Hershberger, 1973; Kostial et al.,
1969; Spencer et al., 1973; Price et al., 1986).
Sillen and Kavanagh (1982:75)note that
A n important consequence of pregnancy
and lactation may be an alteration in the
strontium levels of maternal skeletons.
The effect has been demonstrated in laboratory animals and occurs when there is
(a) an increase in the absorption of all
alkaline earths and (b) maintenance of
discrimination against strontium in the
transport of ions across the placenta and
mammary glands. The result is a signifi-
cant net increase in the Sr/Ca ratios of the
maternal plasma, and, in turn, maternal
skeletons (Kostial et al., 1969; Blanusa et
al., 1970) [emphasis in the original].'
The authors go on to point out that it is
unclear whether this occurs in humans,
since the rate of bone mineral turnover is
slower than in laboratory animals (Bronner
and Lemaire, 1969). Studies of modern industrial populations have not revealed significant differences in Sr/Ca ratios or in
strontium levels of adult male and female
skeletons (Turekian and Kulp, 1956; Tanaka
et al., 19811, but these data may not be
applicable to prehistoric populations, for
whom it can be assumed that more women
were either pregnant or lactating throughout most of the reproductive years. Price et
al. (1986) estimate that 50% or more of the
adult females in preagricultural samples
were either pregnant or lactating. Studies of
strontium in prehistoric human remains
have almost routinely reported elevated
strontium in adult females (Brown, 1973;
Gilbert, 1975; Lambert et al., 1979, 1982;
Sillen, 1981;Katzenberg, 1984).Usually this
is attributed to dietary differences between
the sexes, often to lower meat intake among
women. (Katzenberg does relate the difference a t the Serpent Mounds site in Ontario
to pregnancy and lactation.)
SrKa ratios will go up when 1)the level of
calcium is decreased, 2) the level of strontium is increased, or 3) both occur simultaneously. With absorption of more calcium
into the placenta and mammary glands,
pregnancy and lactation account for a reduction in the calcium available to maternal
bone (Atkinson and West, 1970). According
to Wasserman et al. (19581,about 85%of the
calcium in maternal milk originates from the
diet; the other 15% comes from the maternal
In vivo experiments by Price and coworkers (1986) show that strontium available to
maternal bone is increased during preg'Because of discrimination against strontium in favor of calcium in the transuort of ions to the mammarv glands. and the fact
that lactose facilitates the absorption of cal"cikn (Lengemann et
al.. 1959: Fournier et al.. 1971). maternal milk has exceDtionallv
low Sr/Ca ratios-n
the order of 0.14 to 0.3 mg'Sr/g Ca
(Rosenthal, 1981). Therefore, even though infants discriminate
against strontium less efficiently than adults, and alkaline
earths are more completely absorbed from liquids than from solid
foods (Marcus and Lengemann, 19621,the skeletons of unweaned
infants also have low SriCa ratios (Lough et al., 1963;Twardock,
1963). At weaning, Sr/Ca ratios rise sharply before declining to
adult values (Sillen and Smith, 1984).
nancy and lactation. In vitro studies by Kostial and colleagues (1969) demonstrate that
this is due to the fact that pregnancy and
lactation produce morphological changes in
the intestinal mucosa and serosa that facilitate the absorption of alkaline earths from
the gut. Their results indicate that the absorption of strontium and calcium in lactating rats was two to three times greater than
in controls. Whether this is sufficient to
account for the elevated bone strontium observed in female skeletons from archaeological sites is not known.
One test for the association between Sr/Ca
ratios and pregnancy and lactation would be
the demonstration that the highest Sr/Ca
ratios occur in females of reproductive age.
In the present study, archaeological samples
from the southeastern United States showed
that reproductive-age women had both elevated strontium and depressed calcium compared to adult males and postmenopausal
females. Lowered calcium is attributed to
discrimination against strontium in favor of
calcium in the transport of ions to the mammary glands. Increased strontium is associated with both enhanced intestinal absorp-
N o r t h Carolina
tion of alkaline earth metals and a dietary
preference among reproductively active
women for foods high in these elements. (The
data do not reveal what portion, if any, of the
difference might be due to dietary choice or
necessity among reproductive-age females,
but it is not unreasonable t o think that dietary supplements would have been beneficial. The Creek Indians, who archaeological
and ethnohistoric accounts show were direct
descendants of the peoples represented by
the skeletal series [Hally, 19881,had taboos
against eating meat at times during pregnancy and throughout menstruation [Swanton, 19221.) We include a cautionary note:
Until we know the effects that normal physiological processes and attendant behaviors
have on trace element concentrations, we
will continue t o reconstruct paleodiets incorrectly.
The samples used in this study were recovered from the Etowah and King sites in
northwestern Georgia (Fig. 1). The Etowah
site is situated on the flood plain of the
Etowah River as it winds westward through
Fig. 1. Location and chronology of the Etowah and King sites.
the Piedmont Province. The site’s location
allowed its inhabitants to exploit three distinct ecological zones-Piedmont, Great Valley, and Appalachian Plateau-as well as to
utilize the rich alluvial valley soil for agriculture (Larson, 1971). Etowah is best known
for the elaborate ceremonial paraphernalia
and design motifs associated with burials in
Mound C and ascribed to the “Southeastern
Ceremonial Complex,” or “Southern Cult”
(Waring and Holder, 1945).These Wilbanksphase interments, numbering 171 individuals, date to the thirteenth and fourteenth
centuries m (Larson, 1971).
In a village area at Etowah, another segment of the population is interred. These
Lamar-phase burials, numbering 76 individuals, date principally to the fifteenth and
sixteenth centuries m (Kelly and Larson,
1957). In sharp contrast to the Mound C
interments, those in the village generally
contained fewer, less exotic, and more utilitarian grave accoutrements. Because the
two burial grounds were not contemporaneous, they do not represent different ranks
within the same social system; but Larson
(1971) is convinced on the basis of grave
goods and demographic composition that
Mound C constituted the superordinate dimension of its society. The social ranks of the
village interments remain unclear.
Thirty-five kilometers west of the Etowah
site, the Etowah and Oostanaula Rivers join
to form the Coosa River. On the alluvial flood
plain of the Coosa, some 50 km west of
Etowah, the King site is located. As at
Etowah, residents at the King site exploited
the diverse biotic communities of the Piedmont, Great Valley, and Appalachian Plateau. Hally (1988) notes that the approximately 3,200 km2 of fertile bottomland
surrounding the site forms one of the largest
tracts of alluvial land in the northwestern
part ofthe state. Cross-dating shows that the
site dates to the sixteenth centurym (Smith,
1987). Because the stockade received only
limited repair and there is little crowding of
architectural features, the site seems to have
been occupied briefly-probably for less
than 50 years (Hally, 1988). One hundred
eighty-nine skeletons were recovered. Artifactually defined low- and high-ranking individuals exhibit no appreciable differences
in trace element concentrations (Brown and
Blakely, 1985).
For the trace element analyses, individuals under 14 years of age were excluded,
since strontium and calcium levels fluctuate
dramatically during growth and development (Sillen and Kavanagh, 1982; Price et
al., 1986). Specimens with little intact cortical bone were also excluded, reducing the
samples to 26 individuals (13 females, 13
males) from Etowah Mound C, 25 individuals (12 females, 13 males) from the Etowah
village, and 43 individuals (19 females, 24
males) from the King site. The Smirnov test,
a two-sample, nonparametric test of ordinally scaled variables, indicated that only
the age structure of Mound C males differed
significantly from the others, having an
overrepresentation of older individuals. To
compare strontium and calcium levels between reproductively active and reproductively inactive females, the samples were
arbitrarily divided into subsamples consisting of individuals under and over age 40
Diagenesis is one of the most nettlesome
problems facing those who use trace element
analysis as a paleodietary technique (Price
et al., 1985; Price, 1988). Lambert et al.
(1985:481) argue that “under any circumstance, the potential effects of diagenesis are
so pervasive that no study of ancient diet
based on inorganic composition [of bone]
should be carried out without proper diagenetic controls.” A growing body of literature
offers contradictory information on the extent to which strontium and calcium are
subject to diagenetic change. Discrepancies
arise in part from different methods of analysis (Lee, 19831,different bones-or parts of
bones-tested (Tanaka et al., 1981; Lambert
et al., 1982; Price et al., 1985),and disparate
geochemical environments from which samples are extracted (Sillen and Kavanagh,
1982; Price et al., 1985).
Vlasak (1982), using microprobe analysis
of cross sections of prehistoric femora, observed homogeneous distributions of strontium throughout the bone sections and concluded that no postmortem enrichment or
depletion had taken place. Calcium was
more mobile, leaching out of bone. In a com3Age of menopause varies interindividually and between populations. Moreover, menopause and “age of mother at birth of last
child”need not be the same; fecund women may choose not to be
fertile (see Bongaarts and Potter, 19831,and infertile females can
be of any age. In the absence of more precise demographic data
from prehistoric populations, adult females under age 40 years
are herein considered the group most likely to be fertile.
parative analysis of 10 elements in modern
and prehistoric bone from the U.S. Midwest,
Lambert et al. (1979) found strontium and
zinc least sensitive to diagenesis; postdepositional depletion of calcium did occur. In a
follow-up study, Lambert et al. (1982) assayed concentrations of strontium, calcium,
and other elements in the porous, trabecular
bone of ribs and the dense, cortical bone of
femora from archaeological sites in Illinois.
The results showed similar levels of strontium in ribs and femora, whereas calcium
loss was greater in ribs than in femora (for a
critical discussion, see Price et al., 1985427).
Other investigators report diagenetic effects on strontium as well as on calcium.
Using inductively coupled plasma atomic
emission spectroscopy to assay strontium,
calcium, and other elements in well preserved Sicilian skeletons, Klepinger and colleagues (1986) observed that calcium exhibited a unidirectional increase with time; the
behavior of strontium was more erratic. Nelson et al. (1986) employed X-ray diffraction
and infrared spectroscopy to evaluate bone
mineral diagenesis in prehistoric and modern marine and terrestrial mammals and
noted contamination by strontium in the
prehistoric samples. Byrne and Parris (1987)
measured bone strontium and calcium at the
Middle Woodland Abbott Farm site in New
Jersey and detected strontium enrichment
by a factor of three to four and calcium
depletion by a factor of 1.1-1.6.
Although the data are ambiguous, the
message is clear: To use strontium and calcium to infer diet or physiological processes
from archaeological samples, one must control for diagenesis by using X-ray diffraction
analysis, infrared spectroscopy,animal bone
standards, or other appropriate means. In
the present study, diagenetic differences
within and between samples from the
Etowah and King sites were negligible for
the following reasons.
1. The geochemical environments at the
locales, even during seasonal flushings, are
virtually identical (S.E. Rose, personal communication); the sites are situated in the
alluvial valley of the same river drainage
(EtowaWCoosa),less than 50 km apart. This
is consistent with the observation of Skougstadt and Horr (1966) that strontium and
calcium levels in soils and water tend to be
uniform in moderately sized drainage systems.
2. At both sites, most inhumations were
primary interment^.^
3. At both sites, all remains were above the
water table.
4.At the King site, burial took place within
a 50 year period.
5. At Etowah, borrow pits used to construct the mound were located in the flood
plain adjacent to the village burials.
6. The pH a t both locales today ranges
between 5.2 and 6.0. Price et al. (1985) point
out that, as bone decays, its constituent elements gradually move into the surrounding
soil matrix, and other elements permeate
into the bone; the higher the pH, the less
bone deterioration will occur (Gordon and
Buikstra, 1981). The high pH levels at the
Etowah and King sites indicate that the soil
was not so acidic that it dissolved bone and
thus released elements to be carried off by
ground water. However, the occasional use of
lime by modern farmers in the region may
have slightly elevated the pH from its aboriginal level.
7. The recent use of superphosphate fertilizers, which are high in strontium
(Schroeder et al., 19721, may have elevated
strontium in bone recovered from cultivated
fields-i.e., the Etowah village and King
site-but the effect should be consistent
across sexes and age groups within the samples.
To reduce further the potential effects of
diagenesis, the following procedures were
adopted for this study.
1. All bone samples were taken from the
diaphyses of well preserved femora.
2. Direct comparisons of Sr/Ca ratios and
of strontium levels are made only within
population samples from a single site.
3. Between-samples observations are
based on relative rather than absolute element concentrations.
‘Seven individuals in the Etowah Mound C samplefrom but
two burials (numbers1 and 1 5 t h a d unusually low levels of zinc.
Depressed concentrationsof zinc have been associatedwith small
stature (Prasad, 19661, endocrine disorders (Miller et al., 19681,
lowered disease resistance (Weinberg, 19721, retarded bone development (Haumontand McLean, 19661, delayed wound healing
(Pones and Strain, 1966). and elevated copper (Guggenheim and
Gaster, 1973). (Because zinc and copper are antagonistic, high
levels of copper ingestion inhibit the absorption of zinc.) No such
patterns were noted in the skeletons from burials 1 and 15. The
only discernible link, which also distinguishes them from other
mound interments, is open-airexposure prior to inhumation (see
Larson, 1971:65;Blakely and Beck, 1981:427). If open-air exposure does reduce zinc, the reason eludes this author.
Although the controls indicate that diagenesis was similar in the groups tested,
they do not measure the extent to which
(1988:57-58) has shown that variability in
Sr/Ca ratios decreases with diagenesis. Coefficients of variability (CVs) for modern
browsing and grazing animals generally
range from 30%to 35%.For modern humans,
CVs are reported between 32% and 40%.
Archaeological human remains have yielded
CVs ranging from 25-30% for a 400-year-old
Dutch sample to 9.6% for a 20,000-year-old
Aurignacian sample. At the King and
Etowah sites, CVs of 2 6 2 6 % for Sr/Ca ratios
and 23-27% for strontium levels suggest
that diagenesis was not a serious problem.
Atomic absorption spectroscopy
With one exception, elements tested included strontium, calcium, copper, magnesium, and zinc. Calcium data are not available for Etowah. The analysis was performed
by atomic absorption spectroscopy, using an
Instrumentation Laboratory atomic absorption spectrophotometer (IL 250) fitted with a
graphite furnace and an air-acetylene flame
system. Standard wavelengths and useful ranges for determination are listed in
Thompson and Reynolds (1978:33-34). For
strontium, atomic absorption spectroscopy
offers fewer chemical interferences than
atomic emission spectroscopy, and the linear
range is comparable (Lee, 1983). To reduce
interferences, lanthanum chloride was
added to the solution. The IL 250 atomic
absorption spectrophotometer has detection
limits of 10-20 parts per billion (ppb) for
strontium, 3-6 ppb for calcium, 5-10 ppb for
copper, 1 ppb for magnesium, and 1-3 ppb
for zinc (Thompson and Reynolds, 1978).
Ten grams of cortical bone were removed
from the midshafts of well preserved femora
using a stainless steel bone saw. Sample
preparation entailed first cleaning the bone
fragments with distilled water. After drying,
the specimens were crushed into a fine powder with a porcelain mortar and pestle. One
gram samples were ashed at 600°C for 3.5 hr.
The bone ash was digested with nitric acid;
the solution then was heated to dryness,
resolubilized with concentrated nitric acid,
and filtered to remove the silica residue. The
filtered samples were diluted t o 50 ml with
deionized water. This procedure, as noted by
Szpunar and coworkers (1978), has the advantage of complete dissolution of bone,
yielding reproducibly higher results than
those obtained by digestion of bone only.
Each specimen was tested twice. Average
difference between replicates for strontium
was 6.3%; average difference between replicates for calcium was 6.4%. Values for each
individual were calculated by averaging the
two readings.
Following Beck (1985), Price et al. (19861,
Sillen (1988), and others, a difference-ofmeans test was chosen to compare the concentrations of elements between population
samples. The 0.05 level of confidence was
used to reject the null hypothesis that no
significant differences existed between samples. Concordant distributions of strontium
between females from the Etowah village
and Mound C permitted those samples to be
pooled for subsequent tests. The same was
true for males from the two burial grounds,
and they too were combined.
Figure 2 depicts the distributions of strontium for males and females at the Etowah
site. The difference is statistically significant. When plotted against age, as shown in
Figure 3, strontium among males is randomly distributed. Females, on the other
hand, exhibit a clear pattern: The broken
line, a best-fit curve by category means
(Zeller and Carmines, 19781, shows that
strontium peaks between ages 20 and 40,
before declining precipitously in the postmenopausal years. Mean strontium level of
reproductive-age females exceeds that of
older females by almost 25%. Table 1 indicates that the difference in bone strontium
between women under and over age 40 years
is statistically significant beyond the 0.005
level of confidence. Strontium exhibits less
variability in females under age 40 years (CV
12.8%) than in any other group, possibly
because of the functional importance of the
absorption of alkaline earths during pregnancy and lactation. For men, age is not a
predictor of strontium content. It is not surprising that the difference between men and
women under age 40 years is significant;
between men and women over age 40 years,
the difference is not significant.
In Figure 4, Sr/Ca ratios at the King site
are plotted against age. Males exhibit little
patterning, except for a wide dispersion in
the forties and fifties largely resulting from
variation in concentrations of strontium.
The coefficient of variability for strontium is
91 D
80 0
Strontium (ppml
Fig. 2. Distribution of strontium by sex among postadolescents from the Etowah site; t
-1.631,49 df, P % 0.05.
30 40
I: :
R( = 25)
30 4 0
70 80
Age in years
Age In years
Fig. 3. Strontium levels by age among postadolescent males and females from the Etowah
site. Broken line is a best-fit curve.
TABLE 1. Mean strontium of postadolescent females and males from the Etowah site (Statistical comparisons are
between groups sharing the same superscript letter)
Females under age 40 years".b
Males under age 40 yearsb.c
Females over age 40
Males over age 40 yearsczd
'P < 0.005. t = 2.981, 23 df.
'P < 0.05. t = 1.942, 22 df.
EP> 0.10. t = 0.038, 24 df.
d P> 0.10. t = -0.304, 25 df.
X Sr
g o
;; 1.25
. .y - .
30 40
70 80
Age in years
Age In years
Fig. 4. Sr/Ca ratios by age among postadolescent males and females from the King site.
Broken line is a best-fit curve.
TABLE 2. Mean strontium, calcium, and Sr/Ca ratios o f postadolescent males and females f r o m the King site
X Sr
X Ca
X Sr/Ca
aDifference of means: t = -2.000, 41 df, P < 0.05
over 28%; for calcium, it is 6%-within the
limits of error indicated by the replicability
data. Among females, Sr/Ca ratios peak in
the twenties and thirties, then decline in the
postmenopausal years. The difference in Sr/
Ca ratios between pre- and post-menopausal
females barely failed to achieve significance
because the subsample of those over age 40
years included two individuals with unusually high Sr/Ca ratios. This may be an artifact of incorrect age assessment, strontium
contamination of the remains, or endogenous differences in strontiumfcalcium metabolism. Nevertheless, the mean Sr/Ca ratio offemales was over 14%greater than that
of males. Table 2 shows that the difference in
SrlCa ratios between the sexes at the King
site is statistically significant and reflects
both higher levels of strontium and lower
levels of calcium among women.
Pregnancy and lactation
Investigators working with living populations have generally found that among
adults strontium and Sr/Ca ratios either
remain constant or increase modestly with
age (Lengemann, 1963; Tipton et al., 1969;
Schroeder et al., 1972; Tanaka et al., 1981).
This finding is at odds with the data €or
females from the Etowah and King sites. The
discrepancy is resolved by assuming that
many women at the archaeological sites
were either pregnant or lactating throughout most of their reproductive years. This
would result in discrimination against strontium in favor of calcium in the transport of
ions to the placenta and mammary glands,
decreasing the amount of calcium available
to maternal bone. Normal bone demineralization during lactation would lower further
the level of calcium in the maternal skeleton.
Enhanced intestinal absorption of alkaline
earths would increase the amount of strontium available to maternal bone, and, given
the ethnographic evidence for the likelihood
of taboos against eating meat a t times during the reproductive cycle (Swanton, 19221, I
suspect that reproductive-age women from
( N = 9)
( N = 11)
(N = 11)
[ N = 12)
( N = 18)
1 0-
Fig. 5. Percent carious teeth per individual between the sexes at Etowah Mound C, Etowah
village, and King site. Range equals 1SD on either side of the mean.
the Georgia sites periodically supplemented
their diet by consuming large quantities of
food rich in alkaline earths. Diet, diagenesis,
and differences in fertility schedules, rather
than differences in reproductive physiology
or age alone, probably account for most of the
variation in strontium observed in reproductive-age females from archaeological sites.5
Among food resources said to be highest in
strontium are fish (Bisel, 1980); freshwater
molluscs (Schoeninger and Peebles, 1981);
nuts; certain medicinally important herbs;
leguminous plants, such as beans; and cereals, including corn (Alexander et al., 1956;
Comar and Wasserman, 1964; Gilbert, 1977,
1985). Fish probably can be ruled out as a
source of dietary strontium, since the edible
5Lambert and coworkers (1982) found bones with thinner
cortices more subject to diagenesis than bones with thicker
cortices. Since females generally have thinner cortices than
males, diagenetic enrichment by strontium and leaching of calcium could partially account for the elevated Sr/Ca ratios of
females, but it does not explain why premenopausal females have
higher Sr/Ca ratios than postmenopausal females. Hormonal
changes with age, however, cannot be ruled out entirely. At
menopause, estrogen levels decline, leading to more frequent and
more severe cases of osteoporosisamong other things (Perzigian,
1973). At the King site, cortical thickness and other measures of
bone rohusticity do decrease with age but not significantly so.
Although far from conclusive, these indices of bone maintenance
do not suggest that estrogen-based changes contributed appreciably to age-related differences in Sr/Ca ratios.
portions store little strontium (Boroughs et
al., 1956). Molluscs also were an unlikely
source because the EtowaWCoosa drainage
was ecologicallyunsuited for shellfish (Wauchope, 1966). Beans and medicinal plants
were consumed but probably not in quantities sufficient to explain elevated strontium
in reproductive-age women a t Etowah and
King (Swanton, 1922).
Corn, as in so many communities throughout the Southeast in the Mississippian and
Historic periods, formed a dietary staple at
both sites-more so at the Etowah site than
at the King site (Kestle, 1988). Corn adversely affects oral health, because the sucrose in corn, like sugar in candy today, leads
to decay (Mormann and Muhlemann, 1981),
and the “sticky” consistency of porridges
made from corn thwarts attempts to clean
the teeth (Cook, 1984; Powell, 1985). Since
the incidence of caries covaries with the
amount of corn consumed, caries can be used
to estimate the relative proportion of corn
in diets (Rose et al., 198416
‘Many studies have asserted a positive correlation between
maize and dental caries (see, for example, Cassidy, 1972; Cohen
and Armelagos, 1984; Rose et al.,19841, but corn was not solely
responsible for the prevalence of caries in aboriginal farming
groups. Other cariogenic agents include genetic susceptibility; a
wide variety of foods and techniques of food preparation; and
levels of such elements as calcium, strontium, fluorine, selenium,
and molybdenum in the soil and water (Schroeder et al., 1972).
As a crude measure of the percent carious consider reproductive processes in paleoditeeth per individual in the Georgia samples, etary research employing strontium.
The present study suggests that pregcarious teeth plus teeth lost antemortem
(most of which were surely carious) were nancy and lactation as well as diet contribdivided by the number of teeth present plus ute substantially to SrfCa ratios and stronthose lost antemortem. The results are pre- tium levels in prehistoric samples. It may
sented in Figure 5. The high incidences of eventually prove possible to use Sr/Ca ratios
caries among females from the King site and to estimate rates of fertility and age of weanEtowah villageboth statistically different ing, as well as dietary preferences attendant
from their male counterparts-suggest that to pregnancy and lactation, in ancient popucorn, although sometimes mineral-poor lations (Sillen and Kavanagh, 1982; Sillen
(Buikstra et al., 19811,may have contributed and Smith, 1984; Price et al., 1986).
Another caveat deserves mention: Stronto bone strontium in those groups. Corn did
not significantly elevate strontium levels in tium and calcium metabolically interact
Mound C females a t Etowah, and it may not with other elements used in paleodietary
have been the principal source of strontium research. For example, linked to diet as well
as to strontium and calcium are barium (Linin any of the populations.
I believe that nuts provided much of the ieki, 19711, cadmium (Jones and Fowler,
dietary strontium. Ethnobotanical and eth- 19801, copper (Guggenheim and Gaster,
nohistoric evidence indicates that nuts made 19731, magnesium (Solomon and Styner,
up a substantial part of the diet throughout 1969), and zinc (Guggenheim and Gaster,
the region (Hudson, 1976; Hatch and Geidel, 1973). To use these elements to infer paleo1983; Beck, 1985). Nuts are high in magne- diets, their relationship to strontium and
sium, which among other things aids in the calcium must be firmly established and fitabsorption of other alkaline earth metals ted to information on Sr/Ca ratios in repro(Solomons and Styner, 1969). This may ex- duction. Because one seldom knows beforeplain why females at both archaeological hand what diets may be encountered in
sites exhibit elevated levels of m a g n e ~ i u m , ~paleoanthropological research, this argues
but nuts were probably a preferred food for the use of an array of elements, including
among pregnant and lactating women be- but not limited to the alkaline earth metals.
Paleodietary reconstruction based solely
cause they are so rich in proteins and carboon trace elements-without macroscopic or
microscopic corroboration from bone, teeth,
hair, or mummified tissue-remains a risky
The results of this study suggest that an- business, and intersite comparisons are
thropologists have often overlooked a com- fraught with difficulties. Only after we conmon cause of variation in Sr/Ca ratios. Even trol for diagenesis, age changes, element
in the absence of a concomitant dietary interactions, and gender-related physiologichange, pregnancy and lactation elevate ma- cal differences can we confidently associate
ternal bone strontium and depress maternal trace elements with diet.8
The hypothesis tested h e r e t h a t pregbone calcium. In an experiment using rats
fed a low-strontium diet, Price and col- nancy and lactation elevate SrfCa ratios in
leagues (1986) found that pregnancy and archaeologically recovered human bone
lactation account for roughly a 6%increase -should be tested at other sites. The results
in strontium, a 2%decrease in calcium, and a of this study should be replicable, since we
9%increase in the Sr/Ca ratio. These figures
are not applicable to humans because of
differences in the rates of bone mineral turn&rhe same problem confronts those using trace elements to
over between rats and humans, nor do the diagnose disease (Brown et al., 1979; Price et al., 1985). It is
axiomatic that, if we are to recognize the "abnormal,"we must
authors address the effects of repeated preg- first be able to recognize the normal. Strontium and calciumcan
nancy and lactation events on Sr/Ca ratios. be used as diagnostic or corroborative tools in paleopathological
Although aboriginal populations seldom lived under
However, their work provides the clearest research.
chronic conditionsof strontium or calcium deprivation,depressed
experimental evidence to date of the need to levels have been observed (Schroederet al., 1972). Hypocalcemia
'Mean concentrations of magnesium at the Etowah site are
1,019.6 ppm for females and 937.6 ppm for males. At the King
site, mean concentrations of magnesium are 1,064.2 ppm for
females and 1,036.0ppm for males.
and hypercalcemiacan be indicative of osteoporosisand tuberculosis, respectively (Shils and Young, 1988). Strontium and calcium are dependent on vitamin D for proper absorption through
the intestinal wall, implicating both elements in osteomalacia
and rickets (Wasserman, 1963). Strontium toxicity is also known
but appears to have been uncommon in preindustrialpopulations
are dealing with reproductive processes common to all human groups. If such studies can
delimit more precisely the contribution of
pregnancy and lactation to bone Sr/Ca ratios, then paleodietary research will be advanced.
A preliminary version of this paper was
presented at the fifteenth annual meeting of
the Paleopathology Association in conjunction with the fifty-seventh annual meeting of
the American Association of Physical Anthropologists, March 23, 1988, in Kansas
City, Missouri. I am grateful to Lane Beck
and Antoinette Brown, who collaborated
with me on earIier trace element anaIyses of
the Etowah and King samples, respectively.
H. James Bronaugh, Department of Chemistry, Georgia State University, kindly carried
out the atomic absorption spectroscopy. I am
indebted to David Hally for loan of the King
site skeletons and to Lewis Larson for loan of
the Etowah skeletons. The thoughtful comments of Lane Beck, Ray Crook, Bettina
Detweiler-Blakely, and anonymous reviewers for the Journal materially improved this
work. This research was supported in part by
National Science Foundation grants BNS8217377 and SOC-7503833 and Georgia
State University grant 8504702.
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