Hominin palaeoecology in Late Pliocene Malawi : First insights from isotopes ( 13 C , 18 O ) in mammal teeth

© 2011. The Authors. Licensee: OpenJournals Publishing. This work is licensed under the Creative Commons Attribution License. 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.


Introduction
Links between the environment and key episodes of hominin evolution in Africa have often been suggested. 1,2,3,4,5,6It 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. 7,8,9,10,11,12,13,14,15,16,17To 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. 18,19,20A 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. 21owever, the study was made difficult by the taphonomic biases of the localities 22 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. 18,23The 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. 24,25or 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. 26Wood and Strait 27 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.

Significance of isotopic (palaeo-)ecology
The relative abundance of carbon-13 ( 13 C) 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. 28For example, giraffes and the proboscidian http://www.sajs.co.za S Afr J Sci 2011; 107(3/4) Deinotherium are exclusively browsers and therefore exhibit C3-consumer isotopic signatures, while the Alcelaphini antelopes exclusively consume C4 grasses. 10,29,30,31,32In 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. 8,33,34,35ygen-18 ( 18 O) 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. 36,37Different habitats and water conservation strategies between herbivores lead to coherent patterns in the oxygen isotopic signatures of African herbivores, with giraffes systematically 18 O-enriched compared to other terrestrial herbivores 11,38 and hippopotamuses systematically 18 O-depleted compared to terrestrial herbivores. 8,34,39These biogenic patterns can also be used to track possible diagenetic alteration in fossil material.The variations of δ 18 O 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 δ 18 O values within a living population. 39

Materials and methods
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. 20,21Tooth 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. 40,41,42chemical pre-treatment aimed at the removal of exogenous contaminants, such as organic residues and carbonates, was applied to the enamel, dentine and bone samples. 8Powdered 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% H 3 PO 4 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 δ 13 C and δ 18 O 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 δ 13 C and δ 18 O values, respectively. 8

Results
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).

Effects of diagenetic alteration and preservation of enamel isotopic signals
The predicted biogenic patterns in δ 13 C values were found for the enamel isotopic signatures in exclusive browsers such as Giraffa and Deinotherium, in comparison to grazers such as Megalotragus.Giraffids exhibited more positive δ 18 O values than other herbivores and Hippopotamus exhibited lower δ 18 O values than the average of terrestrial herbivores.In contrast, the isotopic signatures of dentine and bone from the same specimens did not display such a clear trend.For instance the δ 13 C values tended to gather around intermediate values ranging from -8‰ to -1‰, instead of clustering according to the predicted dietary preferences (Figure 1).Interestingly, the δ 13 C values of carbonate from the surrounding matrix and concretions showed δ 13 C values between -10‰ and -7‰, which suggests that the δ 13 C values of dentine were influenced by this background carbon, especially for grazers that tended to shift towards these values.A similar pattern was visible for the δ 18 O values, in which the differences related to taxonomic affiliation exhibited in enamel were not reflected in bone and dentine (Figure 1).This pattern suggests that the δ 18 O values of bone and dentine were also affected by diagenetic alteration, in contrast with those of enamel.These results are similar to those published by Lee-Thorp 28 on South African material.In this study, there was no evidence that the enamel isotopic ratios were significantly altered by diagenesis.

Palaeoenvironmental reconstruction of the Chiwondo Beds
Although the small number of individuals analysed per species does not allow statistically based inferences, the isotopic patterns seen in various taxa will be used to draw preliminary palaeoenvironmental conclusions.An interesting pattern is observed in the giraffid Sivatherium, which exhibited less negative δ 13 C values than the purely browsing Giraffa, -7.9‰ compared to -11.3‰ to -12.8‰ (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 δ 13 C values similar to those of Giraffa in the same site. 15This difference could indicate that Malema is a more open environment than the South African site, Makapansgat.In conclusion, the environmental reconstruction that can be tentatively drawn from the available isotopic data suggests a dominance of savannah habitats, based on the δ 13 C values of Hippopotamus and possibly Sivatherium, with some trees and shrubs yielding C3 biomass present, as indicated by the low δ 13 C values of Deinotherium, Camelus and Giraffa.

Regional comparison
A preliminary comparison is possible with contemporaneous sites in eastern and southern Africa; specifically the Ndolanya Beds at Laetoli (Tanzania) and Swartkrans 1 (South Africa), for which the carbon and oxygen isotopic signatures of fossil material have been published. 11,44Comparison of the isotopic data with Swartkrans is made difficult by the fact that δ 18 O values are not published and the taxa are different from those in the Chiwondo Beds.Nevertheless, the bovid assemblage in general indicates more arid conditions at Swartkrans than at Sterkfontein, 45,46 suggesting a less woodland and more open habitat at Swartkrans -a conclusion also supported by a comparison of the micromammal fauna 47 and the stable carbon isotopes of fossil mammals 48 from these cave sites.In contrast, there are common taxa in the Chiwondo Beds and Ndolanya Beds, such as Sivatherium, Alcelaphini, Hipparion (=Eurygnathohippus), elephantids (Loxodonta cf.exoptata and Elephas recki, respectively) providing δ 13 C values that can be compared between both sites (Figure 3).Elephantids and Hipparion do not exhibit a clear pattern for δ 13 C and δ 18 O values, but for Alcelaphini and Sivatherium, the δ 13 C values appear slightly more positive in the Chiwondo Beds and the δ 18 O clearly more positive.This could reflect more arid conditions for the Chiwondo Beds than for the Ndolanya Beds.The latter has been interpreted as semi-arid bushland, 49 comprising a faunal mixture of 75% from bushland and 25% from grassland habitats 50 and corresponding to an area dominated by wooded grassland, ranging from limited areas of closed woodland to much more extensive areas of open bushland and grassland. 51At present, the preliminary results on Sivatherium, present in both sites, suggest more arid conditions in south-eastern than in eastern Africa.

Implications for hominin palaeoecology
The discoveries of Paranthropus aethiopicus in the Ndolanya Beds, 52 and of P. boisei in the Chiwondo Beds 19 imply that the eastern African robust australopithecines could adapt to open bushland and grassland conditions.This finding is quite striking because the Laetoli area has never been adjacent to a lake, while the Chiwondo Beds' fauna was associated with a lake throughout most of its succession.Wood  Interestingly, carbon isotopic data have been recently published for P. boisei from Tanzania, at Olduvai East and Peninj. 13In contrast with the robust australopithecines from South Africa that present δ 13 C values indicative of limited amounts of C4 biomass in their diet, those from eastern Africa exhibit δ 13 C 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. 55,56Another 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. 13,57e geographic position of the Malawi Rift in southeastern 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.

Conclusion
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 δ 13 C and δ 18 O values of large herbivorous mammal tooth enamel, was consistent with that based on the analysis of the faunal community. 20,21,59he 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.

FIGURE 1 :
FIGURE 1: δ 13 C and δ 18 O 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.

FIGURE 2 :
FIGURE 2: δ 13 C and δ 18 O values of enamel from different large mammal species from the Chiwondo Beds.

FIGURE 3 :
FIGURE 3: Comparison of δ 13 C and δ 18 O values of enamel in selected species from the Chiwondo Beds (CB) and the Ndolanya Beds (NB).

TABLE 1 :
List of isotopic results obtained on fossil material from the Chiwondo Beds, Malawi.
SMOW, standard mean ocean water.
55d Constantino53summarised the combined evidence of locality reconstructions and indicated that P. boisei favours grassland and/or open woodland habitats.Although Shipman and Harris 54 placed P. boisei towards the closed habitat spectrum, Wood and Constantino53and Wood and Strait 27 argue that 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.