Nitrogen isotopic ecology in southern Africa: Implications for environmental and dietary tracing

MM-7037/87/s3.00

Gmchtmia a Cosmahtmica .4aa Vol. 51, FQ. 2707-2717 6 Pcqpmon JowmbLtd.1987.Riatiin U.S.A.

~i~~e~

JUDITH

+ .oo

isotopic ecology in southern Africa: Irnp~~~~~s for environmental and dietary tracing

C. SEALY*, NZKOLAAS J. VAN DER MERWE, JULL+A. LEE THCXP and JOHNL. LANHAM Dqmtmcnt of Archaeology, University of Cape Town, Rondebosch 7700, !Gxth Africa (~~e~~~ Sep&ewt~er 3, 1986; accepted in revisedform Jidy 13, 1987)

Abatmct-In o&r to establishbaseline nitrogenisotope data for certain Africanemsystems, we have measured the ‘JN/14Nof some 300 marine and terrestrialorganisms. The majority of these specimens come fmm the southwestern Cape, and were chosen to representa cross-sectionof the foods importantin prehistoricdiets

in the region.StsNanalysesof 78 Holocene human skektons from the same area are interpreted in the light of these results. Additional tmestriat animal samples were colkcted firornthe northern and eastern Cape and from Botswana and Ma&i. They represent a wide range of ciimatic and en~~nrnen~ zones, from semi-desert to s&-tropical swamps. The patterning in the values far marine organisms is consistent with pnviously pub&bed data; that for &m%riai organisms, however, is more complex than recent studies have indicated. Our data contirm the proposal that animal P5N values vary with rainfhllzhigh b”N values for herbivores occur in areas nceiving k~ than 400 mm of raiinper annum. We critically examine a recently proposed model expIainingthis phenomenon, and suggestsome additional mechanisms which should be considered. In such arid areas, nitrogen isotope ratios cannot be used as marinc/terreat& indicatom, but may provide some indication of the tmphic kvei of tbe food consumed.Dietarystud& on human eons

can only be uadertakenwith a thoroughapprccWon of the isotopic ecology of the relevant f&web. INTRODUCI-ION

marine and terrestrial IsN/“N averages, with the inof STABLENITROGEN ISOTOPEratios have been used as tention of applying the resu&sto the apron prehistoric human diets. Analyses of more than 100 dietary indicators for prehistoric human populations (DENIRO and EPSTEIN, 1981; SCHOENINGER et al., marine and terrestrial animais from widely scattered 1983; SCHOENINGERand DENIRO 19&r, FARNSWORTH collection sites showed clear diffennces in a”N (see below) between marine and terrestrial organisms et al., 1985; SCHWARCZet al., 1985; AMBROSEand (&,uint = 14.8 4: 2.5960, R = 61, range 9.4 to 23%0; DENIRO, 1986a; HEATON et al., 1986; WALKER and m = 5.9 + 2.2%, n = 27, range 1.9 to 10%~) DENIRo, 1986). This work has dmwn on broadly-based &XOENINGER and DENIRO, 1984). This observation ecological studies of nitrogen isotope distribution (HOERING, 1955; MIYAKE and WADA, 1967; WADA has been used as a basis for determining the amounts of marine foods in the diets of various historic add et al., 1975; WADA and HA?-~oRI, 1976; PANG and NRIAGU, 1977;SWEENEY et ai.. 1978; WADA et al., prehistoric populations, including Alaskan eskimoes, 1981;D~N1~oandE~~, 1981;M~c~oetal.. 1982; Haida and Tlingit Indians from the north-western U.S.A., Havisu agriculturalists from New Mexico and VIRGINIA and DELWICHE, 1982; SCHOENINGERand maniac fmers from Colombia. Prehistoric popuiaRENIRO, 1984; MINAGAWAand WADA, 1984). Howtions sampled include those from the j3anish Mesoever, there remain a number of questions regarding lithic and European N~ti~c as weil as Mesoamerican the d~~bu~on of “N/*‘N in specific ecosystems. In this study, we present the nitrogen isotope ratios of a agriculturalists, Bahamian fisher-gatherers and Californian Indians @CHOENINGERet al., 1983; WALKER range of fauna, flora and human remains from southern and DENIRO, 1986). One study has reconstructed the Africa, as background to continuing archaeological reamounts of fish in the diets of historic Dutch whalers search in the region. (SCHOENINGER, 1986). 15N/“N measurements were Erst used in ar&aeo@y Nitrogen isotope ratios undergo marked trophic level to estimate the proportions of kgumes in terrestriallyba&d prehistoric diets (DENIRO and EPSTEIN,1981; fractionation. Organisms from higher trophic levels are FARNSWORTH et al., 1985; SCHWARCZet al., 1985). enriched in the heavier isotope, compared with their food. Studies of this enrichment have suggested that This specialized application is useful principally in the difference between terrestrial herbivores and carareas where legumes were important cuitigens. Nitrogen isotopes have attracted broader interest as nivores is +3.0 to 3.5%0 (SCHOENINGERand DENIRO, 1984) or +5.0 to 6.0% (AMBROSE and DENIRO, a method of ~~~hi~ marine from terrestrial 1986b). A similar pattern has been observed in marine contributions to sediments (SWEENEY et al., 1978; SWEENEYand KAPLAN, 1980) and to diets (SCHOEN- food chains (MINACAWA and WADA, 1984). This effect l~~~~efaL,1983; WALKER~~~DENIRO,~~~~).O~~ has been used to reconstruct the proportions of animal food eaten by certain historic, pro&-historic and arstudy has attempted to measure the difference between chaeological human populations in East and South Africa (AMBROSEand DENIRO, 1986a). l Corning author. Two recent papers (HEATON et al., 1986; AMBRCJ% 2707

270R

.i. C. Scaly et ul

and DENIRO, 1986b) report the results of further in- of the lighter dietary “N will have been excreted in vestigation into terrestrial nitrogen isotope patterning. urea), and drou~t-tolemnt animals should have higher Their samples include more positive 1sN/‘4N for ter- readings than obligate drinkers. restrial animals than those reported earlier (SCHOENIn this paper. we character% a prehistoric human INGER and DENIRO, 1984). Both papers propose that food-web in terms of nitrogen isotopes. We have colthe effects of water stress on the animals’ metabolism lected samples of marine and terrestrial animals, as account for this. HEATON ef al. (1986) present data well as corresponding plant material, from the southshowing that herbivore 6”N values vary with the rainwestern Cape of South Africa. The animals selected fail of the area they inhabit: the highest values occur were implant in the diets of prehistoric hunter-gathin the most arid regions. AMBROSE and DENIRO erers in this region (PARKINGTON. 1976: BUCHANAN, (1986b) develop a model to explain why aridity leads 1985). Most of the specimens are modern, and were to high 6”N in animals. They examine the role of urea chosen from ecologically undisturbed areas where arin water conservation in mammals, especially the find- tificial fertilizers have not been applied. We have also ings of MAr_oIY f 1972, 1973) and LEVINSKYand BER- analysed a small sample set of prehistoric animal bones from an archaeolo~cal excavation dating to the Iast LINER (1959). One method of conserving water is the 3000 years. The results are essentially the same as those excretion of concentrated urine. Their model postulates that, since the concentration of urea increases disprofor the modem animals from the same area. The patterning in lsN/14N observed in the modem samples is portionately as urine concentration increases, water stress leads to increased urea nitrogen loss. Hence the therefore used to interpret 6”N measurements on preanimal needs to eat a high-protein diet in order to historic human skeletons from this area. Analyses of an initial terrestrial animal sample from maintain nitrogen balance, During the dry season, the protein content of dicot leaves is higher than that of the south-western Cape yielded somewhat unexpected results. Therefore, a larger sample of terrestrial animal dry grass; browsing animals thus generally consume bones from the eastern and northern Cape and from more protein than grazers, and are more able to supply Botswana and Malawi was measured (Figs. I and 2). urea to the kidneys when water-stressed. In addition, These collection sites represent a wide range of southern browsers are able to concentrate their urine to a greater African environments. We have attempted to interpret degree than grazers, and are therefore more droughtour resutts in terms of the previously published model tolerant. Excreted urea is depleted in 15N relative to diet outlined above (AMBROSEand DENIRO, 1986b). In some cases, however, the model did not fully explain (STEELE and DANIEL, 1978). Thus Ambrose and observed variation in “N/14N. We will discuss addiDeNiro’s model predicts that, in arid areas, browsers tional mechanisms to account for these observations. should have higher 615Nvalues than grazers (since more

i

ZIMBABWE

BOTSWANA 6

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,

,,’

/

a-_

,’

i(

.. SOUTH

AFRICA

FIG. 1. Map of southern and south-central Africa showing collection sites

South Africa nitrogen isotopic ecology

FIG. 2. Map of South Africa showing collection sites.

METHODS

ture. Table 1 lists species that were important dietary

Cleaned whole bone samples were decalcified using 1.5% hydrochloric acid, and rinsed in distilled water. Archaeo&$ai samples were further treated with 0.1 M sodium hydroxide to remove humic acids, Modern bones were de-fatted in a chloroform:metbanol:water (2:1:0.8 v:v) solution. The resulting bone collagen was kezedried. Meat samples (including shellfish) were rinsed in distilled water and freeze&i&, plants were rinsed, ground in a kezer-mill at liquid nit-n temperatureandthenficabdrie&TwektofifteenmiUigrams of sample (more in the case of plants) were weighed into a

items for prehistoric hunter-gatherers. The 6”N values range from +7.1 to +19.4%0. This is a larger range than that reported previously (SCHOENINGER and DENIRO, 1984); however, our sample included low trophic level shellfish. These are filter feeders (Choromyfihs) or grazers and detritus feeders (Patella and Ifaliofis). The only value for shellfish previously reported is +7.3%0 for a North Atlantic clam, presumably also a

quartzbr&seai tube with excesscopperoxide, coppermetal and silver foil. The tube was evacuated, sealed and cornbusted at 800°C for six hours, and then allowed to cool slowly. Tbe resulting mixture of CQ, Nz and water vapour was separated cryogenically. The nitrogen yield was measured manometritally and collected by keezing onto coconut charcoal at liquid nitrogen temperatum The isotope ratios were measured on a VG Micromass 602E 90” sa%or double-colkctor mas spectrometer. The results are. expressed in the. d notation, where

Reference gas was calibrated against atmospheric nitrogen and IAEA standards N-I andN-2.6”N measurements are reported relative to atmospheric nitrogen. The reproducibility of the method for homogeneous sample materials is better than 0.2% RESULTS The results

AND DISCU!3SION

of the 615N analyses

are presented

in

Tables I to 4 and Figs. 3 to 5. Marine samples The results for marine samples (Tables I and 2) are in broad agreement with those reported in the litera-

.sMam No.

6l’a (‘/.,I

741 Arctocephalwpu.GZw (Capefur seal) 770 ArctocephaZue puaiZZus(Capefur mall 770 ArctocephalwpueiZZu8(capefur ssiU denweua (jadraes pnguin) 740 Spheniecw 767 Pha&crocom+ capensis (cape cammant) Cape gmmet) 768 M0nur mpeneis 742 Lixa cf. rormda haatder flsh) 766 Lithognathue ZithognatkuaMite rrteerllQas fish) 818 JLlSUS ZQZundii krayflsh~ 1020 PateZlo gmnatina (1-j 1021 Patozklgmnuklti (lilpcel 1022 PateZZoargenviZl& (lirqmt) 1019 naZiotismi&e kibalone~ 1013 ChomnytiZuametiicmaLia blzk d) (11/U)* 1014 Chozw@iZw mwidionaZi8 (blak mssell~3/62)* 1015 Choroqitilue mtiionatis (blbc nuawllWW)* 1017 Chomn@iZue meridionolie(black d) U/82)+ 1018 Chora@iZus meridicmZis (black d)(9/82)* 788 male l.?‘Fecies unku*n) 1920 ielLs hF%Aes UnkIKwn)

15.9 19.3 19.4 16.1 14.6 13.7 18.0 15.3 11.8 8.0 a.4 7.2 7.1 6.2 8.9 8.1

c

0.7 0.4 13.5 12.7

n n c C

c n II n M I4 II II I4 rr l4 n n I4 M

J. C. Scaly et al.

1710

filter feeder (HOERING, 1955). The six samples of Ch+ collected at Elands Bay at different times of the year, were analysed to determine whether or not the seasonal upwelliqs ofcold, nutrient-rich water that occur off the Cape coast affect h”N values; this does not seem to be the case. The crayfish (a kelp bed/rocky subtidal area predator and scavenger) is somewhat more enriched in “N, and carnivorous fish. fish-eating birds and seals most enriched. Trophic level patterning is also iilustrated in Table 2. These organisms were all collected in the Oudekraal kelp bed, off the Cape Peninsula. Four species of algae have an average d”N value of +3.5%: planktonic organisms average +7.6’&: filter feeders t-8.4% and carnivorous o~nisms, scavengers and detritus feeders + 11.O%O.These samples do not include the fish-eating birds and seals shown in Table 1, and hence the upper end of the d15Nrange is somewhat under-represented. When Tables 1 and 2 are taken together, the full range of marine 6”N values is -0.9 to +19.4%. Excluding the algae and plankton, the range becomes +6.8 to +19.4%0(Z= 11.2t3.3%0,n=31).Themeanislower than the value of +14.8 + 2.5k (n = 61) reported by SCHOENINGERand DENIRO ( 1984), because our samples include a large proportion of shellfish and few high trophic level marine mammals. Thus knowledge of the trophic level most heavily exploited in marine-based diets is necessary before nitrogen isotopes can be used for dietary reconstructions in prehistoric coastal pop ulations. ~~~.vr~~~~, ail

Terrestrial sampkx Animals and plants

Many of the terrestrial animals measured in this study (Figs. 3 and 4) have significantly more positive 6rSN values than those reported by !SCHOENINGER and DENIRO (1984). They are also more positive, on the whole, than those reported by HEATON el al. (1986)

sJmL2 M.

517 586 590 515 588 585 584 587

10.1 12.9 10.1 12.2 11.7 9.6 Il.1 10.2

6.8 6.8

518 520 521 522

Average= 11.0

9.5

Avetage= a.4

6.2 9.1

AWmqe 7.6

=

Awage

=

0.9 -0.9 3.2 7.3

3.5

sAMPm M.

61SN ("/.,) collected at cape mint.

2082 2084 2085 2087

Carpabrotus sdulis 1.3 Rhue tosvigati 2.6 Lgucadsndranzanthoconus 1.7 dstomceae ipen. et sp. in&t. i 1.4 CcilM

2088 2090 2091 2092

at OwrcNulven.

Carpabrotus edulis Rhu8 .?p. no. I Rku8 sp. no. 2 Rhus ep. no. .?I

1.2 -3.5 -2.9 -0.2

where the highest 615N reading for a terrestrial animal (and one of only three animals with 6J5N > IO’%) is 14% for an elephant from Damaraland. in northern Namibia. AMBROSEand DENIRO f 1986b) report mean values for each animal species in their large East African sample. Their highest mean di5N value for a herbivore species is IO.6560for elephant and Grant’s gazelle. The highest values for individual herbivorous animals (impala, dikdik and hyrax) are between 12 and 13%. The south-western Cape sample, on the other hand, includes a number of herbivores with &15Nof 15 to 17% (springbok, steenbok, rock hyrax) (Fig 3). Thus there is an almost complete overlap of marine and terrestrial 6”N values in this area. Figures 3 to 5 show the distribution of high terms&al 6t5N values. All readings are on bone collagen. RegionaL groupings emerge clearly, although there may be considerable variation in the dJSN values of animals collected from one location. The plot of b”N va1ues of herbivores for each collecting station against average rainfall for that station (Fig. 6) suggests that 6”N vahzs vary with minfa)l as proposed by HEATONet al. (1986). High disN values (> 10%) occur in regions with leas than 400 mm of rain per year. The same critiCat point was suggested by HEATON et al. for a small sample of elephants from Namibia, and for a larger set of pmhistoric human bones from the interior of South Africa. In areas where the animats have high 6”N values, trophic level patterning is much less apparent, and the intra-species range of di5N values is much greater. There is no clear correlation with other environmental variables such as vegetation type, temperature, etc. The widespread occurrence of high 8”N values in areas some distance from the ocean suggests that oceanic nitrogen input in the form of nit~te-~ng sea spray and mist is not the exphnation for this phenomenon, although such input has been documented for the south-western Cape (STOCKand LEWIS, 1986). In addition, animals from certain areas almost SUI* rounded by sea (the Cape Point Nature Reserve) have low &“N values. We analysed small sample sets of pIants from two areas of the south-western Cape, and animals from the

South Africa nitrogen isotopic cc~logy

2711

FIG. 3. I”N values of animals from the northern and south-western Cape. Scientific names of animals are: steenbok (Raphicew wnpesfris) MFjDT,torbise (Chersina angulata/Psammobatesuntorius verroxii) B, hare (Lepuscaptwis) MF/DT, springhare (Pedetes capensis) G/DT. grey duiker (Syhkapra grimmia) B/IX, dune mole rat (Bathyergussuillus)B/DT, rock hyrax (Rzxnvia capensis)B/M; spriqgbok (Antia%z nwsu~~iulti) IWDT, eland (Taurosmgur oryx) B/DT, hontebok (DMlaliscus &rw donzas)G/OD, baboon (Papio ursinus)MF/OD. Note the similaritybetweenvalues for modern animals from Elands Bay and those foranimllnfromaa~~cxcavationdatedbawan300and3000yeanbefonpreseat(B=~, G = grazer, MF = mixed-feeder, DT = drought-tolerant, OD = obligate drinker.) same localities. Cape Point receives about 8 I5 mm of rain per annum, and the animal bones have low 615N readings (3.1 to 5.4%). Churchhaven receives only 244

mm of rain per annum. Herbivore bone collagen PN readings range from 11.8 to 16.3% This large difference in the values for animals contrasts strongly with

FIG. 4. b15N values of animalsfrom the southern and eastern Cape and Botswana. Scientific names of animals ax hootebok (Lhamaliscus dorcas dorcas) G/OD, rhebok (Peka capreolus)G/DT, grysbok (Raphicerus mt4anatis)B, tortoise (Chersina angulata) B, blue duiker (Cephalophus momicola) B/OD, elephant (Laxodotua &iwm) MF/OD, buahbuck (Tragelaphus scriptus)B/OD, bushpig (Potamachoerusporcus) O/ OD, kudu (Tragelaphns sfrepsiceros)BIOD, buffalo (Syncerus c&r) G/OD, eland (Taurotmgus oryx) B/ DT, springbok (Anfid~rcasmarsupialis)MF/DT, gem&ok (Oryx gaze/la) G/DT, gmy duiker (Syivicapra grimmia) B/M, zcbm(Equs burchelli)G/OD, gin& (Gira& camelcymr&alis) B/DT, warthoe(Phacoclhomcs aerhiopinrr)G/DT, bluewM&eest(Cuwwchat~esratinus) G/OD. These m into drought-tokrant/ obligate drinkers (SMITHERS,1983) differfromthosein AMBROSEand DENIRO( 1986b) for busbbuck, &afk and warWg. There is clearly some latitude in these categories. (B = brow, G = m, MF = mixedfeeder, 0 = omnivore, DT = drought-tolerant, OD = obligate drinker.)

,

FIG. 5. 6”N values of animals from Kasungu National Park, Malawi. Scientific names of animals are: spotted hyaena (Crocuta crocukz), leopard (Pat&era purdus), lion (Pantheru Ieo), serval (F&r serral), Sena (Genefta genettu), puku (Kobus vardonii) G/OD, warthog (Phacochoerus aefhiopicus) G/DT, hippo (Hippopotamus amphibius) G/OD, buffalo (Syncerns q&r) G/OD, sable (Hippotrugus niger) G/OD. reedbuck (Reduncu a~~ndinum) G/OD, hartebeest (~iceluphus iichfenstejn~;) G/OD, zebra (Equus burcheili) G/OD, roan (~jp~tr~ ~jn~) G/OD. vervet monkey (Cercopifhc~~s p~~e~~h~~s) B/D-f? grey duiker (~~~vic~~r~ ~imrnju) B/DT, eland (~~~r~r~ oryx) B/DT, kudu (~ru~e~uphz~~.~zrep.~~cer~s) B/OD. black rhino (Diceros bicornis) B/OD, bushbuck (Tragelaphus scriptus) B/OD. (B = browser, G = grazer. DT = drought-tolerant, OD = obligate drinker.) The mean li”N value + one s.d. for the herbivores in this sample is 3.6 ir 1.2%, n = 44, while that for carnivores is 7.5 4 0.4%. n = 12. The average trophic level enrichment for this sample is therefore 3.9%0. Previous studies obtained figures of 3 to 3.5740(SCHOENINGER and DENIRO, 1984; MINAGAWAand WADA, 1984) or 5 to 6% (AMBROSEand DENIRO, 1986b).

li "N (%*I ‘5.

0

0 0

1;i

0

I

FIG. 6. Plot of relationship between rainfall at various collection sites and &“N values of animals. Data compiled from DEPARTMENT OFWATERAFFAIRS(f985). WEATHERBUREAU(1954,1965), and JACHWANN and BELL( 1985).

South

Africa nitrogen isotopic ecology

2713

Such a difference is not apparent in other published data sets: that presented by HEATON et al. (1986) is probably simply too small, while that of AMBROSEand DENIRO ( 1986b, Table 1) is obtained from specimens collected in a number of different localities, SO that differences that may exist are likely to have been obscured. The third prediction. that these differences will be more noticeable in samples from arid areas compared with those from well-watered regions, is not met by any of the available data sets. The highland savannahf montane forest collection areas (AMBROSEand DENirrogen and water conservation: Ihe Ambrose and NIRO, 1986b) have a mean annual rainfall of between DeNiro model 600 and 1000 mm. Etosha and Klaserie, where the On the basis of the model proposed by AMBROSE browsers and grazers analysed by HEATONef al. ( 1986) and DENIRO ( 1986b) it is possible to make a number were collected, receive 450 and 550 mm of rain per of predictions: annum. respectively. Kasungu National Park hasabout 780 mm of rain annually (JACHMANNand BELL, 1985). 1) In any given environment, obligate drinkers All these areas therefore fall well above the proposed should have lower 615N values than drought-tolerant 400 mm critical point. We have only one set of animals animals. which includes both obligate drinkers and drought-tol2) Grazers should have lower 6”N values than erant browsers and grazers from an area with less than browsers. 400 mm of rain. This is from the Addo National Park 3) These differences should be more noticeable in in the Eastern Cape (see Fig. 4). The sample is small: arid areas than in well-watered areas. 3 elephant (mixed feeders, obligate drinkers), 3 buffalo We have examined our data to see whether the pat- (grazers, obligate drinkers), 3 eland (mainly browsers, terning in our results can be satisfactorily explained by drought-tolerant) and 3 kudu (browsers, obligate these predictions. In doing this, data sets from different drinkers). The patterning proposed by Ambrose and localities were kept separate, since climatic factors in- DeNiro and clearly visible in the Kasungu sample is, fluence animal 615N values. if anything, reversed here: the browsing species have Most of the data sets presented here have insufficient slightly lower 615N values than the grazers. (Elephants numbers of obligate drinkers and drought-tolerant anare excluded from this discussion as they are mixed imals from the same colLection site for us to be able to feeders.) This reversal is also the case for the small compare then. The largest set, from Kasungu, contains sample of animals analysed by Ambrose and DeNiro mostly obligate drinkers. The eland, warthog, grey from the arid north-east shore of Lake Turkana. The duiker and possibly, to some extent, the vervet monsingle value for a browser (b”N = 7.7 for a dikdik) is keys are drought-tolerant. As the model predicts, lower than two values for grazers (8.9 for an oryx and most of these species do have higher 615N values than 9.7 for a warthog) (AMBROSEand DENIRO, 1986b, Tamany of the other herbivores (Fig. 5). Similarly, the ble 2). In addition, the drought-tolerant~animals gendata presented in Table 1 of AMBROSEand DENIRO erally have lower b”N values than the obligate drinkers. (1986b) shows a significant (Student’s t-test, p = 0.05) One would expect, according to the model, that the difference in b15N between obligate drinkers and “browser/grazer, obligate drinker/drought-tolerant’* drought-tolerant species (&,,iglte drinkcn= 6.0 + 3.3%, patterning seen in better watered areas would be inn=90;Z d,,+,,_,dcnnt = 7.8 i 2.0% n = 57). However, tensified in arid regions. Since this is clearly not the elephant and hippopotamus, both obligate drinkers case, some other mechanism(s) must come into play. with high b15Nvalues, are excluded from this synthesis. (We have assumed that the summarised data published Nitrogen in the digestive tract in this study are normally distributed.) The second prediction of the model, that grazers One aspect of nitrogen metabolism not considered should have lower b15N values than browsers, is also fully in previous stable isotope studies is that of mimet in the Kasungu data (.&_ = 3.0 + 0.9460,n = 24; crobial activity in the digestive tract. This occurs par&.,,,- = 4.3 + I. I %o,n = 20). These distributions are ticularly in the rumen of ruminants, but also in the significantly different (Mann-Whitney U-test). Some enlarged hindgut of herbivores with hindgut fermenof the variability is due to the fact that the droughttation (primates, elephants, hyraxes, pigs, rhinoceroses tolerant animals in this sample are browsers; however, equids), and in non-ruminant forestomach fermenters if one compares grazers and browsers within the ob(hippopotamus) (LANGER, 1984). ligate drinker category alone, the difference is still sigMicrobial activity in the rumen is often thought of nificant (6 = 3.0 * l.OL, n = 22; &_._ = 4.0 Primarily in relation to its role in breaking down long* 1.3%, n = 12). chain structural carbohydrates such as cellulose. It also, the broad similarity of plant b15N values from the two areas: measurements from Cape Point range from 1.3 to 2.6460,and from Churchhaven -3.5 to 1.2% Clearly, large differences in animal b15N values from one area to another are not mirrored in the plants; this supports the suggestion made previously (!WHOENINGERand DENIRO, 1984; HEATON et al.. 1986; AMBROSEand DBNIRo, 1986b), that high 615N values in terrestrial animals are the result of metabolic processes within the animals themselves.

2714

J. C. Scaly 6~u/

however, plays an important part in nitrogen metab olism. Most dietary protein is digested by these microorganisms and the nitrogen converted to ammonia, which is used by the bacteria to synthesise bacterial protein, either directly or via urea. The urea is produced in the liver and then returned to the rumen by diffusion through the rumen wall (SIMMONET et al.. 1957) and via inclusion in the parotid saliva (SOMERS. 1961).The rapidly reproducing bacteria eventually pass out of the rumen into the abomasum where they are digested by proteases and the nitrogen finally becomes available for incorporation into the proteins of the host animal (KINGDON, 1982). This process has several advantages for the animal: non-protein nitrogen in the feed can be used to synthesise proteins, and the amino acid balance of poor-quality protein feed can be improved. It effectively adds one or more steps or trophic levels to the food-chain through which the nitrogen passes before being absorbed by the herbivore. It is well known that urea excretion in a range of species (including camels, cows, humans and dogs) is very much reduced on low-protein diets (SCHMIDTNIELSEN etal.,1957; LEVINSKYand BERLINER,1959: LIVINGSTONet al., 1962). In ruminants, this is the result of nitrogen conservation as urea diffuses from the bloodstream back into the rumen, as described above, to provide raw material for another generation of protein-synthesising microbes. An analogous process has been observed in non-ruminant animals such as hyraxes (HUME et al.. 1980) and wallabies (KENNEDY and HUME, 1978). A number of studies have demonstrated increases in the proportion of recycled nitrogen in response to lowering of the protein content of the diet (NOLAN and STACHIW, 1979; KENNEDY and HUME, 1978); although, if protein intake is too low, it may be insufficient to maintain an adequate population of micro&s (‘T MANNETJE, 1984). In arid environments, the quality and protein content of the feed available to herbivores is generally inferior to that from better-watered areas (LENG, 1984; ‘T MANNETJE, 1984). Animals in areas receiving less than 400 mm of rain per annum may consume rather low-protein diets and hence be more dependent on recycling their urea to conserve nitrogen. If this is the case, and grazers habitually consume diets lower in protein than browsers, then grazers might be expected to recycle their urea to a greater extent than browsers. If each cycle increases the 615N of the protein synthesised by the symbiotic microorganisms, then grazers from arid areas should have higher 61SN values than browsers. This process may explain the patterning in the Addo and Lake Turkana samples. Testing of this hypothesis is necessary. Studies of wild animal bones should be augmented by 61SNmeasurements of their food plants, and of the soil nitrogen. A thorough understanding of the effects of metabolic processes on animal b”N will probably only be achieved by means of controlled feeding experiments on laboratory animals. Analyses of feed, salivary ni-

trogen, gut contents and excreted nitrogen as well as of the animal tissues themselves are required. The animals should be selected to cover a range of feeding preferences (grazers, browsers) and digestive physiologies (ruminants. non-ruminants) and maintained on high and low-protein diets under varying degrees of water stress. The pathways involved in nitrogen cycling in animals are clearly enormously complex. We suggest that. in addition to the renal processes emphasised previously, the complicated mechanisms of protein digestion and synthesis in the digestive tract should be considered in attempts to explain high II’~N values for terrestrial animals. Hl4mun.s

Figure 7 presents some results of nitrogen Isotope analyses of prehistoric human skeletons from the southwestern Cape. Carbon isotope measurements have been included for this set of samples, since they help in interpreting the 6”N values. An extensive carbon isotope survey of the foods available to these people has been presented elsewhere (SEALY,1986; SEALYand VAN DER MERWE, 1986). The nitrogen isotope data on many of these same samples is contained in this paper (Tables I. 2 and 4, Fig. 3). Most of the analyses in Tables 1 and 2 are on the meat that would actually have been eaten by prehistoric people. Figure 3 contains analyses of bone collagen. Table 4 shows that there is no consistent difference in 61SNbetween meat and bone collagen from the same animal. The 613Crest&s showed that terrestrial foods in this region are entirely C, based, and thus clearly distinguishable from marine foods. Nitrogen isotope analyses of marine and terrestrial foods. however, show almost complete overiap. We are therefore confident that the 6°C measurements on the skeletons provide a useful indicator of the proportions of marine and terrestrial foods eaten, whereas the &15Nmeasurements do not. However, this is not ag parent from the data presented in Fig. 7. There is a correlation between b13C and d”N readings on these skeletons. Elevated 6°C readings (-I I to -12%) reflect strongly marine-based diets, and low values (-17 to - 18%) strongly terrestrially-based ones. We suggest that. in this area, low 615N values result from a large proportion of low trophic level foods in the diet. Terrestrial diets based principally on plant foods, and marine diets based principally on shellfish should therefore both result in lower 615N values than diets heavily reliant on the meat of terrestrial or marine vertebrate animals. The archaeological literature can provide some indication of the likely composition of prehistoric human diets in this area, through reconstructions using excavated foodwaste (PARKINGTON, 1972, 1976: BUCHANAN. 1985). Such reconstructions are the topic of ongoing debate. and the aim of the isotopic studies is, in

South Africa nitrogen isotopic ecology

2715

S15N ( %o1

FIG. 7. d”C and dt5N values of prehistoric human skeletons from the southwestern Cape. Solid symbols: skeletons from the Cedarbeq area. Open symbols: Coastal skeletons found between the Cape Peninsula and Elands Bay. Of the 88 skeletons we have analysed Born this area, 56 are directly dated by radiocarbon measurements of the bone. Individuals which pm-date 4000 years are not included hem. We have, however, included analyses of 27 skeletons for which we are awaiting dates. These ate all from open (as opposed to cave) sites. Only 4 of 48 skeletons from open sites dated thus far ate older than 4000 B.P. Hence, we expect the great majority of the undated skeletons to date from the Late Holocene. Climatic fluctuations during the Holocene are unlikely to influence the interpretation of these results. The fitted tqpession equation is: btJN = 22.5 + 0.57 IS’%,with a cotrelation coefficient of 0.44. A hypothesis test of no cotselation between the two variableswas carriedout and the hypothesis rejectedat the 1%level.The C/N ratios of all archaeclogical bone collagen specimens in this study lie within the range of values for undegradcd collagen (HASAN and HARE, 1978; DENIRO, 1985).

part, to help answer some of these questions. It is, however, clear that terrestrial hunter-gatherer diets included large amounts of plant foods, with meat providing a supplement rather than a regular staple. After 2000 B.P. when pastoralism first appeared in the area, meat and/or milk of domesticated animals may have increased the terrestrial animal food component of peoples’ diets. Marine diets, on the other hand, were animal-food based. Shellfish were important, particularly in the period immediately preceding the arrival

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of pastoralism, but mammals (seals and probably whales) and fish-eating birds were regular dietary items. Thus the archaeological evidence suggests that terrestrial diets are predominantly plant-food orientated, and marine diets animal-based. The correlation between low b13Cand b”N for terrestrial diets may therefore result from a high plant food intake. In the case of marine diets, we suggest that the correlation between high 8°C and high 8”N values is attributable to a greater intake of animal foods. The relative amounts of protein in plant and animal foods are relevant to this suggestion. Plant foods are generally thought to contain little nitrogen. Nutritional data for 13 species of edible plants from this area are available (ARCHER, 1982). These include a number of varieties that we know to have been important items of diet in prehistory. The protein contents vary from 3.1 to 15.3%. Equivalent values for shellfish (mussels) are 7.8 to 18.7% (SIDWELL, 1981). An interesting corollary of this interpretation is that certain kinds of (high trophic level) terrestrial diets may raise the d15Nof some human groups above the regression shown in Fig. 7. For example, the brsN values of individuals eating ternstrial diets may be raised by terrestrial animal products, rather than marine foods (especially in arid areas). Compared with br5N values of 17.3 and 13.8L for springbok meat from Churchhaven

2716

J. C. Sealv et al.

(Table 4). large intakes of low trophic level marine shellfish with 6”N values of only 7-8460 (Table 1) will ir,n’er the lsN/14N ratio of consumer collagen. Thus, in certain situations, the marine/terrestrial patterning in nitrogen isotopes proposed previously (SCHOENINGER and DENIRO, 1984) may be inverted. This could account for some of the more scattered values in Fig. 7. There are no isotopic grounds for separating the

later skeletons into pastorafist and non-pastomlist groups(cJ: AMBROSE and DENIRO, 1986a). it is possible that all the individuals here are representative of one group or the other, or perhaps the boundaries between the two groups were sufficiently flexible to make it difficult to separate them (ELPHICK. 1977: SCHRIRE. 1980). Two conclusions emerge: firstly. extensive isotopic

monitoring of the foods available to any prehistoric population is a prerequisite for palaeodietary studies. Secondly, these data require sensitive interpretation within the framework of the local archaeology. Unless firmly placed in such a context, isotopic studies of palaeodiet can, at best, provide limited information. At worst, they may actually be misleading. SUMMARY AND CONCLUSIONS We have presented data on nitrogen isotope ratios of a wide range of marine and terrestrial organisms from southern Africa. The patterning of the results for marine organisms is broadly consistent with that reported previously. Our sample included a number of low trophic level organisms, such as shellfish, which have not been well represent& in earlier studies. These have Iow 615N values, and were often extremely important items of diet for prehistoric coastal populations. Thus shellfish-based diets have very different 615Nvalues from those orientated around marine mammals. This should be taken into account in reconstructions of ancient diets. tsN/i4N of terrestrial animals varies widely with rainfall: values above 10% for herbivores occur in areas receiving less than 400 mm of rain per annum. This is partly due to the regulation of urea excretion in response to water stress: increased excretion of isotopitally light urea allows animals to reduce the volume of urinary output. The body ofthe animal is therefore enriched in the heavier isotope. This explanation sometimes, but not always. accounts for observed variations in the 615N values of drought-tolerant animals as compared with obligate drinkers, and grazers compared with browsers. These corollaries of the model are not supported by the results of anaIyses of animals from arid areas. In such repions, animals are likely to consume low-protein diets. The additional protein produced by symbiotic bacteria in the animals’ digestive tracts may then assume greater significance. Nitrogen incorporated into the animal via this pathway has undergone additional trophic level f~ctionat~on compared with that absorbed directly

from the feed, and thus has a higher 615Nvalue. Morcover. nitrogen circutating in the bloodstream tn the form of urea may be re-absorbed into the digest&c tract to re-enter the cycle. In the arid south-western Cape. nitrogen isotopes do not differentiate marine from terrestrial foods. However. the remains of prehistoric people who ate predominantly terrestrial diets (as revealed by their carbon isotope ratios) have lower 615N values than those with largely marine diets. This may be due to atrophic level effect, since terrestrial diets probably included a large proportion of plant foods. whereas marine diets centred around animal foods. Isotopic surveys of the environment are clearly essential before dietary studies on human populations are attempted. valuable discussions about nitrogen cycling in plants and animals we thank Professors 0. Lewis (Botany) and G. N. Louw (Zoology) ofthe University ofCape Town, and Dr. W. Stock ofthe University of Natal. The animal samples were collected over a number of yean for different studies. Many individuals cont~but~ to the c&&ion. too many to name: we thank them all. We are grateful to Margaret and Graham Avery of the South African Museum and Alan Morris of the University of Cape Town Medical School for help in obtaining human bone samples. Mary-Lou Thompson kindly advised us on statistical tests, and Andrew Sillen, Stanley Ambrose and Stephen Macko made valuable comments on the manuscript. The research was supported by the Foundation for Research Development (C.S.I.R.. South Africa). the Harry Oppenheimer Institute for African Studies and the University of Cape Town. Acknowledgemenrs-For

Editorial

handling:

H. P. Schwartz REFERENCES

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