Carbon-13 and oxygen-18 abundances were measured in large mammal skeletal remains (tooth enamel, dentine and bone) from the Chiwondo Beds in Malawi, which were dated by biostratigraphic correlation to ca. 2.5 million years ago. The biologic isotopic patterns, in particular the difference in carbon-13 abundances between grazers and browsers and the difference in oxygen-18 abundances between semi-aquatic and terrestrial herbivores, were preserved in enamel, but not in dentine and bone. The isotopic results obtained from the skeletal remains from the Chiwondo Beds indicate a dominance of savannah habitats with some trees and shrubs. This environment was more arid than the contemporaneous Ndolanya Beds in Tanzania. The present study confirms that robust australopithecines were able to live in relatively arid environments and were not confined to more mesic environments elsewhere in southern Africa.

Links between the environment and key episodes of hominin evolution in Africa have often been suggested.^1,2,3,4,5,6 It is therefore of prime importance to have the most accurate knowledge of the environmental conditions at the time and place that hominins were present. Isotopic investigations of mammal remains from Plio-Pleistocene hominin sites have proved highly informative regarding palaeoecosystems in southern and eastern Africa.^{7,8,9,10,11,12,13,14,15,16,17} To date no such investigation has been attempted in Malawi – an area that has yielded hominin fossils important for closing the gap between localities in southern and eastern Africa.^18,19,20 A recent study of the mammalian fauna indicated a palaeoecological reconstruction that was relatively arid, with a strong affinity to the Somalia-Masai ecozone, and more arid than it is today.²¹ However, the study was made difficult by the taphonomic biases of the localities²² leading to the preferential preservation of large species. To help in refining this palaeoecological reconstruction, we present here preliminary isotopic results on mammal remains from unit 3A of the Chiwondo Beds that yielded Homo rudolfensis and Paranthropus boisei.^18,23 The fauna from both hominin sites are biostratigraphically correlated to the Plio-Pleistocene boundary, around 2.5 million years ago (MYA), a period for which an aridification event has been tentatively linked to a turnover and a radiation of hominin species, with the first appearance of the genera Paranthropus and Homo.^24,25 For almost 50 years, the conventional opinion on this dichotomy of the hominin clade has favoured the hypothesis that the major adaptive differences between the Homo and Paranthropus lineages developed because of the increasing dietary specialisation of Paranthropus as a result of climate change, while Homo adopted a generalist strategy.²⁶ Wood and Strait²⁷ tested the diet/climate hypothesis by analysing a set of criteria and suggested that both genera probably were eurytrope and that derived morphology does not always mirror specialised adaptation towards a particular diet or habitat preference. Therefore it is striking to see how many of the habitat reconstructions for early Homo and Paranthropus draw a mosaic picture, interpreting that both hominin groups existed in variable environments. The goal of this study is to evaluate the state of preservation of the fossil mammal material for carbonate isotopic investigations and to draw some first conclusions on the palaeoenvironment inhabited by these early hominins in south-east Africa in order to improve our knowledge about their environmental distribution and constraints.

The relative abundance of carbon-13 (¹³C) in mammalian tissues is directly linked to their average diet. In African tropical environments, two types of vegetation are clearly distinguished by their carbon isotopic signatures: plants using the C3 photosynthetic pathway (trees and shrubs) and plants using the C4 photosynthetic pathway (grasses). As herbivores record the carbon isotopic signature of their plant food, analysing their fossil remains allows the reconstruction of some aspects of the vegetation in their preferred habitat, as long as the isotopic signatures have not been significantly modified post-mortem. Some species exhibit a restricted dietary spectrum and can be used as tracers of possible diagenetic alteration.²⁸ For example, giraffes and the proboscidian Deinotherium are exclusively browsers and therefore exhibit C3-consumer isotopic signatures, while the Alcelaphini antelopes exclusively consume C4 grasses.^{10,29,30,31,32} In contrast, other species are more opportunistic and their carbon isotopic signatures can be used to evaluate the relative importance of C3 and C4 plants available to them. For instance, hippopotamuses consume different amounts of C3 plants depending on their availability.^8,33,34,35

Oxygen-18 (¹⁸O) abundances in skeletal tissues are linked to those of drinking water and water contained in the food, and they vary according to temperature and aridity. They typically increase with increasing temperature and decreasing precipitation.^36,37 Different habitats and water conservation strategies between herbivores lead to coherent patterns in the oxygen isotopic signatures of African herbivores, with giraffes systematically ¹⁸O-enriched compared to other terrestrial herbivores^11,38 and hippopotamuses systematically ¹⁸O-depleted compared to terrestrial herbivores.^8,34,39 These biogenic patterns can also be used to track possible diagenetic alteration in fossil material. The variations of δ¹⁸O values of a given herbivorous species through space and time can be tentatively related to changes in climatic conditions, but caution is necessary in the interpretation of small datasets as terrestrial mammals typically exhibit significant variation of their δ¹⁸O values within a living population.³⁹

All specimens studied were derived from unit 3A-2 in the Chiwondo Beds (Malawi), either from Malema RC11 (12 specimens) or from Uraha (2 specimens). Biozone 2 in unit 3A is relatively dated by the correlation of suid remains with other radiometric dated sites in eastern and South Africa to between 2.5 MYA and 2.3 MYA. Most of the material comes from the Malema excavation site RC11 from the same level that yielded the Paranthropus maxilla fragment HCRP-RC-911.^20,21 Tooth or jawbone fragments with teeth have been selected from the following taxa: proboscidians (Deinotherium sp., Elephas recki), giraffids (Giraffa sp., Sivatherium sp.), bovids (one undetermined specimen, Megalotragus sp.), camel (Camelus sp.), Hippopotamus sp. and equids (Hipparion sp.). Small enamel fragments were retrieved, as well as fragments of dentine and bone for some specimens (Table 1). Whenever possible, the calcareous matrix was also sampled. Comparing enamel, dentine, bone and limestone isotopic signatures allows evaluation of possible diagenetic alteration of the isotopic signatures.^40,41,42

A chemical pre-treatment aimed at the removal of exogenous contaminants, such as organic residues and carbonates, was applied to the enamel, dentine and bone samples.⁸ Powdered samples were soaked in 2–3% NaOCl for 20 h at 20 °C to oxidise organic residues, rinsed with distilled water, then treated with 1 M acetic acid-Ca acetate buffer (pH = 4.75) for 20 h at 20 °C to remove exogenous carbonate. Carbon dioxide was produced from the treated powders (± 15 mg) by dissolution in 100% H₃PO₄ at 50 °C for 5 h. Carbon dioxide was collected and purified by cryogenic distillation in a vacuum line, and carbon isotope compositions were measured on a VG Optima gas source mass spectrometer (Manchester, UK). The isotopic ratios are expressed as δ¹³C and δ¹⁸O values with an analytical precision better than 0.1‰ and 0.2‰, respectively; the international standards are PeeDee belemnite (PDB) and standard mean ocean water (SMOW) for δ¹³C and δ¹⁸O values, respectively.⁸

The carbon and oxygen isotopic signatures of enamel exhibited a much larger variation than those of dentine, bone and embedding limestone (Table 1, Figure 1). The δ¹³C values ranged from -12.9‰ to +1.6‰ in enamel, from -7.9‰ to -1.5‰ in dentine, from -4.0‰ to -2.7‰ in bone and from -9.4‰ to -7.4‰ in embedding limestone. A similar pattern was observed for δ¹⁸O values: they ranged from 28.0‰ to 35.7‰ in enamel, from 29.8‰ to 31.7‰ in dentine, from 28.3‰ to 31.2‰ in bone and from 24.0‰ to 26.1‰ in embedding limestone.

The isotopic signatures of fossil enamel were clearly related to the specific origin of the samples. The browsing taxa, such as Giraffa and Deinotherium, clearly exhibited δ¹³C values indicating exclusive consumption of C3 plants (-12.9‰ to -11.3‰), while Megalotragus, a specialised grazer, exhibited δ¹³C values typical of exclusive C4-plant consumption (1.3‰ to 1.6‰). The variations of the δ¹⁸O values were also related to taxonomic affinity of the samples: the Giraffa samples exhibited the most positive δ¹⁸O values (34.4‰ and 35.7‰) while Hippopotamus specimens exhibited slightly less positive δ¹⁸O values (29.1‰ and 30.1‰).

Figure 1: δ13C and δ18O values of enamel, dentine, bone and limestone matrix from samples from the Chiwondo Beds. Arrows connect the enamel and dentine values from the same tooth.

Effects of diagenetic alteration and preservation of enamel isotopic signals

Palaeoenvironmental reconstruction of the Chiwondo Beds

(Table 1 and Figure 2). This fossil genus has been interpreted as a mixed feeder based on hypsodonty and tooth wear,⁴³ and it seems that the studied individual from Malema incorporated some C4 grass in its diet. This was, however, not the case for Sivatherium marusium from Makapansgat member 3 dated to 3 MYA, that exhibited δ¹³C values similar to those of Giraffa in the same site.¹⁵ This difference could indicate that Malema is a more open environment than the South African site, Makapansgat.

Both Hippopotamus analysed in this study exhibited high δ¹³C values, indicating a purely C4 diet. Such values are reached in modern Hippopotamus living in open surroundings without closed forests.³³ These isotopic values suggest a predominance of open environments dominated by C4 plants.

In conclusion, the environmental reconstruction that can be tentatively drawn from the available isotopic data suggests a dominance of savannah habitats, based on the δ¹³C values of Hippopotamus and possibly Sivatherium, with some trees and shrubs yielding C3 biomass present, as indicated by the low δ¹³C values of Deinotherium, Camelus and Giraffa.

Figure 2: δ13C and δ18O values of enamel from different large mammal species from the Chiwondo Beds.

Regional comparison

Implications for hominin palaeoecology

P. boisei possibly had a broad ecological tolerance. According to Reed⁵⁵, P. robustus appears to be slightly more arid adapted than eastern African P. boisei. In any case, the appearance of P. boisei in the Chiwondo Beds about 2.5 MYA suggests ecological conditions that may be comparable to the ones of A. robustus in South Africa after 2 MYA.

Interestingly, carbon isotopic data have been recently published for P. boisei from Tanzania, at Olduvai East and Peninj.¹³ In contrast with the robust australopithecines from South Africa that present δ¹³C values indicative of limited amounts of C4 biomass in their diet, those from eastern Africa exhibit δ¹³C values of about -1.0‰, indicating a C4 biomass in their diet of up to 80%. It remains unclear if this very high C4 component was acquired directly through C4 grasses, especially their seeds (though these are highly seasonal resources), or indirectly through the consumption of the flesh of herbivores that consumed C4 plants, other small mammals or invertebrates, such as termites.^55,56 Another possibility is the consumption of sedges such as papyrus, a semi-aquatic plant that bears perennial underground storage organs available to hominins all year round.^13,57

The geographic position of the Malawi Rift in south-eastern Africa is of special interest when comparing the dietary adaptations of east and South African robust australopithecines. Ungar et al.⁵⁸ showed that the diet of

P. boisei included similar amounts of tough (or fibrous) foods to that of A. africanus. In contrast, the food of P. robustus was much harder (including seeds, nuts and hard fruits) but less tough (i.e. there were fewer fibrous foods such as leaves) than that of P. boisei. Additional isotopic data may prove whether this distinction is as a result of different diets or different feeding strategies.

Figure 3: Comparison of δ13C and δ18O values of enamel in selected species from the Chiwondo Beds (CB) and the Ndolanya Beds (NB).

The isotopic preservation of tooth enamel carbonate fraction in the fossil mammals of the Chiwondo Beds was sufficient to allow preliminary palaeoenvironmental reconstruction. This reconstruction, based on the analysis of δ¹³C and δ¹⁸O values of large herbivorous mammal tooth enamel, was consistent with that based on the analysis of the faunal community.^20,21,59 The environment was dominated by a savannah ecosystem with some trees, and was probably drier than the modern ecosystem in this region. The environment in the Chiwondo Beds was possibly drier than in Tanzanian sites at the same period, about 2.5 MYA, but additional isotopic data are necessary to confirm this trend.

The present study supports the view that P. boisei was able to live in arid environments and underlines the broad ecological spectrum of this hominin.

We acknowledge the technical assistance of D. Billiou and A. Zazzo in the Department of Earth Sciences of University Paris 6 (France) in the preparation and isotopic analysis of the specimens. We also thank the Department of Antiquities, Lilongwe and the Cultural and Museum Centre Karonga for permitting access to the material. We express our gratitude to W. Joyce for his help in editing this manuscript, and to A. Morris and three anonymous reviewers for the suggested improvements to this manuscript.

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