Elemental and isotopic analyses of mammalian fauna from Southern Africa and their implications for paleodietary research.код для вставкиСкачать
AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 76:49-60 (1988) Elemental and Isotopic Analyses of Mammalian Fauna From Southern Africa and Their Implications for Paleodietary Research ANDREW SILLEN Department of Archaeobgy, University of Cape Town,Rondebosch, 7700 South Africa KEY WORDS Strontium, Carbon isotopes, Bone, Diet, Mammals ABSTRACT Elemental analyses of mammalian bone (e.g., strontium-calcium ratios, or Sr/Ca) distinguish between herbivores and carnivores; however, the relationships among herbivores are unclear. To study this question, a modern faunal sample from the Nagupande Tsetse Control Area (Zambezi drainage, Northwestern Zimbabwe) was used. This collection has the advantage of well-established geographical controls in addition to a varied fauna, which includes both bovids and suids. The grazinghrowsing dietary status of each species was ascertained by means of isotopic analysis of carbon. Clear differences were seen in the 613C of grazing and browsing animals; a specialized grazer was found to have significantly lower Sr/Ca than less specialized grazers and browsers. In this study it was also possible to examine differences in Sr/Ca by sex; female warthogs were found to have significantly lower Sr/Ca than males. The variation in certain animal groups was found to be abnormal. Implications for reconstruction of prehistoric human diets using trace-element techniques are discussed. The application of trace-element relationships in food chains, such as strontium-calcium ratios (Sr/Ca)and multielement studies, to dietary reconstruction has been hampered by the lack of background information on modern animals from natural settings. The physiological rationale for using Sr/Ca as a paleodietary technique is well-established and documented in a large biochemical literature (for reviews, see Wasserman and Comar, 1961; Wasserman, 1977; Sillen and Kavanagh, 1982);yet these data are no substitute for measurements of wild animals in the environment. For example, recent studies of North American mammals have demonstrated that the SdCa of wild specimens of white-tailed deer are more variable than that of laboratory animals (Price et al., 1985). Moreover sex differences among some wild animals do not appear to conform to expectations based on laboratory models. Although some data exist on the Sr/Ca of wild animals, they were generally not collected with the aim of developing background information for paleodietary research. A prominent example is the study of 0 1988 ALAN R. LISS, INC. Elias et al. (19821, who examined the Pb/Ca, Sr/Ca, and BdCa of herbivores and carnivores from Thompson Canyon, a subalpine ecosystem in the High Sierras. The principal aim of the study was to establish the input of industrial lead into this remote ecosystem. As part of the research strategy, the biopurification of calcium in this foodchain was established not only for lead, but also lead in comparison to strontium and barium. For example, there was a fourfold reduction in Sr/ Ca from sedge leaves to voles; pine martens, feeding on voles, had a further sixfold reduction in Sr/Ca. The reduction in BdCa in the food chain was even greater. Paleodietary reconstruction depends upon the development of specialized data, which such studies do not provide. In Sr/Ca research, fauna is used in two ways: the demonstration of ideal “herbivore” and “carnivore” diets, against which humans may be compared, and in the assessment of diagenetic change after interment. The rationale for the first category is the development of Received May 13, 1987; accepted August 13, 1987. 50 A. SILLEN TABLE 1. SrlCa in selected masses and legumes’ Grasses Sr (fieq/gm) Ca ( w k m ) Sr/Ca 1.49 1.31 1.19 1.19 1.07 1.01 .95 .95 348 366 390 352 306 235 352 235 4.28 3.58 3.05 3.38 3.50 4.30 3.70 3.96 4.70 3.81 3.57 3.51 3.27 3.20 3.09 2.53 1500 995 1105 1020 995 940 976 718 3.13 3.83 3.23 3.44 3.29 3.40 3.17 3.52 Bromus inermis, Manchar Lolium perenne, Oregon Commercial Lolium perenne, A.lO1 Festuca elatior, Late Otofte Festuca arundinacea, Aka Phleum pratense, Amer. Commercial Phalaris Tuberosa, Harding Grass Dactylis glomerata, Potomac Legumes Trifolium subterraneum, Tallarook Medicago sativa, Caliverde Trifolium fragericum, Salinas Trifolium repens, SlOO Trifolium repens, Dutch White Trifolium pratense, Kenland Trifolium repens, Ladino Lotus corniculatus. Los banos ‘Source:Vose and Koontz, 1959 standards based on species whose diets are well understood against which to compare humans or other species whose diets are unknown. Since background levels of Sr/Ca differ from one terrestrial environment to the next, it is necessary to provide these data wherever the Sr/Ca technique is applied. The second category stems from the observation that bone Sr/Ca may change after interment (Sillen, 1981a,b; Klepinger et al., 1986; Nelson et al., 1986; Pate and Brown, 1986; Price et al., 1986). One way to monitor and correct for this phenomenon is to plot changes in the Sr/Ca through time of species whose diets are understood to be invariate. The documentation of faunal relationships other than herbivore to carnivore comparisons has been largely overlooked. In particular, there is uncertainty regarding the relative Sr/Ca of grazing and browsing mammals, and of omniverous species like certain suids. In the first publication to suggest that Sr/ Ca would be of value in the reconstruction of fossil food chains, Toots and Voorhies (1965) suggested that grazers would have lower Sr/ Ca than browsers for the simple reason that grasses contain less Sr than browse. These authors did not attempt to demonstrate the point with modern animals, yet the notion that dietary strontium alone determine the Sr concentration in skeletons has persisted. However, ample evidence exists that grass also contains less Ca than browse, with the result that the Sr/Ca of the two categories may not differ in any given soil. With few exceptions, the SdCa of pIants are identical to that available to the plants in the form of ground water and soil nutrients. The best data for dicotyledonous plants is on legumes (Menzel and Heald, 1959; Vose and Koontz, 1959), as summarized in Table 1. A review of the biochemical and physiological literature on Sr suggests that dietary SdCa, rather than Sr alone, determines skeletal levels of Sr (Sillen and Kavanagh, 1982). Following this logic, no difference is expected between the Sr/Ca of grazers and browsers from any given environment. To date no study has set out to establish the relative Sr content of grazing and browsing mammals. This research has become feasible particularly for tropical African ecosystems since it is now possible to discriminate very clearly between grazers and browsers using measurements of carbon isotopes (Ambrose and DeNiro, 1986; Vogel, 1978). These measurements provide a n additional quantitative control for browsing and grazing behavior beyond the conventional assessments based on dental morphology, field observation, and stomach content analysis. In order to provide this information, it is necessary to work with a varied faunal collection derived from a well-documented geographic locality. The Nagapande’ faunal collection housed at the Zimbabwe Natural History Museum in Bulawayo meets this specification, and was chosen for this study. ’Current maps adhering to the Names (Alteration)Act of 1983 (Zimbabwe) use the spelling “Nagapande”; thls spelling is used throughout this article except where referring specifically to the historical “Nagupande Tsetse Control Area.” 51 PALEODIETARY RESEARCH AND MAMMALIAN FAUNA / Fig. 1. Map of Zimbabwe showing the Nagupande Tsetse Control Area. Historically, the Nagapande fauna dates from the early 1960s and was collected incidentally to a tsetse-fly control program. The program established a number of hunting stations (of which the Nagupande station was only one), which were intended to control or eliminate game vectors of the tsetse fly (Child and Wilson, 1964). The Nagupande Tsetse Control Area covered an area of 209 square miles at 3,000' in the Zambezi drainage of North Western Zimbabwe (approximately 18"15'S, 27'40'E) (Smithers, personal communication; Fig. 1).Child and Wilson (1964) describe the area: . . undulating country on the headwaters of the Nagupande (sic) ~ river. . .(with) . . . an uneven overlay of windblown Kalahari sand obscuring areas of Karoo soils. The annual rainfall was about 25 to 30 inches. An open mixed species savannah woodland with sparse perennial grasses occurred on the Kalahari sand ridges. Elsewhere the dominant vegetation was mopane woodland in which grass growth was poor and consisted mainly of annual species. Interspersed through the mopane there were areas of scrub thicket dominated by Combretum elaeagnoides while along water courses Acacia spp. were well represented. The eastern end of the area took in part of the open perennial grassland of the Matabolo 52 A. SILLEN TABLE 2. Specimens from Nagapande used in this study Species English name Redunca arundinum (Boddaert, 1785) Trageluphus strepsiceros (Pallas, 1766) Equus burchelli (Gray, 1824) Potumochoerus porcus (Linnaeus, 1758) Phucochoerus aethiopicus (Pallas, 1766) Reedbuck Kudu Zebra Bushpig Warthog flats where trees such as mopane or Acacia spp. were restricted to water courses. There were also a few dambos on the contacts between Kalahari sand woodland and mopane veld where perennial grasses were well represented. Whereas the tsetse control operations in the former state of Rhodesia were ecologically questionable, the mammalian fauna assembled provides various research opportunities. The varied fauna from this one drainage includes reedbuck (Redunca arundinum, Boddaert, 1785), Burchell’s zebra (Equus burchelli, Gray, 1824), kudu (Tragelaphus strepsiceros, Pallas, 1766), bushpig (Potamochoerusporcus, Linnaeus, 17581,and warthog (Phacochoerus aethiopicus, Pallas, 17661, most of which are of known sex. Approximately 90 specimens were examined in this study; a summary is provided in Table 2. In order to evaluate the dependence of each species on grazing or browsing, stable carbon isotopic analyses were performed. The rationale for using carbon isotopes to distinguish between grazing and browsing animals in tropical environments is by now well established (Vogel, 1978; van der Merwe, 1982; Ambrose and DeNiro, 1986). Briefly, plants that fix atmospheric carbon dioxide during photosynthesis initially into a three-carbon molecule (the Calvin, or C3 photosynthetic pathway) fractionate carbon isotopes more than those using a four-carbon molecule (the Hatch-Slack, or C4 pathway). As a result, the two groups have different 13C/12C,or 613C, and the ranges do not overlap. Tropical and savannah grasses follow the C4 pathway, whereas trees, most shrubs, and temperate grasses follow the C3 pathway. Because less significant fractionation occurs in mammals, these differences are perpetuated in mammalian food webs: the practical application is that the carbon of browsing and grazing animals in tropical ecosystems contain distinctive isotopic signatures. In examining the Nagapande fauna, the following questions were addressed: 1)Is it Dossible to detect a difference in the Sr/Ca of Number 10 28 6 13 31 grazing and browsing bovids, and how do any differencesrelate to their grazing and browsing status as indicated by the carbon isotopic signature? 2) Is a similar pattern seen in the Sr/Ca of grazing and browsing suids? 3) Does the Sr/Ca of free-ranging animals, e.g., equids, differ from those of territorial ones? 4) Are there differences in Sr/Ca that are due to sex, and can these differences be related to previously reported field and laboratory observations? 5) How does the pattern of variation within populations compare to those previously reported? Answers to such questions have direct bearing on the research design of paleodietary studies using trace elements. Following a presentation of the methods and results, these implications are discussed in the final section. METHODS For the carbon isotope analyses, diaphyseal cortical bone specimens were demineralized in dilute HC1; the total remaining organic component was recovered, defatted, and converted to pure C02 by combustion and cryogenic separation according to methods described elsewhere (Sealy, 1986).Mass spectrometry was performed using a VG Micromass 602E light-isotope mass spectrometer. Replicate analyses of the same samples give 6I3C values within 0.2%0. Specimens were prepared for elemental analysis of strontium and calcium according to methods described previously (Sillen, 1981a; Sillen and Smith, 1984). Briefly, 4-5 mg diaphyseal cortical bone fragments were weighed with a Perkin-Elmer A D 4 autobalance and digested with 100 pl concentrated nitric acid (Aristar) in 12 x 75 mm borosilicate glass culture tubes at 150°C. The samples were brought to dryness and redissolved in 1 ml 0.2 N HNO3. These solutions provided stocks from which aliquots could be removed for analysis. The digestion procedure was performed in duplicate for each specimen. In 6% of the specimens, the difference in Sr/Ca between duplicates was greater than 10%; in these cases repeat duplicate digestions were analyzed. 53 PALEODIETARY RESEARCH AND MAMMALIAN FAUNA TABLE 3. 613C in Nagapande faunal sample Animal Grazers reedbuck zebra warthog Browsers kudu bushpig N 613~0/00 S.D. 3 3 6 - 8.4 0.3 3 8 -21.1 - 19.6 0.6 0.9 Concentrations of strontium were determined with a Perkin-Elmer model 5000 atomic absorption spectrophotometer (AAS) fitted with an HGA 500 graphite furnace; concentrations of calcium were determined with a Varian AAS using an airlacetylene flame and a matrix consisting of 0.2 N HN03 and 0.1%lanthanum (as LaC13). RESULTS AND DISCUSSION Herbivore 613C Carbon isotopic values for the herbivores are presented in Table 3. A clear difference is seen between the 613C of the grazers, zebra, and reedbuck, and that of the browsing kudu. The mean value of -8.5960 for zebra closely agrees with that reported previously for this species in East Africa (-8.3960,Ambrose and DeNiro, 19861, and is slightly more positive than those reported from southern Africa previously ( x = -9.3960, Vogel, 1978). Reedbuck values have not been reported and it is of interest that the mean carbon isotopic value for this specialized grazer, -6.4%0, is more positive than that of zebra. Vogel(1978) reports a value of -6.0960 for related species, Redunca fulvorufula, the mountain reedbuck. Since C4 grasses average - 12.5960,and the positive shift in 613C from food to consumer collagen is approximately +5.3%0for ungulates2 (Vogel, 19781, the value of -6.4960 is at or near the theoretical maximum for a total grazer. These isotopic data confirm behavioral and other field observations that zebra are somewhat less than specialized grazers (Ansell, 1960; Darling, 1960; Smithers, 1983). For example, dicotyledons have been identified in zebra faeces (Stewart and Stewart, 1970); detailed observations of feeding zebras have also documented the inclusion of herbiage *Although the exact enrichment value for collagen is the subject of continuing discussion (see Bumsted, 19841, I have used the value previously reported specifically for large African mammals. Minor differences in this value do not affect the interpretation of the results. - 6.4 8.5 0.8 0.2 and the pods of at least nine species of shrubs or trees (Brynard and Pienaar, 1960; Smuts, 1972).With minor exceptions, reedbuck have by contrast been observed to be virtually exclusive grazers (Brynard and Pienaar, 1960; Jungius, 1970,1971). Kudu are understood to be somewhat generalized browsers, eating leaves, shoots, and the reproductive parts of woody plants. Only small quantities of grass are accepted (Brynard and Pienaar, 1960; Wilson, 1970; Novellie, 1983). Suid 613C Carbon isotopic values for the suids are also presented in Table 2. The mean values of -19.6960 for the bushpig and -8.9960 for the warthog also agree with recently published values for East Africa (Ambrose and DeNiro, 1986). Bushpigs are omnivorous, generalized feeders. Underground rooting is directly largely at bulbs and tubers (Smithers, 1983).The diet includes ferns, other monocotyledons, and dicotyledons(Phillips, 1926), with extensive utilization of fruit in the summer (Maberly, 1950; Brynard and Pienaar, 1960; Breytenbach and Skinner, 1981). Bushpigs also eat earthworms and the pupae of defoliating insects, carrion, reptile eggs, and young birds (Thomas and Kolbe, 1942; Williemse, 1962; Skinner et al, 1976). One study identified reedbuck hoof and hair in dung (Breytenbach and Skinner, 1981). The omnivorous aspect of the diet may be significant in contributing to the relatively low Sr/Ca (discussed below) for this species. In contrast, warthogs are more strictly vegetarian, living on annual and perennial grasses (Brynard and Pienaar, 1960; Field, 1970; Cumming, 1975). Like zebra, they are partial to freshly sprouting grasses after a burn (Smithers, 1983). Inspection of stomach contents of 32 animals collected in October 1962 a t the Nagupande station revealed grass roots (Loudetia superba) to the almost complete exclusion of other matter (Child, A. SILLEN Fig. 2. Frequency distribution of Sr/Ca in grazing and browsing bovids. The specialized grazer (reedbuck) have slightly lower Sr/Ca than the generalized browser (kudu). The ranges overlap considerably. Fig. 3. Frequency distribution of Sr/Ca in grazing and browsing suids. Browsing, omnivorous bushpigs have lower Sr/Ca than grazing warthogs. Neither distribution is normal (see text for discussion). TABLE 4. S d C a in Nagapande faunal sample cv Animal N Sr/Ca (%) Reedbuck' Kudu (all)' male' female' Zebra Bushpigs3 Warthoes (all)3 male4female4 10 28 7 20 6 13 31 18 11 1.15 1.74 1.78 1.75 3.27 1.86 2.26 2.53 1.79 37 34 22 38 71 27 34 32 26 'Reedbuck and kudu (Student's t test) p = ,0089. 'Male and female kudu (Mann-Whitney U testl p = ,7028 (no significant diff.). "Bushpigs and warthogs (Mann-Whitney U test) p = .0640. 4Male and female warthogs (Mann-Whitney U testl p = .0022. 1965; see also Cumming, 1975). Dicotyledonous plants have been rarely observed; these and perhaps some C3 grasses account for the 6I3C values seen in this study, which are slightly more negative than that of the pure C4 grazing reedbuck they are, in fact, comparable to that of zebra. SrlCa Grazing us. browsing bovids: A significant difference was observed between the Sr/Ca of the specialized grazer, reedbuck, and the generalized browser, kudu (Table 4); however, considerable overlap exists in these distributions (Fig. 2). Clearly Sr/Ca is not as sensitive to grazingbrowsing dietary status as carbon isotopes, where no overlap exists. However, these data support the view that in wild animals total dietary Sr (as opposed to Sr/Ca) is at least a partial determinant of bone mineral Sr/Ca. This suggestion could be confirmed in the future by analysis of the Sr and Ca content of specific plant species and plant parts utilized by these animals. Grazing us. omnivorous suids: In this case the grazing warthog was found to have significantly higher Sr/Ca than browsing, omnivorous bushpigs. Neither distribution was normal (Fig. 3); the demonstration of significance is therefore based on the Mann-Whitney U test rather than the t distribution (Table 4). The relative Sr/Ca of these animals are reversed when compared t o grazing and browsing bovids. Given the discussion of bushpig diets in section 2, the reason is likely to be that bushpigs are also omnivorous: this would have the result of reducing dietary Srl Ca. 55 PALEODIETARY RESEARCH AND MAMMALIAN FAUNA Sr/Ca i n nonruminants: The Sr/Ca of zebra, the only nonruminants in this study, are broadly comparable to those of the bovids (Table 4); however, the mean values are significantly higher than that of the specialized reedbuck. The likely interpretation is that the slight browse component of the zebra diet, indicated by 613C values 2 per mil more negative than reedbuck, provides enough additional dietary Sr to appear in the skeleton. In other words, the difference seen in SrICa between grazers and browsers may occur only when dealing with extremely specialized animals. This hypothesis could be further tested by sampling other sensitive grazers, e.g., roan and sable. Although the sample size is relatively small, the zebra SdCa is characterized by a very wide range (Sr/Ca = 0.97-7.12) when compared to other species reported in this study. There are at least two possibilities to account for this variation, which may also contribute to the high mean SrICa. First, the relatively fast transit time of food in the gut of nonruminants such as a zebra may result in nonrepresentative absorption of dietary Sr/Ca. That is, only the most available alkaline earths may be absorbed, and these may not reflect the total Sr/Ca of the plant material. This explanation seems unlikely, however, when the relative transit time of foods among ruminants themselves is considered. As specialized grazers, reedbuck have a relatively large rumen with very slow transit time. In contrast, kudu have a relatively small rumen, which is adapted to a rapid throughput of food (Hofmann and Stewart, 1972; Giesecke and Van Glyswyk, 1975).The CV in Sr/Ca of these two species is nevertheless similar. A more likely explanation concerns the ranging behavior of the species under consideration. Reedbuck are territorial animals that restrict themselves to well-defined ranges (Burt, 1943; Hediger, 1949; Jungius, 1971). The same may be said for kudu, although there are some significant variations on this theme, which are discussed below (Simpson, 1972). In contrast, zebra are not territorial and range widely over large areas (Smuts, 1972; Smithers, 1983). For the present it seems that the ranging behavior of zebra, coupled with likely differences in Sr/ Ca entering various potential habitats is contributing to the high CV of this species. Differences i n SrlCa by sex: Potential differences in SrICa between sexes of the same species were examined in both kudu and warthogs. From Figure 4 it may be seen that, whereas no significant difference exists in the mean SrICa, female kudus are more variable than males. The CV for males in 22%; that for females is 38%. Among warthogs, males have an average higher SrICa than females, although there is considerable overlap and neither distribution is normal (Fig. 5). In contrast to kudus, males are slightly more variable than females (male CV = 32% female CV = 26%). Since these observations have not been reported before, some discussion of the question of sex differences is provided here. Laboratory studies under controlled conditions have repeatedly demonstrated that 0.10 om 110 1.m zoo zw ldo 530 am sr/m I imo Fig. 4. Frequency distribution of Sr/Ca in male and female kudu. Females are more variable than males. 1.m 1.m zm 240 P/ca ldo am am Am 64 x lmo Fig. 5. Frequency distribution of Sr/Ca in male and female warthogs. Female Sr/Ca is significantly lower than male Sr/Ca. 56 A. SILLEN pregnant or lactating animals have higher SrICa than nonpregnant or lactating controls (Kostial et al., 1969; Blanusa et al., 1970; Price et al., 1986). During pregnancy there is an increase in the absorption of all alkaline earths, and the maintenance of discrimination against strontium in the transport of ions across the placenta (Hartsook and Hershberger, 1973;Jacobson et al., 1978).The result is a significant net increase in the Sr/ Ca ratio of the maternal plasma and, in turn, maternal skeletons. A similar phenomenon occurs during lactation inasmuch as the mammary glands also act as a relative barrier to Sr (Lough et al., 1963; Twardock, 1963). Similar sex differences do not appear to occur in natural human and other animal populations. No difference in SrICa by sex has been seen in studies of modern Western human populations (Turekian and Kulp, 1956). A study of white-tailed deer from midwestern North America has documented decreased Sr/Ca among females (Price et al., 1985). In certain instances it was possible in the present study to measure the SrICa of individual animals observed to be pregnant or lactating at the hunting station itself. A lactating reedbuck was found to have the lowest SrICa among specimens of that species (Sr/ Ca = 0.72). A pregnant kudu was similarly found to be at the lower margin of the respective range (Sr/Ca = 1.39). What explanations may account for the apparent disparity betewen laboratory animals and natural populations? First, all laboratory studies on pregnancy and maternal Srl Ca have been based on a rat model. Rats have significantly faster bone mineral turnover than larger mammals (Bronner and Lemaire, 1969),with the result that any potential effect of pregnancy on the skeleton may be more pronounced in this species. Second, laboratory studies generally include controls for age, diet, and drinking water; these factors may indeed vary for wild populations. For example, male and female kudu have been shown to differ in important details of range exploitation (Simpson and Cowie, 1967). Specifically, males may range less widely on a seasonal basis than females, and this observation has been related to: 1)the greater water requirements of females during the winter dry season, and 2) the need to shelter calves particularly during the same period. Females may thus be more pressured to follow water and cover with the change of seasons, whereas males are not so dected by these constraint^.^ The greater dispersion of females in a mosaic of habitats is thus one hypothesis to explain the greater variability in Sr/Ca seen in the Nagapande specimens. Moreover, it would also explain the similarity in CV between male and female warthog Sr/Ca; in contrast to kudu, there is little difference in the range size of male and female warthogs (Cumming, 1978). As mentioned above, the elevated Sr/Ca seen in pregnant and lactating rats is likely to be related to the high rate of turnover typical of rat skeletons. Rat skeletons may more sensitively reflect elevated serum Sr/ Ca during these physiological conditions. At least one study using rabbits has shown that the turnover of Sr is greater than for Ca (Kshirsagar, 1966);in larger animals Sr may thus be preferentially mobilized during periods of skeletal demineralization as in lactation. This coupled with greater renal clearance of Sr (Spencer et al., 1960; Walser and Robinson, 1963) would result in lower skeletal Sr/Ca in lactating animals. Variability in Sr/Ca: With the exception of zebra, the CVs seen in this study range between 30-35%. These values are broadly comparable to the scant data available elsewhere. It should be noted that the variability seen in these populations is somewhat greater than that seen in laboratory animals and other well-controlled studies (Table 5). This issue has recently received attention elsewhere (Price, 1987). What remains unexplained is the peculiar skewed distribution seen for suids in this study. A search of the biochemical literature on indicates that such distributions are in fact the norm for this element in bone (Eckelmann et al., 1958; Kulp et al., 1959; Kulp, 1960,1961).Similar patterns have been reported for common Sr in the skeletons of Australian sudden-death victims (O’Connor et al., 1980). The skewing of Sr distribution curves to the right received some comment in the epidemiological studies of the 1950s; the phenomenon was ascribed to the different rates at which individuals may equilibrate their bones with diet (Eckelmann et 3This is one possible interpretation, but it should be kept in mind that ranging behavior may be quite variable from one environment to the next. Female kudu live and breed in the Kalahari with no water for months at a time (Child, personal communication). 57 PALEODIETARYRESEARCH AND MAMMALIAN FAUNA TABLE 5. Coefficients of variation (CV in natural, modern human, controlled, and archaeological populations reported previously Natural populations cv (%) Species Price et al., 1985 Sillen, unpublished data wild deer wild gazelle Modern human studies Population U. K. Med. Res. Council, 1959-1970 Thurber et al., 1958 Turekian and Kulp, 1956 Great Britain New York City worldwide Controlled diet studies Schoeninger, 1988 Kyle, 1986 Price, 1985 Sillen, 1981b Sillen, 1981b 32.8 32.0 40.0 Animal model Schoeninger, 1979 Price et al., 1986 Archaeological studies 35.0 45.0 farm mink lab. rats Sample Dutch whalers New Guinea Late Archaic Natufian Aurignacian al., 1958). Moreover, it was noted that it is possible to increase the amount of "Sr per gram of calcium by factors of 100 to 1,000 in soils, but to decrease it by factors of only 2 to 10 (before reaching the effective detection limit). Whereas natural strontium certainly varies far less in a given environment than did "Sr in 1955, the same principle may apply. That is, the potential for increased Srl Ca may be greater than for decreased Sr/Ca in a given environment. A related possibility is that, barring conditions of physiological demineralization as in lactation, Sr accumulates in skeletons with age. The elevated SrICa seen in some individuals may therefore be related to the age curve of the population. (It may be possible to test this idea further since the criteria exist for aging warthog up to 48 months if time of death is known [Child et al., 19651. Examination of the early biochemical literature on common Sr, as well as related data on lead (Pb), provides some evidence for this suggestion. One study of over 400 human samples from England and Wales noted an increase in Sr concentration with age (Bryant et al., 1958; Bryant and Loutit, 1961; see also Thurber et al., 1958). Similar data exist for mule deer from Colorado (Farris et al., 1967). Related data exist for the heavy metal Pb; this element behaves vis a vis calcium in much the same way as Sr (Elias et al., 1982). When controls for pathological demineralization as 19.3 22.0 Date 400 BP 300-1000 BP 3000-700 BC c.10,OOO BC c.17-20,000 BC 25.0-30.0 18.0 11.0-21.1 13.0 9.6 in osteoporosis were incorporated, Pb concentrations in skeletons from ambient exposure have indeed been shown to increase with age (Barry and Mossman, 1970; Gross et al., 1975; O'Connor et al., 1980). These considerations provide a framework for understanding the skewed distributions seen in the suid data. Suids have been shown to have unusual population structure because they are multiparous with a potentially very high reproduction rate; in this respect they differ from other large ungulates (Cumming, 1975). Indeed, one study from western Rwanda has reported warthog longevity to be 17 years, but with a mean length of life of only 2.62 years and a mean life expectancy of 3.03 years (Spinage, 1972). Whereas hunters tend to select large targets, and hence adult animals (Child, personal communication), the sample of warthogs may contain relatively more young adults than the sample of kudu; coupled with the observation that skeletal Sr may increase with age, this would explain the skewed distributions seen in skeletal Sr/Ca for warthogs but not for kudu. IMPLICATIONS FOR PALEODIETARY STUDIES Sr/Ca as atrophic indicator is of interest to prehistorians because it can potentially address the central issue of the origins of human omnivory. The application of SrICa and other trace-elemental relationships to pa- 58 A. SILLEN leoanthropological issues has been hindered, however, by the recognition that the biological signals may become obscured or obliterated after interment. This phenomenon is called diagenesis; efforts to understand it have to some extent dominated the Sr literature (Sillen, 1981a,b, 1986, 1988; Lambert et al., 1982, 1985; Klepinger et al., 1986; Pate and Brown, 1986; Price, 1988)at the inadvertent expense of sufficient attention to the biological assumptions on which the technique is based. The results of the present study do not show that Sr is insensitive to diet and other biological phenomena, but rather that it may be more sensitive than previously thought. This sensitivity implies that it may be necessary to devote more attention to the details of wildlife ecology than has been the case until now. In the past comparisons of human to faunal skeletal material have not considered the natural distributions of Sr in animal species; a consideration of such distributions would be useful firstly in clarifying the theoretical basis for biopurification in food-webs.For example, some confusion has existed over whether the biopurification of Sr is due to the reduced Sr/Ca in meats (from intestinal discrimination by herbivores) or due to the absolute low levels of Sr in certain foods, notably meats and grasses. The answer is probably both the reduced Sr seen in specialized grazers in this study provides evidence that total dietary Sr may well be a factor, but this conclusion needs to be strengthened by analysis of wild plant species from the region? With regard to the research design of paleodietary studies, the Nagapande data bears directly on the selection of appropriate species against which to compare humans, on the detection of diagenesis, especially where carnivores are unavailable, and on the necessary sample size. It is clear from the Nagapande data that zebra are troublesome animals from the point of view of Sr because of their high variability, and this may be related to their ranging behavior. Reedbuck are virtually exclusive grazers with low Sr values, which are not representative of other less specialized bo4This issue should not be confused with the purely methodological one of whether to report bone assays in terms of Sr or SrICa. Since bone ash has a constant Ca value of approximately 30% (Price, 19871,it is necessary to report SrICa values only when whole bone (rather than bone ash) is analyzed. vids. On the other hand, kudu vary similarly to humans and have Sr values more representative of a generalized herbivore. Kudu are therefore an attractive candidate against which to compare human bones at African archaeological and palaeontological sites. It has been previously asserted that measurement of both carnivore and herbivore bones provides the best control for diagenesis (Sillen, 1981a; Sillen and Kavanagh, 1982). One problem with this approach is that carnivores are usually quite scarce at archaeological sites (Price et al., 1985). For critical applications, there is no real substitute for the measurement of carnivores, since this is the only way to ascertain the spacing between known herbivore and carnivore diets; this spacing has been shown to change with diagenesis (Sillen, 1981a,b).Nevertheless, the examination of herbivore bones alone can provide an indication of the presence of diagenesis, if not its extent. That is, if the extent and shape of the biological variability for given taxa in a given environment are understood, they may be compared to fossil taxa. Any deviation from the variability seen in analogous modern taxa would be a clear danger signal. In general, older material is found to have lower variability (Table 5),and this is presumably a diagenetic phenomenon. Finally, the variability seen in the modern fauna in this study makes it possible to estimate the kind of sample numbers that would be required to make confident statements about the diets of prehistoric humans. An approximation for sample number is based on the equation: where: 1 - /3 = the specified power (in this case .go), cx = the level of significance (in this case .05), p1 and ~2 are hypothetical population means, and i? = the estimate of variance (taken from the kudu sample in this study). Thus n = 2('6)2 (1.8 - 1.0) n = 12 (1.96 + 1.29)2 A sample number of at least 12 is therefore appropriate. In summary, the Sr/Ca of modern faunal animals from southern Africa have been shown to vary in relation to diet and sex. PALEODIETARY RESEARCH AND MAMMALIAN FAUNA Ranging behavior may also contribute to variability i n Sr/Ca. Further attention t o the details of wildlife ecology will enhance the application of trace-element techniques to the study of prehistoric human diets. ACKNOWLEDGMENTS I wish to thank Dr. H.D. Jackson, director of the National Museum of Zimbabwe, and Mr. A. Kumirai, the cadet curator of mammalogy, for making specimens available for this study; my thanks also to Ms. J. Sealy, Professor N.J. van der Menve, and Dr. Graham Child for useful suggestions and comments. Mr. J. Lanham, Ms. M. de Rocha Mille, Cedric Poggenpoel, and Dr. R.S. Sparks (Department of Mathematical Statistics, UCT) provided valuable technical support. LITERATURE CITED Ambrose SH and DeNiro MJ (1986) The isotopic ecology of East African mammals. Oecologia (Berlin) 69:395406. 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