Paleoecological Reconstruction of a Lower Pleistocene Large Mammal Community Using Biogeochemical (␦13C, ␦15N, ␦18O, Sr: Zn) and Ecomorphological Approaches

Home , Eucladoceros, Hippopotamus antiquus, Megantereon, Soergelia, Ursus etruscus

Paleobiology, 29(2), 2003, pp. 205–229

Paleoecological reconstruction of a lower Pleistocene large mammal community using biogeochemical (␦13C, ␦15N, ␦18O, Sr: Zn) and ecomorphological approaches

Paul Palmqvist, Darren R. Gro¨cke, Alfonso Arribas, and Richard A. Farin˜a

Abstract.—Ecomorphological and biogeochemical (trace element, and carbon, nitrogen, and oxygen isotope ratios) analyses have been used for determining the dietary niches and habitat preferences of large mammals from lower Pleistocene deposits at Venta Micena (Guadix-Baza Basin, Spain). The combination of these two approaches takes advantage of the strengths and overcome the weak- 13 ness of both approaches. The range of ␦ Ccollagen values for ungulate species indicates that C3 plants 13 were dominant in the diet of these mammals. ␦ Ccollagen values vary among ungulates: perissodactyls have the lowest values and bovids the highest ones, with cervids showing intermediate values. The hypsodonty index measured in lower molar teeth and the relative length of the lower premolar tooth row indicate that the horse, Equus altidens, was a grazing species, whereas the rhino, Ste- 13 phanorhinus etruscus, was a mixed feeder in open habitats. The similar ␦ Ccollagen values shown in both perissodactyls does not reflect differences in feeding behavior with other ungulates, but rather a lower isotope enrichment factor in these monogastric herbivores than in ruminants, owing to their lower metabolic efficiency. The cervids Eucladoceros giulii and Dama sp. show low hypsodonty values, indicating that they were mixed feeders or browsers from forested habitats, an ecomorphol- 15 ogically based conclusion corroborated in the former by its low ␦ Ncollagen content (canopy effect). Bovid species (Bovini aff. Leptobos, Soergelia minor,andHemitragus albus) presumably inhabited 15 open environments, according to their comparatively high hypsodonty and ␦ Ncollagen values. Car- nivore species (Homotherium latidens, Megantereon whitei, Pachycrocuta brevirostris, Canis falconeri,and 15 Canis etruscus) exhibit higher ␦ Ncollagen values than ungulates. These results record the isotopic enrichment expected with an increase in trophic level and are also supported by low bone Sr:Zn 15 ratios. The elevated ␦ Ncollagen value for a sample of Mammuthus meridionalis, which came from an 15 individual with unfused epiphyses, confirms that it was a suckling animal. The ␦ Ncollagen value of the scimitar-cat H. latidens is well above that obtained for the young individual of Mammuthus, which indicates that juvenile elephants were an important part of its diet. The hippo, Hippopotamus 15 antiquus, yielded unexpectedly high ␦ Ncollagen values, which suggest feeding on aquatic, non-N2- 18 fixing plants. The high ␦ Ohydroxyl values of bovids Hemitragus and Soergelia and of cervid Dama indicate that these ungulates obtained most of their water requirements from the vegetation. The 18 megaherbivores and Eucladoceros exhibit the lowest ␦ Ohydroxyl values, which suggest increased water dependence for them. Paleosynecological analysis was based on the relative abundance of species of large mammals from different ecological categories, determined by feeding behavior and locomotion types. The comparison of the frequencies of such categories in Venta Micena with those found in modern African communities indicates that the composition of the paleocommunity closely resembles those of savannas with tall grass and shrubs. The net above-ground primary productivity estimated for the on-crop biomass of the mammalian species preserved in the fossil assemblage also yields a figure congruent with that expected for an open environment.

Paul Palmqvist. Departamento de Geologıá y Ecologıá (A´ rea de Paleontologıá), Facultad de Ciencias, Cam- pus Universitario de Teatinos, 29071 Ma´laga, Spain. E-mail: [email protected] Darren R. Gro¨cke. Department of Geology, Royal Holloway, University of London. Egham Hill, Egham, Surrey TW20 0EX, United Kingdom. E-mail: [email protected] Alfonso Arribas. Museo Geominero, Instituto Geolo´gico y Minero de Espanã (IGME), Rıós Rosas, 23, 28003 Madrid, Spain. E-mail: [email protected] Richard A. Farinã. Departamento de Paleontologıá, Facultad de Ciencias, Universidad de la Repu´blica, Igua´, 4225, 11400 Montevideo, Uruguay. E-mail: fariϳ[email protected]

Accepted: 1 November 2002

Introduction Pleistocene, with an estimated age of 1.3 Ϯ 0.1 Venta Micena (37Њ44Ј15ЉN, 2Њ24Ј9ЉW, eleva- Ma (Arribas and Palmqvist 1999). The fossils tion 974.5 m) lies near the village of Orce, in were preserved in 98–99% pure micritic lime- the eastern sector of the Guadix-Baza Basin stone, precipitated on a caliche paleosol that (Betic Chains, southeastern Spain; Fig. 1). This surrounded a shallow Pleistocene lake with site is dated by biostratigraphy to the early swampy marginal zones (Arribas and Palm-

FIGURE 1. Geological map of the Betic Chains, showing the situation of the Guadix-Baza intramontane basin and the stratigraphic profile of the early Pleistocene locality at Venta Micena. This sedimentary basin was endorheic (i.e., characterized by interior drainage) until late Pleistocene times, thus facilitating an exceptional record of Plio- Quaternary taphocenoses of large mammals preserved in swampy and lacustrine sediments. The 80–120-cm-thick Venta Micena stratum (VM-2) is one of the various fossiliferous units in the sedimentary sequence of Orce, whose surface stands out topographically in the ravines of the region and can be followed along ϳ2.5 km. This stratum has the following vertical structure from bottom to top: (1) A basal unit that is one-third to one-half the total thick- ness, formed by homogeneous micrite with some carbonate nodules and small mud banks. The sediment preserves abundant shells of freshwater mollusks and is sterile in vertebrate fossils, thus attesting to a first generalized lacustrine stage in the region, in which the micrite was precipitated in water of variable depth. The absence of both pyrite and carbonate facies rich in organic matter is evidence that the lake was not eutrophic. (2) A 4–15-mm-thick calcrete paleosol (hardpan) developed on the surface of the micrite sediments. The calcrete forms an irregular surface, subparallel to the bedding plane, and is thicker at topographic highs. It defines a stratigraphic unconformity indicating a major drop of the Pleistocene lake level, and thus the emergence of an extensive plain around the lake. (3) An upper unit of micrite deposited in a subsequent rise of the lake level, which continues up to the top of the stratum, showing rootmarks, mudcracks, and a high density of fossil bones of large mammals resting on the paleosol. qvist 1998). The macrovertebrate assemblage Arribas and Palmqvist 1998). The selection by comprises ϳ5800 identifiable skeletal remains predators of specific ungulates was basically a of 225 individuals, which belong to 20 species function of differences in the body mass of ju- of large mammals (Table 1). venile and adult prey individuals, as well as Taphonomic research on the composition of in the sex of prey (Palmqvist et al. 1996). Major the Venta Micena assemblage has shown that taphonomic biases in the preservation of the the skeletal remains were scavenged by the gi- bone assemblage are related to the selective ant, short-faced hyena Pachycrocuta brevirostris transport by hyenas of ungulate carcasses and from carcasses of ungulates preyed upon by body parts to their maternity dens, and to the flesh-eating carnivores (Palmqvist et al. 1996; preferential consumption of low-density, mar- ECOLOGY OF PLEISTOCENE MAMMALS 207

TABLE 1. Herbivores larger than 10 kg and carnivores larger than 5 kg found in the fauna of Venta Micena, their trophic habits, their number of identifiable specimens (NISP), their minimal number of individuals (MNI)(data from Palmqvist and Arribas 2001), their estimated mass (data from Palmqvist et al. 1996), their calculated on-crop biomass, and their mass-specific basal metabolic rate. Abbreviations: Br ϭ browser, Ͼ75% leaves. Mf ϭ mixed feeder, 25–75% grass. Gr ϭ grazer, Ͼ75% grass. F ϭ flesh eater, Ͼ70% vertebrate flesh in diet. Mi ϭ meat and insect eater, 20–70% flesh. Mb ϭ meat and bone eaters. O ϭ omnivore, Ͻ20% flesh.

Basal Body mass On-crop metabolic Trophic NISP MNI (adults, biomass rate Species habits (teeth/bones) (juv./adults) in kg) (kg kmϪ2) (J kgϪ1 sϪ1) Mammuthus meridionalis Mf 48 (16/32) 5 (4/1) 6000 840.5 0.47 Hippopotamus antiquus Gr 58 (19/39) 5 (3/2) 3000 706.8 0.55 Bovini aff. Leptobos Gr 775 (382/393) 27 (16/11) 450 439.8 0.89 Soergelia minor Mf 334 (215/129) 13 (3/10) 225 369.9 1.06 Praeovibos sp. Gr 6 (3/3) 1 (0/1) 320 403.9 0.97 Hemitragus albus Gr 305 (209/96) 14 (2/12) 75 281.0 1.39 Caprini gen. et sp. indet. Mf 1 (0/1) 1 (0/1) 10 169.8 2.31 Eucladoceros giulii Br 962 (557/405) 36 (15/21) 385 423.0 0.93 Dama sp. Mf 417 (231/186) 20 (3/17) 95 298.1 1.31 Stephanorhinus etruscus Br 90 (55/35) 6 (2/4) 1500 594.3 0.66 Equus altidens Gr 2562 (1183/1379) 70 (32/38) 350 413.1 0.95 Vulpes praeglacialis Mi 24 (19/5) 1 (0/1) 5 3.6 2.93 Canis falconeri F 65 (40/25) 3 (0/3) 30 6.9 1.80 Canis etruscus Co 33 (20/13) 4 (0/4) 10 4.7 2.43 Lynx aff. issiodorensis F 6 (2/4) 1 (0/1) 10 4.7 2.43 Megantereon whitei F 16 (7/9) 3 (0/3) 100 10.7 1.30 Homotherium latidens F 7 (6/1) 2 (0/2) 200 13.8 1.08 Pachycrocuta brevirostris Mb 62 (34/28) 10 (4/6) 70 9.4 1.44 cf. Meles sp. O 1 (1/0) 1 (0/1) 10 4.7 2.43 Ursus etruscus O 27 (15/12) 3 (1/2) 375 17.2 0.91 row-rich skeletal parts (Palmqvist and Arribas vore and ungulate species (e.g., Damuth and 2001). MacFadden 1990; Anyonge 1993). The main objective of this study was to de- Feeding preferences of extinct ungulates termine the autecology of those species of can be determined from their craniodental large mammals represented at Venta Micena morphology, because several features of the using biogeochemical and ecomorphological skull and dentition are indicative of diet (see techniques, in order to (1) interpret niche and review in Janis 1995; see also Spencer 1995; resource partitioning by the species from each Mendoza et al. 2002). In herbivores, the hyp- trophic level; (2) infer ecological relationships sodonty index (HI) or relative tooth crown such as those between predators and their height (defined here as unworn molar tooth prey; and (3) study the synecological proper- crown height divided by molar width [Janis ties of the paleocommunity. The use of this 1988]) is widely accepted as a useful indicator combined approach allows the researcher to of diet (Fortelius 1985; Williams and Kay take advantage of the strengths and overcome 2001): grazing ungulates from open habitats the weakness of both techniques. that feed upon abrasive grasses with high sil- icophytolith contents generally show higher Ecomorphological Analyses hypsodonty values than browsers from for- Autecological inferences are presented for ested environments that consume succulent large mammals from Venta Micena, following leaves (in this article grazers are defined as an ecomorphological approach. Size estimates species in which grass represents Ͼ75% of for these species (Table 1) range between 5 kg diet, browsers include ungulates consuming and 6000 kg and were obtained by Palmqvist Ͼ75% of leaves, and those species taking be- et al. (1996) using ‘‘taxon-free’’ regression tween 25% and 75% of grass are considered as equations for body mass on craniodental and mixed feeders [Mendoza et al. 2002]). Muzzle postcranial measurements in modern carni- shape is also a good indicator of the specific 208 PAUL PALMQVIST ET AL.

FIGURE 2. Mean values of relative length of the lower premolar tooth row [(length P2–P4/length M1–M3) ϫ 100] and hypsodonty index [(unworn M3 crown height/average width) ϫ 100] in modern perissodactyls (data from Mendoza et al. 2002) and extinct species (horse E. altidens and rhino S. etruscus) from Venta Micena. adaptations related to the ‘‘cropping mecha- dental morphology are related to phylogenet- nism,’’ which includes the shape of the pre- ic constraints. For example, horses have rela- maxilla and the corresponding mandibular tively more narrow muzzles than grazing ru- symphyseal region, as well as the relative pro- minants of similar body size (Janis and Ehr- portions of the incisor teeth (Gordon and Il- hardt 1988; MacFadden and Shockey 1997) lius 1988; Solounias and Moelleken 1993; and not all exclusively grass-eaters are similar Pe´rez-Barberı´a and Gordon 2001): browsers in their degree of hypsodonty (Williams and usually show narrow muzzles (i.e., short pre- Kay 2001). Furthermore, different ungulate maxillary width), consisting of a rounded in- groups have adopted different solutions when cisor arcade with the ﬁrst incisor generally faced with the same ecological specializations larger than the third, whereas grazers have (Mendoza et al. 2002). Grazers, for example, broad muzzles with transversely straight in- require a comparatively greater grinding area cisor arcades, showing equal or subequal- of cheek teeth than browsers and frugivores sized teeth. (Janis 1995). Perissodactyls have faced this Although the hypsodonty index is probably problem by enlarging the size of the premolar the best single variable for predicting diet in tooth row, which in low-crowned, browsing both extant and ancient ungulates, in some and mixed feeding rhinos is comparatively cases molar crown height does not seem to be shorter than the molar tooth row (Fig. 2). In a good indicator of feeding habits (see review these species, the mesiodistal length of the in Mendoza et al. 2002). For example, most premolar row represents ϳ75% of the corre- grazing and mixed feeding ungulates have sponding measurement for the molar row, but hypsodont teeth, but the hippo (Hippopotamus grazing perissodactyls have lower premolar amphibius) and the rock hyrax (Procavia capen- and molar cheek teeth of nearly the same sis) have brachyodont (i.e., short-crowned) length, as can be seen in the white rhino (Cer- teeth (HI Ͻ 1.4 and Ͻ 1.7, respectively). Both atotherium simum), or even have a premolar species have relatively low metabolic rates, row that is longer than the molar row, as in consuming less food per day than would be horses (Fig. 2). However, ruminants and ca- expected for animals of their body size (No- melids show an opposite trend in the size of vak 1999), which means that the total amount the premolar tooth row; in these groups, graz- of wear on the teeth would correspondingly ers have comparatively shorter premolar tooth be less. rows than browsers (premolars ϳ45% of the Some second-order differences in cranio- molar tooth row, vs. ϳ70%; Figs. 3, 4). This ECOLOGY OF PLEISTOCENE MAMMALS 209

FIGURE 3. Mean values of relative length of the lower premolar tooth row [(length P2–P4/length M1–M3) ϫ 100] and hypsodonty index [(unworn M3 crown height/average width) ϫ 100] in modern bovids (data from Mendoza et al. 2002) and extinct species (Bovini aff. Leptobos, S. minor,andH. albus) from Venta Micena. The position in this diagram of nine extant species covering the whole range of values for hypsodonty and premolar tooth row length is shown, in order to facilitate the visual interpretation of the diagram. The feeding category ‘‘high level browsers’’ includes those browsing bovids that feed from trees and bushes at high levels above the ground (e.g., the long- necked gazelles of the genus Litocranius). difference is probably due to differences in the al. 1996). These variables provide discrimina- way food is orally processed in foregut and tion between hypercarnivores, bone crackers, hindgut fermenters (Mendoza et al. 2002). and omnivores. Relevant variables in the post- In carnivores, features of the dentition re- cranial skeleton of carnivores include the bra- lated to diet include the morphology of the chial and crural indexes (i.e., radius length di- 1 upper canine (C ), lower carnassial (M1), and vided by humerus length and tibia length di- fourth premolar (P4). Particularly indicative of vided by femur length, respectively), the un- feeding habits are the relative length of the tri- gual phalanx shape and manus proportions, gonid blade and the morphology of cusps in the ratio of phalanx length to metacarpal 1 the talonid basin of M1, the shape of C and P4 length, the biceps brachii leverage index, and (i.e., tooth length divided by tooth breadth), cross-sectional geometric properties of long the total grinding area in the dentition, and bones such as the midshaft femoral cross-sec- the smaller masseter and temporalis moment tional shape (Gonyea 1976; Van Valkenburgh arms (Van Valkenburgh 1988, 1989; Biknevi- 1985, 1987; Anyonge 1996; Lewis 1997). These cius and Van Valkenburgh 1996; Biknevicius et variables allow the estimation of different as- 210 PAUL PALMQVIST ET AL.

FIGURE 4. Mean values of relative length of the lower premolar tooth row [(length P2–P4/length M1–M3) ϫ 100] and hypsodonty index [(unworn M3 crown height/average width) ϫ 100] in modern cervids (data from Mendoza et al. 2002) and extinct cerrid species (E. giulii and Dama sp.) from Venta Micena. The position in this diagram of five extant species is shown for illustrative purposes. The feeding category ‘‘high level browsers’’ includes the moose, Alces alces, which is the only cervid that is able to feed at a high level above the ground. pects related to habitat preferences and hunt- one hyenid (P.brevirostris); three canids (Canis ing techniques: for example, the brachial and [Xenocyon] falconeri, Canis etruscus,andVulpes crural indexes (Fig. 5) are useful in felids to praeglacialis); one mustelid (cf. Meles sp.); and discriminate between predators that ambush one ursid (Ursus etruscus). They can be clas- and those that pursue their prey. sified in one of the following sub-categories: The species of large mammals preserved at Venta Micena can be classified in the follow- 1. Hypercarnivores (i.e., predators whose diet ing trophic groups, according to their cran- consists of Ͼ70% flesh): saber-tooths, H. la- iodental and postcranial morphology: tidens and M. whitei; the lynx, L. issiodoren- Carnivores. The order Carnivora is repre- sis; and wild dog, C. falconeri. sented in the assemblage by nine species, in- 2. Carnivores (i.e., those species in which cluding three felids (Homotherium latidens, Me- flesh constitutes between 20% and 70% of gantereon whitei,andLynx aff. issiodorensis); the diet, with fruits and invertebrates mak- ECOLOGY OF PLEISTOCENE MAMMALS 211

FIGURE 5. Mean values of brachial and crural indexes in several species of extant felids (data from Gonyea 1976 and Anyonge 1996) and in the saber-tooth species preserved in Venta Micena. The value for H. latidens is the mean obtained by averaging unpublished length measurements of major limb bones from the early Pleistocene site at Incarcal (kindly provided by A. Galobart) and those published for the North American species H. serum (Rawn- Schatzinger 1992). Given the absence of at least one complete radius and tibia of M. whitei, the means of the values estimated in M. cultridens (Lewis 1997) and in the closely related genus Smilodon (Gonyea 1976) were used. The brachial index is positively correlated in modern felids with their cursorial abilities, and the values obtained in both indexes are useful to describe the transition from closed environments, with dense tree cover, to open habitats.

ing up the balance): small-to-medium- Palmqvist 1996). The low value estimated for sized canids, C. etruscus and V.praeglacialis. the brachial index (ϳ80%; Fig. 5) and the short 3. Bone crackers (i.e., species that fracture metapodials indicate that it was an ambush bones for access to their marrow content): predator, hunting in closed, forested habitats. the hyena, P. brevirostris. The forelimbs are powerful, with large claws, 4. Omnivores (i.e., those species consuming and the upper canine teeth are extremely long, Ͻ20% of vertebrate flesh): the ursid, U. sharp, and laterally compressed (Arribas and etruscus, and the badger, cf. Meles sp. Palmqvist 1999). M. whitei was a dirk-toothed machairodont H. latidens was a scimitar-toothed cat similar with a strong body, similar in size to that of a in size to modern lions, Panthera leo (Anyonge jaguar, Panthera onca (Martıńez-Navarro and 1993). It had small claws and elongated fore- 212 PAUL PALMQVIST ET AL. limbs (brachial index of ϳ90%; Fig. 5), which gesting that this extinct species was also om- provided considerable leverage. These fea- nivorous. tures suggest increased cursoriality in an Herbivores. Ungulates are represented by open habitat (Martin et al. 2000), with less 11 taxa in Venta Micena, including one pro- prey-grappling capability than other saber- boscidean (Mammuthus meridionalis); one hip- tooths (Rawn-Schatzinger 1992). The upper popotamus (Hippopotamus antiquus); two pe- canines were shorter and broader than in Me- rissodactyls (the horse, Equus altidens,andthe gantereon, bearing coarse serrations in the rhino, Stephanorhinus etruscus); and seven ar- enamel margins. tiodactyls (five bovids, Bovini aff. Leptobos, The results obtained in a comparative eco- Soergelia minor, Hemitragus albus, Praeovibos sp., morphological analysis of modern and Pleis- and Caprini indet.; two cervids, Eucladoceros tocene canids (Palmqvist et al. 1999, 2002) in- giulii and Dama sp.). These taxa can be classi- dicate that C. falconeri was a hypercarnivore fied into feeding categories by using ecomor- with a body mass of ϳ30 kg. The second meta- phological variables such as the hypsodonty carpal shows a reduced articular facet to the index and the relative length of the lower pre- first metacarpal, which indicates that the latter molar tooth row (Figs. 2–4). bone was vestigial if not absent. Such condi- Concerning the perissodactyls, E. altidens tion is similar to that of the African painted was a grazer, showing high values of both the dog, Lycaon pictus, and indicates increased hypsodonty index (HI ϭ 6.1) and the relative cursoriality in open to intermediate forested lower premolar row length (ϳ110%), similar country. C. etruscus was similar in size (ϳ10 to those of living equids (Fig. 2). This species kg) and feeding habits to the modern coyote, had elongate, slender metapodials and pha- Canis latrans. In this species, the trigonid blade langes, very similar to those of modern Gre- represents Ͻ70% of the mesiodistal length of vy’s zebra, Equus grevyi, which indicates that the lower carnassial, which suggests that scav- it was adapted to open and dry habitats enging probably represented an important (Guerrero-Alba and Palmqvist 1997). S. etrus- fraction of its diet. cus was a browser or mixed feeder with L. issiodorensis had a body mass comparable brachyodont teeth (HI ϭ 1.8) and a short pre- to extant Lynx europaeus. Given the small size molar tooth row (ϳ82%), similar to those of of the prey hunted by modern lynxes, it is not modern rhinos in which grass represents likely that this extinct species was a predator Ͻ50% of the diet (Fig. 2). It was clearly not a of large mammals. grazer, because the white rhino, C. simum,the P. brevirostris was a hyena with a body and only living hypergrazing rhino, shows a hyp- skull 10–20% larger than that of modern spot- sodonty value (HI ϭ 3.9) 2.5 times greater than ted hyenas, Crocuta crocuta, well-adapted for both Stephanorhinus and modern mixed feed- destroying carcasses and consuming bone ing rhinos, and a longer premolar tooth row (Palmqvist et al. 1996; Arribas and Palmqvist (ϳ118%). The Etruscan rhino presumably in- 1998). This giant hyena shows a relative short- habited open to mid-covered habitats, as sug- ening of the distal limb segments (Turner and gested by its slender metapodials. Antoń 1996), which suggests that it was less Within the artiodactyls, the goat H. albus (HI cursorial than other hyenas, although such ϭ 4.4) and the bison Bovini aff. Leptobos (HI ϭ shortening provided greater power and more 3.9) were presumably grazers or mixed feed- stability to dismember and carry large pieces ers dwelling in unforested habitats, as de- of carcasses. Several features of the dentition duced from their comparatively high hypso- (e.g., the relative length of the trigonid blade donty values (Fig. 3), which are similar to in the lower carnassial) indicate that Pachycro- those of modern grazing (HI ϭ 3.8–6.1) and cuta fed more heavily on carrion than spotted mixed feeding ruminants (HI ϭ 2.5–5.3) from hyenas did. open habitats (range of values for extant bo- The overall craniodental morphology of the vids estimated from data in Mendoza et al. etruscan bear, U. etruscus, is similar to that of 2002). S. minor shows intermediate values in modern brown bears, Ursus arctos, thus sug- both the hypsodonty index (HI ϭ 2.9) and the ECOLOGY OF PLEISTOCENE MAMMALS 213 lower premolar row length, indicative of substances during physical and chemical pro- mixed feeding habits (Fig. 3). The dentition of cesses that labels the substances with distinct the giant deer, E. giulii, shows a very low value isotopic ratios. Natural fractionations are of hypsodonty (HI ϭ 1.6). A comparison with small, so isotopic ratios are reported as parts hypsodonty data in modern deer (Fig. 4) sug- per thousand (‰) deviation in isotope ratio gests that it was a mixed feeder from closed from a standard, using the ␦ notation, where habitats (HI ϭ 1.1–2.8) or more probably a ␦X ϭ [(Rsample/Rstandard) Ϫ 1] ϫ 1000, with X ϭ browser (HI ϭ 1.2–1.6 [values from Mendoza C, N, or O, and R ϭ 13C/12C, 15N/14N, or 18O/ 16 et al. 2002]). The fallow deer, Dama sp., was a O. Rsample and Rstandard are the high-mass to mixed feeder, judging from its moderately low-mass isotope ratios of the sample and the hypsodont teeth (HI ϭ 1.7) and diet of its clos- standard, respectively: commonly used stan- est living relative, Dama dama. Of relevance to dards for ␦13C, ␦15N, and ␦18O are Peedee bel-

H. antiquus, modern hippos are basically emnite (PDB), atmospheric N2, and standard fresh-grass grazers, although Bocherens et al. mean ocean water (SMOW), respectively. Pos- (1996) reported carbon isotope values unusual itive ␦ values indicate enrichment in the high- for a diet on terrestrial C4 grasses in Pleisto- mass isotope relative to the standard, whereas cene hippos from localities in North and East negative values indicate depletion. Africa, which suggests that they fed predom- Terrestrial plants can be divided into three inantly on aquatic vegetation. main groups on the basis of their photosyn- The proboscidean, M. meridionalis,wasa thetic pathway (Edwards and Walker 1983): browser or mixed feeder like modern African (1) C3 plants, which follow the Calvin-Benson elephants, Loxodonta africana, which consume cycle, fixing atmospheric CO2 directly through on average 20% grass and 80% leaves, al- the reductive pentose phosphate pathway; (2) though grass was probably a more significant C4 plants, which use the Hatch-Slack cycle (C4- component of diet in Mammuthus according to dicarboxylic acid pathway); and (3) CAM carbon isotopes of tooth enamel (Cerling et al. (crassulacean acid metabolism) plants. C3 1999). plants are all trees, temperate shrubs, and grasses of cool/moist climates and high alti- Biogeochemical Analyses: tudes. Most C4 plants are herbaceous, tropical, Stable-Isotope Ratios arid-adapted grasses and warm/dry herbs. Biogeochemical techniques have proved ex- Succulent or CAM plants use an intermediate tremely useful in determining the dietary C3/C4 photosynthetic pathway, which is mod- niche of fossil mammalian species, and in pro- ified in response to environmental changes. 12 viding detailed environmental reconstruc- All plants take up CO2 in preference to 13 tions (see reviews and references in Bocherens CO2, but there are important differences in et al. 1996; Gro¨cke 1997a; Koch 1998; and their isotopic composition related to their car-

MacFadden 2000). We analyzed carbon, nitro- boxylating enzymes. C3 plants use the ribu- gen, and oxygen isotope content of collagen lose 1,5-biphosphate carboxylase, which dis- 13 material and hydroxylapatite from bone and criminates effectively against CO2, produc- tooth enamel of large mammals preserved in ing a depletion of Ϫ19.5‰. Given that the 13 Venta Micena to determine dietary niches and mean ␦ C value of atmospheric CO2 is Ϫ6.5‰ 13 trophic relationships, following the method- (Koch 1998), C3 plants show an average ␦ C ology described by Gro¨cke (1997a). value of Ϫ26 Ϯ 2‰, with a range from Ϫ34‰ Stable isotopes are useful as paleobiological in dense forests to Ϫ21‰ in open areas ex- and paleoclimatological tracers because, as a posed to water stress. C4 plants use the phos- result of mass differences, different isotope ra- phoenolpyruvate carboxylase, which is less ef- 12 13 14 15 13 tios of an element (e.g., C vs. C, N vs. N, fective at discriminating against CO2,and 16O vs. 18O) have different thermodynamic produces a depletion of only Ϫ5.5‰. As a 13 and kinetic properties. For elements with an consequence, C4 plants have an average ␦ C atomic mass of Ͻ40, these differences can lead value of Ϫ12 Ϯ 1‰, with a more restricted to measurable isotopic partitioning between isotopic range from Ϫ15‰ to Ϫ7‰. CAM 214 PAUL PALMQVIST ET AL. plants are capable of fixing carbon with either ers in humid, closed-canopy conditions to as photosynthetic pathway and therefore display high as ϩ3‰ for hypergrazers. Intermediate 13 13 ␦ Cplant values covering the range for C3 and ␦ Chydroxyl values are observed for mixed C3/ 13 C4 plants (see reviews and references in Smith C4 feeders. A cut-off ␦ Chydroxyl value of Ϫ8‰ and Epstein 1971; Bocherens et al. 1996; has been proposed to identify pure C3 feeders. 13 Gro¨cke 1997a,b; 1998; Ehleringer et al. 1997; ␦ Chydroxyl values for a pure C4 diet are located Collatz et al. 1998; Zazzo et al. 2000; Freeman between Ϫ2‰ and ϩ3‰ (Lee-Thorp et al. and Colarusso 2001; and Franz-Odendaal et 1989; MacFadden and Cerling 1996; Cerling et al. 2002). al. 1997a,b, 1999; Cerling and Harris 1999). When a plant is consumed by a herbivore, The ␦15N composition of collagen in mam- the plant’s carbon is incorporated into the an- mals records their position within the ener- imal’s skeletal tissues with some additional getic pyramid, because each trophic level fractionation. The difference between the ␦13C above herbivore is indicated by an increase in 15 value of the animal’s diet and that subsequent- ␦ Ncollagen between ϩ1‰ and ϩ6‰ (average ly incorporated into collagen translates into ϳ3.4‰ [Robinson 2001]). For herbivores, the 13 15 an increase in ␦ Ccollagen per trophic level from primary factors that affect the ␦ N value ex- ϩ3‰ to ϩ5‰. This implies that a mammal pressed in collagen are (1) soil synthesis of ni- consuming C3 vegetation (i.e., fruits, leaves, trogen, (2) the diet of the animal (i.e., if it con- and roots of trees and bushes) will record an sumes N2-fixing or non-N2-fixing plants), and 13 average ␦ Ccollagen value of Ϫ22‰ (range: (3) nitrogen metabolism in that animal (Koch Ϫ30‰ to Ϫ17‰), whereas a herbivore feed- 1998). Herbivores from forests generally ex- 15 ing on C4 plants (i.e., tropical grass blades, hibit lower ␦ Ncollagen values than herbivores seeds and roots) will exhibit a value around from grassland environments as a conse- 13 Ϫ8‰ (range: Ϫ11‰ to Ϫ3‰). The ␦ Ccollagen quence of soil acidity in densely forested hab- enrichment is similar for carnivores: a preda- itats (Rodie`re et al. 1996; Gro¨cke et al. 1997). 15 tor consuming C3-browsing ungulates will re- Plants that fix nitrogen have ␦ N values that 13 cord an average ␦ Ccollagen value of Ϫ18‰, cluster close to the atmospheric N2 value of whereas a carnivore that consumes C4-grazers 0‰, whereas those that do not fix nitrogen ϩ will show a value close to Ϫ4‰ (DeNiro and and use other sources (e.g., soil NH4 and Ϫ 15 Epstein 1978; Van der Merwe 1982; Klepinger NO3 ) usually show a wider range of ␦ Nplant and Mintel 1986; Gro¨cke 1997a,b; Koch 1998). values (Robinson 2001). As a result, animals 15 Isotope variability among mammals is not consuming N2-fixing plants exhibit ␦ Ncollagen solely a result of diet, however: for example, values between 0‰ and ϩ4‰, whereas her- recycling of CO2 in closed forests (i.e., canopy bivores feeding on non-N2-fixing plants re- 13 15 effect) causes a shift to more negative ␦ Cplant cord ␦ Ncollagen values between ϩ2‰ and values and, thus, in the collagen and hy- ϩ8‰. The ␦15N value of plants near marine droxylapatite of those browsing herbivores and/or salt-affected areas is also enriched, re- consuming such plants. flecting the higher 15N content of soil nitrate The ␦13C value of herbivore hydroxylapatite and ammonium in saline environments (Sealy is also enriched with respect to that of the an- et al. 1987; Matheus 1995; Koch 1998). 13 imal’s diet. ␦ Chydroxyl ranges from ϩ9‰ to The effect of nitrogen metabolism in ani- ϩ14‰ for wild ungulates, but the precise en- mals is also very important. The higher 15 richment value probably varies among species ␦ Ncollagen values observed in animals inhab- because of differences in digestive physiology iting arid regions result from differences in ni- (Cerling and Sharp 1996; Koch 1998). For me- trogen recycling and/or urea loss associated dium- to large-bodied mammals, the enrich- with adaptations for drought tolerance (Am- ment is ϳϩ14‰ (Cerling and Harris 1999; brose and DeNiro 1986a,b; Gro¨cke 1997a; Feranec and MacFadden 2000; Zazzo et al. Gro¨cke et al. 1997; Koch 1998; Schwarcz et al. 2000). Therefore, a continuous range of 1999): in arid regions, the diets of herbivores 13 ␦ Chydroxyl values is observed for mammalian are low in protein content and the animals are herbivores, ranging from Ϫ16‰ for C3 brows- more dependent on recycling their urea to ECOLOGY OF PLEISTOCENE MAMMALS 215 conserve nitrogen; in such conditions, herbi- corder of diets in the geological record (see re- vores concentrate urine and excrete concen- views in Cerling and Harris 1999 and in Spon- trated urea depleted in 15N relative to diet, heimer and Lee-Thorp 1999a,b). Carbon and subsequently causing elevated ␦15N values. nitrogen isotope ratios in bone collagen are in- Similarly, the isotopic signature in cave bears dicative of overall diet during the last few has been related to the physiology of dorman- years of an animal’s life. The information ob- 15 cy: higher ␦ Ncollagen values are recorded in tained from enamel isotopes is more limited, those sites corresponding to colder periods, as it only records the dietary preference of the owing to the reuse of urea in synthesizing animal during the time the teeth were formed amino acids during prolonged periods of dor- (in large mammals, around 1.5 years from mancy (Nelson et al. 1998; Fernańdez-Mos- birth). Moreover, retrieval of environmental 15 quera et al. 2001). In general, ␦ Ncollagen values information from isotopic ratios in collagen, are higher in large monogastric herbivores bone carbonate, and enamel is further com- than in ruminants (Gro¨cke and Bocherens plicated by potential diagenetic overprinting. 1996). Elevated nitrogen isotope levels, how- Tooth enamel is much less porous than bone ever, may also indicate either advanced age or and dentine, and it has greater inorganic con- young suckling animals. Such an elevation, tent, density, and crystallinity. For these rea- caused by excretion of concentrated urea or by sons, enamel is less susceptible to diagenetic ingestion of nutrient-enriched milk, respec- change, reflecting more closely the original tively, can cause an apparent increase in that abundance of trace elements and stable iso- animal’s trophic level by one (Minagawa and topes. Similarly, cortical bone is less prone to Wada 1984; Nelson et al. 1998; Witt and Ay- diagenetic contamination than porous, can- liffe 2001). cellous bone tissue. Because the mineral in Oxygen isotope ratios reflect prevailing cli- bones and teeth, carbonate hydroxylapatite, matic conditions (e.g., paleotemperature), but survives much longer than protein, most iso- for a local fauna they also can be used to in- tope analyses have been performed in enamel terpret the dietary water source (Ayliffe et al. and bone hydroxylapatite (see review in 1992; Kohn et al. 1996; Sponheimer and Lee- Sponheimer et al. 1999). Thorp 2001; Harris and Cerling 2002). Several methods are available to identify al- 18 18 ␦ Ohydroxyl parallels the ␦ O of body water, teration of collagen, including analysis of C:N whose composition is related to three major ratios and amino acid composition (DeNiro oxygen sources: air oxygen, drinking water, and Epstein 1978; Gro¨cke 1997a; Richards et and food. Although the oxygen isotope com- al. 2000). The acceptable values for the C:N ra- position of air is the same worldwide and lo- tio are between 2.9 and 3.6. This C:N ratio cri- cal water compositions show limited variabil- terion allows for the identification and exclu- ity, diet and physiology differ among animals. sion of collagen that is heavily degraded and/ The ␦18O is more positive in plants than in or contaminated. There are no equivalent cri- their source water, which is derived from local teria for integrity of stable isotope measure- rain. Thus, among sympatric herbivorous ments of bioapatite in bone mineral and mammals a more positive result would indi- enamel, and appropriate monitors of its iso- cate that the species is obtaining most of its topic integrity are yet to be developed. water requirements from the vegetation that it eats rather than from drinking. This depends Biogeochemical Analyses: on the digestive physiology of ungulates and Trace Element Ratios on the water content of their food, which rep- In both fresh and fossil bones the hydroxyl- resents only 5% of dry grass but may reach up apatite is far from being chemically pure; rath- to 70% of succulent forage. er it is substituted with small amounts of car- Use of stable isotopes to reconstruct animal bonate, citrate, and a host of minor and trace diets was first demonstrated with collagen elements. Interest in them stems from the fact (DeNiro and Epstein 1978). More recently, it that their concentration in bone reflects die- was shown that tooth enamel is a faithful re- tary intakes. Among the different elements, 216 PAUL PALMQVIST ET AL. 1.65) 1.23) 1.71) Ϯ Ϯ Ϯ — — — — — — — — — 55.6 55.6 27.8 70.1 64.4 61.2 66.6 62.9 65.3 62.8 63.6 64.1 62.8 64.2 65.6 63.3 53.9 58.0 55.5 56.4 96.9 89.9 91.2 93.2 48.95 Sr:Zn 63.86 ( 63.98 ( 55.95 ( 0.13) 0.10) 0.10) collagen Ϯ Ϯ Ϯ — — — — — — — — — — — — — — — 3.1 3.3 3.3 3.4 3.3 3.4 3.5 3.5 3.4 3.1 3.3 3.2 3.2 3.6 3.4 3.4 3.5 3.3 3.45 C:N 3.28 ( 3.40 ( 3.40 ( one standard deviation for those in Ϯ 0.22) 0.31) 0.15) Ϯ Ϯ Ϯ collagen 4.7 2.9 3.8 7.7 7.4 3.8 3.6 3.5 4.0 3.2 3.4 3.8 4.0 3.9 3.7 1.6 1.3 1.8 7.55 — — — — — — — — — — — — — — — N ϩ ϩ ϩ ϩ ϩ ϩ ϩ ϩ ϩ ϩ ϩ ϩ ϩ ϩ ϩ ϩ ϩ ϩ ϩ 15 ␦ 3.73 ( 3.47 ( 3.87 ( ϩ ϩ ϩ 0.32) 0.25) 0.40) Ϯ Ϯ Ϯ collagen — — — — — — — — — — — — — — — 21.4 20.6 21.0 22.3 22.6 22.1 21.5 21.4 21.8 23.2 23.5 23.0 20.9 20.1 20.4 25.9 25.6 25.4 22.45 C 13 Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ N, expressed in ‰) in carbonate hydroxylapatite and collagen material ␦ 15 21.70 ( 23.23 ( 20.47 ( ␦ Ϫ Ϫ Ϫ O, and 18 ␦ 0.86) 0.62) 0.89) 0.27) 0.82) C, Ϯ Ϯ Ϯ Ϯ Ϯ 13 hydroxyl 4.5 3.9 2.8 2.1 5.8 3.7 2.2 4.1 2.8 3.1 5.2 3.7 3.2 4.3 3.3 2.7 2.1 2.3 2.6 2.7 3.4 1.5 3.3 2.1 2.9 3.3 2.8 4.0 4.2 4.6 3.7 3.9 ␦ O Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ 18 ␦ 3.73 ( 3.87 ( 3.54 ( 2.48 ( 2.64 ( Ϫ Ϫ Ϫ Ϫ Ϫ 0.49) 0.24) 0.70) 0.24) 0.61) Ϯ Ϯ Ϯ Ϯ Ϯ 7.1 7.0 6.2 6.4 7.8 6.9 7.3 6.4 7.0 8.7 7.7 7.6 6.9 8.2 7.7 8.2 8.3 8.5 8.1 8.7 5.9 7.3 5.9 6.8 6.3 7.4 7.1 6.7 6.3 8.3 7.0 6.2 hydroxyl C Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ 13 ␦ 6.77 ( 7.03 ( 7.50 ( 8.36 ( 6.44 ( Ϫ Ϫ Ϫ Ϫ Ϫ ected in large mammals species from Venta Micena. The relative abundance of strontium vs. zinc is shown. Asterisk also provided. able) are mples coll VM-3473 (b) VM-3503 (b) VM-4185 (b) VM-4444 (b) VM-OX7 (t) VM-3583 (b) VM-3473 (b) VM-544 (b) VM-4164 (b) VM-4439 (b)* VM-OX1 (t)* VM-3581 (b) VM-4123 (b) VM-OX6 (t) VM-4299 (b) VM-3448 (b) VM-3867a (b) VM-3867b (b) VM-OX10 (t) VM-3982 (b) VM-3802 (b) VM-3922 (b) VM-OX11 (t) VM-3157 (b) VM-3449 (b) VM-3297 (b) VM-4155 (b) VM-3111 (b) VM-3556 (b) VM-OX8 (t) VM-4181 (b) VM-3111 (b) iquus iquus iquus Mammuthus Hippopotamus Soergelia Hemitragus Species Sample Leptobos Leptobos Leptobos Leptobos Leptobos Leptobos Leptobos Leptobos Leptobos 2. Relative abundance of carbon, oxygen, and nitrogen isotope ratios ( Leptobos Mean for Bovini aff. Mean for Mean for Mean for Mean for ABLE indicates skeletal remains from juvenile individuals (i.e., limb bone with unfused epiphyses or milk tooth). Means for species ( which at least three estimates were avail extracted from bone (b) and tooth (t) sa Bovini aff. Bovini aff. Bovini aff. Bovini aff. Bovini aff. Bovini aff. Bovini aff. Bovini aff. Bovini aff. T Mammuthus meridionalis Mammuthus meridionalis Mammuthus meridionalis Hippopotamus ant Hippopotamus ant Hippopotamus ant Soergelia minor Soergelia minor Soergelia minor Soergelia minor Soergelia minor Hemitragus albus Hemitragus albus Hemitragus albus Hemitragus albus Hemitragus albus Eucladoceros giulii Eucladoceros giulii Eucladoceros giulii Eucladoceros giulii Eucladoceros giulii Eucladoceros giulii Eucladoceros giulii ECOLOGY OF PLEISTOCENE MAMMALS 217 0.7) 2.71) 5.59) 2.17) Ϯ Ϯ Ϯ Ϯ — — — — — — — — 68.1 67.2 65.7 64.9 67.8 66.2 78.2 82.4 70.7 78.2 89.9 73.1 73.5 72.6 78.4 82.5 80.1 86.9 91.9 89.3 87.3 90.8 41.3 45.8 45.5 48.2 51.9 Sr:Zn 67.0 ( 93.06 ( 78.15 ( 89.24 ( 0.17) 0.10) 0.12) 0.12) collagen Ϯ Ϯ Ϯ Ϯ — — — — — — — — — — — — — — — — 3.2 3.6 3.5 3.4 3.5 3.4 3.4 3.5 3.5 3.4 3.5 3.4 3.5 3.6 3.5 3.3 3.4 3.5 3.3 3.3 94.1 C:N 3.44 ( 3.43 ( 3.40 ( 3.37 ( 0.22) 0.21) 0.58) 0.20) Ϯ Ϯ Ϯ Ϯ collagen 1.4 2.5 2.9 2.6 2.0 3.5 3.0 3.3 3.5 2.1 2.8 3.1 3.9 3.7 3.5 6.8 5.8 6.1 6.5 5.3 — — — — — — — — — — — — — — — — N ϩ ϩ ϩ ϩ ϩ ϩ ϩ ϩ ϩ ϩ ϩ ϩ ϩ ϩ ϩ ϩ ϩ ϩ ϩ ϩ 15 ␦ 1.53 ( 2.67 ( 2.91 ( 3.70 ( ϩ ϩ ϩ ϩ 0.22) 0.31) 0.55) 0.21) ϩ Ϯ Ϯ Ϯ collagen — — — — — — — — — — — — — — — — 25.8 23.6 23.8 23.2 26.1 26.7 26.0 26.0 25.5 25.0 25.8 26.6 26.5 26.6 26.2 21.7 25.2 22.5 22.7 23.5 C 13 Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ ␦ 25.68 ( 23.53 ( 25.96 ( 26.43 ( Ϫ Ϫ Ϫ Ϫ 0.57) 0.29) 0.82) 0.59) Ϯ Ϯ Ϯ Ϯ hydroxyl 3.1 4.0 3.2 2.6 2.4 2.6 2.9 3.0 2.5 2.5 2.8 3.0 2.9 2.3 3.3 2.3 3.8 3.4 5.2 3.5 3.9 4.3 2.8 4.6 3.7 3.7 3.7 5.1 4.2 4.8 3.7 4.2 4.0 4.8 4.8 3.3 O Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ 18 ␦ 3.73 ( 2.74 ( 3.29 ( 4.26 ( Ϫ Ϫ Ϫ Ϫ 0.65) 0.49) 0.63) 0.78) Ϯ Ϯ Ϯ Ϯ 7.5 6.7 6.6 6.9 7.9 7.0 7.5 7.1 7.8 7.0 8.6 7.3 8.1 6.8 6.9 8.2 8.7 7.2 7.5 7.7 7.1 8.2 7.6 6.9 7.6 7.5 9.4 8.0 7.8 7.5 8.3 8.1 6.8 7.6 7.2 4.9 hydroxyl C Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ Ϫ 13 ␦ 7.02 ( 7.26 ( 7.64 ( 7.81 ( Ϫ Ϫ Ϫ Ϫ VM-3780 (b) VM-3124 (b) VM-3055 (b) VM-3482 (b) VM-4330 (b) VM-OX9 (t) VM-4410 (b) VM-3047 (b) VM-3060 (b) VM-3028 (b) VM-3119 (b) VM-3162 (b) VM-3258 (b) VM-3430 (b) VM-3529 (b) VM-4189 (b) VM-4421 (b) VM-OX2 (t) VM-OX3 (t) VM-3089 (b) VM-4421 (b) VM-3279 (b) VM-3428 (b) VM-3578 (b) VM-4487 (b) VM-4510 (b) VM-OX4 (t) VM-OX5 (t) VM-3610 (b) VM-3578 (b) VM-4340 (b) VM-3301 (b) VM-2226 (b) VM-2261 (b) VM-2254 (b) VM-1172 (b) Eucladoceros Dama Equus Stephanorhinus Species Sample 2. Continued. sp. sp. sp. sp. sp. sp. sp. Mean for Mean for Mean for Mean for ABLE Eucladoceros giulii T Eucladoceros giulii Dama Dama Dama Dama Dama Dama Dama Equus altidens Equus altidens Equus altidens Equus altidens Equus altidens Equus altidens Equus altidens Equus altidens Equus altidens Equus altidens Equus altidens Equus altidens Equus altidens Equus altidens Stephanorhinus etruscus Stephanorhinus etruscus Stephanorhinus etruscus Stephanorhinus etruscus Stephanorhinus etruscus Stephanorhinus etruscus Stephanorhinus etruscus Homotherium latidens Megantereon whitei Pachycrocuta brevirostris Canis falconeri Canis etruscus Ursus etruscus 218 PAUL PALMQVIST ET AL. strontium and zinc have proven particularly Voorhies 1965; Sillen 1986, 1992; Grupe and useful as indicators of paleodietary niches Kru¨ ger 1990; Sillen and Lee-Thorp 1994). (Toots and Voorhies 1965; Wyckoff and Dob- Strontium values can be used to determine erenz 1967; Sillen and Kavanagh 1982; Klepin- paleodiet provided the following conditions ger 1984; Nedin 1991). We analyzed the abun- are met: (1) only bones from the same locality dance of strontium and zinc in the bone tissue are compared, because trace element abun- of large mammals from Venta Micena with in- dance depends heavily on the geochemistry of ductively coupled plasma atomic emission the soil, which varies greatly between locali- spectrometry at Royal Holloway University of ties; (2) only adult bones are used, because ju- London. This was done on the resultant su- veniles show markedly reduced bone stron- pernatant from collagen extraction, evaporat- tium levels owing to the very small amounts ed to incipient dryness and re-dissolved in of strontium in mammalian milk; (3) teeth 40 mL of 3M HCl. Triplicate analyses resulted and ribs are discarded from the analysis, be- in an internal error of Ͻ10%. cause strontium levels in teeth do not change Strontium shares many chemical properties during growth and ribs, which are more met- with calcium, including partial replacement of abolically active than other bones, are prone to calcium in the metabolic processes of plants short-term resetting, especially in lactating fe- and animals. Strontium levels in bone are a males; (4) more than one species should be consequence of strontium levels in the soil and used for comparison; and (5) there is no evi- of biological factors (Toots and Voorhies 1965). dence of diagenetic alteration (Toots and Voor- Plants incorporate strontium in place of cal- hies 1965; Nedin 1991; Sillen 1992; Sillen and cium but the amount is determined by the rel- Lee-Thorp 1994). ative abundance of these elements in the soil. Relative levels of zinc and strontium in bone However, different kinds and even different have also been used as a tool for predicting paleodietary niches (Nedin 1991). However, in parts of plants vary in strontium content: tree contrast to strontium, zinc levels increase and bush leaves as well as the exposed parts through the food chain; carnivores have high- of succulent herbaceous vegetation are usu- er concentrations than herbivores because zinc ally enriched, whereas grass leaves and roots levels in blood and flesh are higher than in of trees, bushes and grasses appear to be de- plants (Elias et al. 1982). pleted (Bowen and Dymond 1955). Animals incorporate elements differentially; they dis- Paleodietary Inferences criminate against strontium, and as a result Table 2 shows ␦13C , ␦18O , and Sr: the proportion of Sr:Ca in the tissues and or- hydroxyl hydroxyl Zn values measured in bone and enamel ob- gans of herbivores is 50–80% less than the lev- tained from fossil mammals preserved at Ven- els in the plants that are ingested (Kshirasagar ta Micena (n ϭ 68). Collagen, preserved in et al. 1966; Schoeninger 1979). Uptake in car- only 37 out of 57 bone samples analyzed, pro- nivores also discriminates against the stron- 13 15 vided ␦ Ccollagen and ␦ Ncollagen values. The tium content of the flesh consumed. The pro- precision for stable-isotope analysis was portion of Sr:Ca is thus useful for discriminat- Ͻ0.1‰ for both carbon and oxygen, and ing between plant-eating, primary consumers Ͻ0.2‰ for nitrogen. C:N ratios of the collagen and flesh-eating, secondary consumers, be- material extracted averaged 3.4, and the ami- cause this proportion is a function of the initial no acid composition from four specimens is intake (Richards et al. 2000; Balter et al. 2001). similar to that of bone collagen in modern Similarly, strontium levels discriminate be- mammals, indicating good preservation (Fig. tween browsing, leaf-eating herbivores and 6). grazing herbivores, with the former showing The recovery of collagen in fossils older higher contents in their bones. Strontium levels than one million years is not rare, and high also allow identification of specific predator- amino acid concentrations have been found in prey pairs; the Sr:Ca ratio of the carnivore is fossils from Cretaceous–Pleistocene samples 50–80% less than that of its prey (Toots and (Wyckoff 1972; Ostrom et al. 1994), although ECOLOGY OF PLEISTOCENE MAMMALS 219

FIGURE 6. Amino acid spectra of the modern Tammar Wallaby (Macropus eugenii) (Gro¨cke 1997a) and the average amino acid abundance (hyp ϭ hydroxyproline; asp ϭ aspartic acid; thr ϭ threonine; ser ϭ serine; glu ϭ glutamic acid; pro ϭ proline; gly ϭ glycine; ala ϭ alanine; val ϭ valine; met ϭ methionine; ileu ϭ isoleucine; leu ϭ leucine; tyr ϭ tyrosine; phe ϭ phenylalanine; hyl ϭ hydroxylysine; lys ϭ lysine; his ϭ histidine; arg ϭ arginine) of four herbivore specimens from Venta Micena (VM-3473, VM-3867b, VM-3297, VM-3047). The similarity in composition of extant and extinct specimens indicates that the bone collagen preserved in the fossils was not altered during diagenesis. as noted above a number of specimens ana- ilar results were reported by Bocherens et al. lyzed here yielded no collagen. Other fossil (1996) and Franz-Odendaal et al. (2002) in the proteins (e.g., albumin and immunoglobulin) isotopic analyses of terrestrial mammals from have been detected in fossil samples from Ven- the early–middle Pleistocene site at Tighenif, ta Micena with immunological techniques Algeria, and from the early Pliocene site at (Torres et al. 2002). We have some reservations Langebaanweg, South Africa, respectively. In concerning the isotopic signature recorded in both localities all ungulate species showed 13 the bone apatite samples, however, because a ␦ Cenamel values exclusive of a diet of C3 plants. previous geochemical study (Arribas and The inferences that can be drawn from 13 Palmqvist 1998) showed that in several fossils ␦ Ccollagen values are complicated by physio- a fraction of the original hydroxylapatite was logical factors. According to the hypsodonty replaced during diagenesis by other mineral index, the Venta Micena perissodactyls in- phases. Therefore, the following discussion of clude one grazing species with high-crowned carbon isotopes focuses on the analysis of col- molars, the horse E. altidens, and another that lagen. was clearly a mixed feeder or browser given Carbon Isotope Ratios. Figure 7 shows a its low hypsodonty, the Etruscan rhino, S. 13 13 range of ␦ Ccollagen values from Ϫ20‰ to etruscus. Thus, the similarity in the ␦ Ccollagen Ϫ27‰ for large mammal species preserved at values shown by both monogastric herbivores Venta Micena, which agrees well with that of (Fig. 7) does not indicate either a similarity in modern mammals eating C3 plants. This in- their feeding requirements or differences with 13 dicates that C4 grasses were not a major con- those of other ungulates that show higher C/ stituent of the plant ecosystem in southern 12C ratios. A t-test indicates that the difference 13 Spain during early Pleistocene times. In fact, between the mean ␦ Ccollagen values for peris-

C4 plants are poorly represented today in the sodactyls (Ϫ26.09‰ Ϯ 0.52‰, n ϭ 11) and ar- vegetation of this semi-desert Mediterranean tiodactyls (Ϫ22.95‰ Ϯ 1.78‰, n ϭ 19) is sta- region, constituting only ϳ5% of grass species tistically significant (one-tailed test, adjusted (Sagredo 1987) and representing Ͻ1% of total for small sample size: t ϭ 6.23, p Ͻ 0.001). This plant biomass; their growth (from April to difference may owe to the fact that perisso- September) reflects a marked seasonality (J. dactyls, being hindgut fermenters, are less M. Nieto personal communication 2002). Sim- metabolically efficient for the extraction of nu- 220 PAUL PALMQVIST ET AL.

FIGURE 7. ␦13Cand␦15N values of collagen material extracted from bone samples of those species of large mammals preserved in the lower Pleistocene site at Venta Micena. The lines represent one standard deviation around the mean for those species in which three or more measurements of stable isotopes were available (data from Table 2). trients from plant foods (ϳ70% on average) erage) than those of non-ruminant ungulates than ruminants, which are foregut fermenters (Crutzen et al. 1986), because ruminant meth- (Janis 1976; Janis et al. 1994). Of interest to this ane has very negative ␦13C values (Metges et study, Cerling and Harris (1999) found that al. 1990). Burchell’s zebras, whose diet is composed of The Venta Micena bovids show the highest 13 100% grass, are consistently 1–2‰ depleted in ␦ Ccollagen levels among ruminants. The three ␦13C values for tooth enamel as compared species show hypsodonty values that are com- with sympatric ruminant hypergrazers such paratively high, similar to those of modern as alcelaphine bovids (e.g., buffalo, wilde- grazing and mixed feeding ruminants from beest, hartebeest, and topi) from Kenya, thus open habitats. Thus, the more positive 13 implying a lower isotope enrichment factor for ␦ Ccollagen values of bovids relative to those of zebras. A similar difference was detected by perissodactyls (Fig. 7) probably indicate that Lee-Thorp and Van der Merwe (1987) in bone the former predominantly fed on grass, hav- hydroxylapatite between zebra and wilde- ing a greater metabolic efficiency for the as- beest. The higher isotope enrichment of ru- similation of carbon. As mentioned above, the minants is probably related to their higher comparison of the hypsodonty values of cer- rates of methane production (six times, on av- vids with those of modern deer suggests that ECOLOGY OF PLEISTOCENE MAMMALS 221 the cervids were mixed feeders or browsers this paleocommunity (Palmqvist et al. 1996). from closed habitats. The difference between The large saber-tooth, H. latidens, shows the 13 15 the mean ␦ Ccollagen values for cervids highest ␦ Ncollagen value and this would indi- (Ϫ24.76‰ Ϯ 1.17‰, n ϭ 7) and bovids cate that it was the top predator in the paleo- 15 (Ϫ21.79‰ Ϯ 1.17‰, n ϭ 10) is statistically community. Interestingly, the single ␦ Ncollagen significant according to a t-test (t ϭ 5.15, p Ͻ value available for this species (Table 2, Fig. 7) 0.001). Such a difference, especially in the case is well above that obtained for the young in- of E. giulii, could indicate the influence of a hy- dividual of Mammuthus, suggesting that ju- perbrowsing behavior in a forested habitat venile elephants were an important part of the and the recycling of CO2 (i.e., the canopy ef- diet of this scimitar cat. The likelihood of such fect). Alternatively, cervids may exhibit a low- specialized hunting behavior is evident in the er metabolic efficiency to assimilate carbon case of the related American species H. serum, (and then a lower isotope enrichment factor) known in high numbers from the late Pleis- than bovids, which are more advanced rumi- tocene site of Friesenhahn cave, Texas. This lo- nants with a better compartmentalized stom- cality is interpreted as a saber-tooth den and ach. is associated with numerous skeletal remains Nitrogen Isotope Ratios. Figure 7 also shows of juvenile mammoths (Rawn-Schatzinger 15 ␦ Ncollagen values for large mammals from 1992; Marean and Ehrhardt 1995). C. falconeri, Venta Micena. It is interesting to mention that a cursorial canid that presumably hunted in the values recorded by all herbivore species an open environment, shows the second high- 15 except the hippo agree with those expected in est ␦ Ncollagen value among the hypercarni- animals consuming N2-fixing plants. Carni- vores. M. whitei, an ambush predator that vores H. latidens, M. whitei, P.brevirostris, C. fal- probably inhabited forests, records the lowest 15 coneri,andC. etruscus show higher values than ␦ Ncollagen value. Such differences may indicate ungulates except in the case of H. antiquus and that these carnivores preyed upon different one sample of M. meridionalis. The isotope en- ungulate species, with Megantereon hunting 15 richment in carnivores (mean ␦ Ncollagen for all browsing and mixed feeding cervids in a taxa: ϩ6.10‰) relative to herbivores (mean closed habitat, and the wild dogs focusing on 15 ␦ Ncollagen for all taxa, excluding the hippo: grazing bovids and horses from open envi- ϩ2.94‰) is in good accordance with the en- ronments. Interestingly, the large hyena P.bre- richment value expected from increasing one virostris, a species that scavenged the prey of trophic level (ϳ3.4‰), thus suggesting that these hypercarnivores (Arribas and Palmqvist 15 the collagen extracted from the fossils did not 1998), shows an intermediate ␦ Ncollagen value. undergo diagenetic alteration. The very high Finally, the medium-sized canid C. etruscus, 15 ␦ Ncollagen record of H. antiquus probably im- whose teeth indicate clearly a more omnivo- plies that this species fed predominantly on rous behavior than that of C. falconeri, records 15 aquatic, non-N2-fixing plants, instead of on C4 the lowest ␦ Ncollagen value of all the carni- grasses as in the case of modern H. amphibius. vores. Such a difference was also suggested by Boch- In the case of the ungulates, the ecomor- erens et al. (1996) for Pleistocene hippopotami phological analyses indicated that all peris- from several African localities. The elephant sodactyl and bovid species presumably inhab- 15 sample that shows a high ␦ Ncollagen value was ited an open environment, without tree cover, obtained from a bone specimen with unfused a finding corroborated by differences in nitro- epiphyses, which belonged to a young indi- gen isotope ratios. These species show more 15 vidual that may still have been suckling; the positive ␦ Ncollagen values (mean for all sam- other sample came from an adult individual ples: ϩ3.40‰ Ϯ 0.55‰, n ϭ 21) than cervids 15 and records a ␦ Ncollagen value similar to those (ϩ2.01‰ Ϯ 0.64‰, n ϭ 7). Such a difference of other herbivores. is statistically significant (t ϭ 4.37; p Ͻ 0.001) 15 Interesting differences in ␦ Ncollagen values and indicates that the latter species tended to 15 among the carnivore species are probably re- feed in a closed habitat. The lower ␦ Ncollagen lated to specific predator-prey relationships in values in the diet of cervids would have re- 222 PAUL PALMQVIST ET AL. sulted from greater soil acidity in the forest levels also provide additional information on (Rodie`re et al. 1996; Gro¨cke 1997a). This is the diet of large mammals from Venta Micena particularly the case for the megacerine deer (Table 2, Fig. 8). As expected from their higher 15 E. giulii, which exhibits the lowest ␦ Ncollagen position within the food chain, carnivores 15 values in the fauna. The high ␦ Ncollagen value show lower Sr:Zn ratios (range ϭ 41.3–51.9) of S. etruscus, a mixed feeding or browsing rhi- than herbivores (53.9–96.9, excluding the ju- no of open habitats, is congruent with that ex- venile elephant). This suggests that the origi- pected from a large monogastric herbivore nal abundances of both trace elements in the (Gro¨cke and Bocherens 1996). fossil bones were not altered during the dia- Oxygen Isotope Ratios. Bovids H. albus and genesis. S. minor and cervid Dama sp. show the highest Homotherium records the lowest Sr:Zn value 18 ␦ Ohydroxyl values among herbivores (Table 2). (41.3), as expected from its hypercarnivorous Given that the ␦18O value in plants is more diet. Megantereon shows a slightly higher ratio positive than in their source water (Sponhei- (45.8), which suggests a different habitat from mer and Lee-Thorp 2001; Harris and Cerling that of Homotherium and, hence, leaf-browsing 18 2002), the high ␦ Ohydroxyl values of these un- ungulates (which show higher Sr levels) as the gulates suggest that they obtained most of main prey. This interpretation agrees well their water requirements from the vegetation with the results obtained in the ecomorphol- rather than from drinking. On the contrary, ogical analysis, which indicate that Homother- the three megaherbivores represented in the ium was a pursuit predator whereas Meganter- assemblage (i.e., those species with a body eon was an ambusher. The giant hyena Pachy- mass above 1000 kg), M. meridionalis, H. antiq- crocuta, a bone crusher that presumably in- uus,andS. etruscus, as well as the megacerine habited open habitats, also shows a higher Sr: deer E. giulii, exhibit the most negative Zn ratio (45.5) than Homotherium, as expected 18 ␦ Ohydroxyl values, which indicate an increased from its diet, which included large amounts of 18 water dependence for these species. ␦ Ohydroxyl bone material (Palmqvist and Arribas 2001). values of the equid E. altidens and the bison The wild dog, C. falconeri, has a dentition ex- Bovini aff. Leptobos are intermediate but closer tremely specialized for meat-slicing and re- to those of megaherbivores and large deer, cords a lower Sr:Zn value (48.2) than the more suggesting that both species had moderate omnivorous species C. etruscus (51.9), which water dependence. These results agree well shows a well-developed talonid in the lower with expectations from their living closest rel- carnassial (Palmqvist et al. 1999). Such differ- atives. For example, goats are particularly well ence indicates that in the latter species bone adapted for arid conditions, obtaining most of material, as well as fruits and insects, proba- their water requirements from the vegetation bly composed a greater part of the diet. eaten (Novak 1999), and this also seems to Concerning the herbivores, Sr:Zn ratios are have been the case for the caprine Hemitragus higher in Bovini aff. Leptobos (mean ϭ 63.9, and the ovibovine Soergelia, according to their range ϭ 61.2–66.9, n ϭ 8), S. minor (mean ϭ 18 high mean values of ␦ Ohydroxyl. Similarly, the 64.0, range ϭ 62.8–65.6, n ϭ 4), and H. albus modern fallow deer, D. dama, tolerates more (mean ϭ 56.0, range ϭ 53.9–58.0, n ϭ 4) than arid climates than the red deer, Cervus elaphus, in the carnivores. These data agree well with showing a lower water intake rate per kg of the ecomorphologically based paleodietary body mass (Braza and Alvarez 1987). On the inference of a grazing niche in an open habitat contrary, large monogastric mammals such as for all these bovids, although it is worthy to rhinos, hippos and elephants are obligate mention that the goat, H. albus, records some- drinkers, with greater water requirements what low ratios. The medium-sized cervid, (Novak 1999), a characteristic that agrees well Dama sp., shows a relatively low Sr:Zn ratio 18 with the comparatively low ␦ Ohydroxyl values (mean ϭ 67.0, range ϭ 64.9–68.1, n ϭ 6), but measured for fossil Stephanorhinus, Hippopota- the large deer, E. giulii, records the highest ra- mus,andMammuthus. tio among ungulates (mean ϭ 93.1, range ϭ Trace Element Ratios. Strontium and zinc 89.9–96.9, n ϭ 5), as expected from its very ECOLOGY OF PLEISTOCENE MAMMALS 223

FIGURE 8. Sr:Zn abundance (%) and ␦15N collagen values (‰) of bone samples of large mammals preserved in Venta Micena (data from Table 2). low hypsodonty value, similar to that of mod- ancy could be due, perhaps, to the fact that ern hyperbrowsers. Such a difference could in- this species had a migratory behavior, as mod- dicate an ecological segregation between ern zebras do, and thus moved between local- Dama sp. and E. giulii, with the former inhab- ities. Finally, the strikingly low Sr:Zn ratio es- iting more open habitats and feeding more timated in one sample from M. meridionalis grass. The high Sr:Zn ratio obtained in the (27.8) may represent a young, suckling indi- case of S. etruscus (mean ϭ 89.2, range ϭ 86.9– vidual; the other sample analyzed, obtained 91.9, n ϭ 5) clearly indicates its browsing or from an adult elephant, records a value (70.1) mixed feeding diet, a conclusion previously in agreement with the mixed feeding diet in- inferred from the low values of the hypsodon- ferred for this species (Cerling et al. 1999). ty index and the length of the premolar tooth row. However, in the case of E. altidens the Taxon-Free Characterization of the moderately high Sr:Zn ratio (mean ϭ 78.2, Paleocommunity range ϭ 70.7–89.9, n ϭ 11) could suggest that Distribution by habitat type of large mam- it was a mixed feeder, a conclustion that mal species in modern African communities is would be in clear disagreement with the graz- shown in Figure 9. Community types were es- ing niche deduced from the very high hyp- tablished by Reed (1998) according to the veg- sodonty index in this species. This discrep- etation cover, and species were assigned to 224 PAUL PALMQVIST ET AL.

FIGURE 9. Average proportion of species of different locomotor types (A) and trophic groups (B ϭ herbivores, C ϭ carnivores) in several modern African communities of large mammals, established according to major vegetation types (frequencies of species estimated from data in Reed 1998). The corresponding values for the lower Pleistocene site at Venta Micena are also included (data from Table 1). Categories of vegetative habitats are broadly characterized and cluster forests (lowland rain, tropical temperate, and montane forests), closed woodlands (including woodland-bushland transition), bushlands (including medium density woodland and bushland areas), open woodlands, shrublands (including scrub woodlands), and savanna (including grasslands and plains). These habitats provide an ecological gradient from areas that are well watered throughout the year (forests) to those that are extremely dry or quite seasonal (shrublands and savannas). Deserts were not included in the analysis because Reed’s sample size of this habitat type was too small. Locomotor types include species adapted to arboreal locomotion (mostly primates), aquatic habitats (e.g., the hippo), mixed terrestrial and arboreal locomotion (e.g., the saber-tooth Me- gantereon), and exclusively terrestrial (e.g., the ungulates except the hippo and most carnivores) and/or fossorial species (e.g., the badger). Feeding categories as follows: frugivores, diet Ͼ50% of fruit; browsers, Ͼ75% leaves; mixed feeders; 25–75% grass; grazers: Ͼ75% grass; ﬂesh eaters, Ͼ70% vertebrate meat; meat/bone eaters, hyenas; meat/insects, 20–70% meat; omnivores, Ͻ20% meat.

several ecological categories by feeding be- increases as grass cover increases. The pro- havior and locomotion, following the ap- portions of locomotor types estimated for proach proposed by Andrews et al. (1979). Venta Micena, in which terrestrial species are The frequencies of such ecological categories dominant, are very similar to those in African in Venta Micena are also shown. savannas. The average frequencies of different When species are grouped by type of loco- types of primary consumers (Fig. 9B) also motion (Fig. 9A), the relative abundance of show a gradient from closed to open habitats. species adapted to arboreal locomotion is pos- In forested environments the dominant spe- itively correlated with the proportion of the cies are frugivores (largely represented by pri- habitat covered by trees and bushes. Con- mates) and browsing ungulates. In open hab- versely, the proportion of terrestrial species itats the most abundant species are mixed ECOLOGY OF PLEISTOCENE MAMMALS 225 feeders and grazers. The proportions of such habitat primary productivity. The three me- trophic categories in Venta Micena are again gaherbivores alone account for the consump- very close to those in modern savannas, al- tion of almost 186 kJ mϪ2 yearϪ1,or3.4gCmϪ2 though frugivores are absent from Venta Mi- yearϪ1. cena. Further, the frequencies of different Table 1 lists also the carnivores at Venta Mi- types of secondary consumers in Venta Mi- cena, which range in mass from 5 kg to 375 kg. cena (Fig. 9C) are similar to those shown by The on-crop biomass for each species was ob- such ecological categories in modern savannas tained by multiplying the calculated popula- and shrublands. The main difference is the tion density by its body mass. The total on- proportion of omnivorous species, which are crop biomass for these carnivores was 71.1 kg represented exclusively by the bear because kmϪ2,or497JmϪ2. Adding up the require- suids are absent from Europe during the early ments of all the large carnivore species, and Pleistocene. converting the units, it follows that they must These results indicate that the region that have needed about 6.6 kJ mϪ2 yearϪ1 as habitat surrounded the Pleistocene lake of Orce at secondary productivity to sustain their basal Venta Micena was very similar to that repre- metabolism if an assimilation efficiency of sented in modern African savannas with tall 50% was assumed (see Peters 1983). It was also grass and low bush/tree cover, suggesing that assumed that the actual maintenance metab- the countryside in the Guadix-Baza basin was olism was 2.5 times as high as the basal rate. relatively unforested during early Pleistocene Therefore, the energy required to carry their times, as happens today. maintenance metabolism was about 16.5 kJ Such reconstruction can be assessed also mϪ2 yearϪ1. For an on-crop biomass such as through an analysis of another aspect of the that estimated here, the net above ground pri- trophic relationships of this fauna, following mary productivity predicted by the equation the general ecological relationships between of McNaughton et al. (1989) is 14.5 MJ mϪ2 population density and body size (Damuth yearϪ1, a figure congruent with that expected 1987) and between basal metabolic rate and for an open environment such as that pro- body size (Kleiber 1932; McNab 1980). This posed above. A savanna has a productivity of type of approach has previously been applied 130gCmϪ2 yearϪ1, or 7.3 MJ mϪ2 yearϪ1 (Mar- to both South and North American faunas at galef 1980). This savanna possibly had small Lujań and Rancho La Brea (Farinã 1996). wooded areas, as deduced from the presence All of the herbivore species found at Venta of the hyperbrowsing deer Eucladoceros; in this Micena were classified according to their case its productivity would have doubled, and probable diet (those species whose masses the estimate of productivity would therefore were estimated at Ͻ10 kg were not consid- be congruent. It should be further taken into ered), and their population densities and basal account that some of the herbivore species are metabolic rates were estimated (Table 1) ac- poorly represented (e.g., Praeovibos sp. and the cording to the appropriate equations of Da- small caprine), which suggests that they may muth (1987) and Peters (1983). The energy re- have been transient species and therefore quirements for each species were obtained by should not be completely included in the re- multiplying its on-crop biomass by its basal quirements of the herbivores. Moreover, ac- metabolic rate. A typical assimilation efficien- cording to nitrogen isotopes, the hippo must cy of 50% (of the edible material) was as- have fed at least partially on aquatic vegeta- sumed, and average actual maintenance me- tion, which may have reduced even more the tabolism was taken to be 2.5 times the basal overall herbivores requirements. rate, an average of the values given for modern As stated earlier, the metabolic require- species (2 to 3, according to Peters 1983). Add- ments of the large carnivores would have been ing up the requirements of all the herbivore fulfilled with 16.5 kJ mϪ2 year Ϫ1. The second- species considered, and converting the units, ary productivity predicted by the appropriate it follows that they must have needed some equations of McNaughton et al. (1989) for an 683 kJ mϪ2 yearϪ1,or12.5gCmϪ2 yearϪ1,in ecosystem able to support the herbivore bio- 226 PAUL PALMQVIST ET AL. mass inferred above is 20 kJ mϪ2 year Ϫ1,ora ———. 1999. On the ecological connection between sabre-tooths and hominids: faunal dispersal events in the lower Pleisto- bit lower according to the primary productiv- cene and a review of the evidence for the first human arrival ity estimated after Margalef (1980). Further, if in Europe. Journal of Archaeological Science 26:571–585. a growth efficiency of 0.025 is assumed (Peters Ayliffe, L. K., A. M. Lister, and A. R. Chivas. 1992. The preservation of glacial-interglacial climatic signatures in the oxygen 1983), the secondary productivity must have isotopes of elephant skeletal phosphate. Palaeogeography,Pa- Ϫ2 Ϫ1 reached 17.1 kJ m year . Both figures are laeoclimatology, Palaeoecology 99:179–191. very close to that obtained for the require- Balter, V., A. Person, N. Labourdette, D. Drucker, M. Renard, and B. Vandermeersch. 2001. Les Neándertaliens e´taient-ils ments of the carnivores, suggesting that all essentiellement carnivores? Re´sultats pre´liminaires sur les te- large carnivore species living in the original neurs en Sr et Ba de la paleóbiocenose mammalienne de Saint- paleocommunity were finally represented in Ce´saire. Comptes Rendus de l’Acade´mie des Sciences, se´rie II, the bone assemblage collected by the hyenas. 332:59–65. Biknevicius, A. R., and B. Van Valkenburgh. 1996. Design for This is congruent with the results obtained by killing: craniodental adaptations of predators. Pp. 393–428 in Arribas and Palmqvist (1998) in the compari- J. L. Gittleman, ed. Carnivore behavior, ecology, and evolu- son of the taxonomic composition of the fau- tion, Vol. 2. Cornell University Press, Ithaca, N.Y. Biknevicius, A. R., B. Van Valkenburgh, and J. Walker. 1996. In- nal assemblage preserved at Venta Micena cisor size and shape: implications for feeding behaviors in sa- with those from other Plio-Pleistocene locali- ber-toothed ‘‘cats.’’ Journal of Vertebrate Paleontology 16: ties of the Guadix-Baza Basin. 510–521. Bocherens, H., P. L. Koch, A. Mariotti, D. Geraads, and J. J. Jae- ger. 1996. Isotopic biogeochemistry (13C, 18O) and mammalian Acknowledgments enamel from African Pleistocene hominid sites. Palaios 11: 306–318. C. Nedin and S. Vizcaıńo provided useful Bowen, H. J. M., and J. A. Dymond. 1955. Strontium and barium comments on trace element ratios and eco- in plants and soils. Proceedings of the Royal Society of Lon- morphological analyses, respectively. B. Mar- don B 144:355–368. tıńez-Navarro and J. L. Santamarıá provided Braza, F., and F. Alvarez. 1987. Habitat use by red deer and fallow deer in Donãna National Park. 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