Kevin T. Uno

Diet of Paranthropus boisei in the early Pleistocene of East Africa

The East African hominin Paranthropus boisei was characterized by a suite of craniodental features that have been widely interpreted as adaptations to a diet that consisted of hard objects that required powerful peak masticatory loads. These morphological adaptations represent the culmination of an evolutionary trend that began in earlier taxa such as Australopithecus afarensis, and presumably facilitated utilization of open habitats in the Plio-Pleistocene. Here, we use stable isotopes to show that P. boisei had a diet that was dominated by C4 biomass such as grasses or sedges. Its diet included more C4 biomass than any other hominin studied to date, including its congener Paranthropus robustus from South Africa. These results, coupled with recent evidence from dental microwear, may indicate that the remarkable craniodental morphology of this taxon represents an adaptation for processing large quantities of low-quality vegetation rather than hard objects.

Stable isotope-based diet reconstructions of Turkana Basin hominins

Hominin fossil evidence in the Turkana Basin in Kenya from ca. 4.1 to 1.4 Ma samples two archaic early hominin genera and records some of the early evolutionary history of Paranthropus and Homo. Stable carbon isotopes in fossil tooth enamel are used to estimate the fraction of diet derived from C3 or C4 resources in these hominin taxa. The earliest hominin species in the Turkana Basin, Australopithecus anamensis, derived nearly all of its diet from C3 resources. Subsequently, by ca. 3.3 Ma, the later Kenyanthropus platyops had a very wide dietary range—from virtually a purely C3 resource-based diet to one dominated by C4 resources. By ca. 2 Ma, hominins in the Turkana Basin had split into two distinct groups: specimens attributable to the genus Homo provide evidence for a diet with a ca. 65/35 ratio of C3- to C4-based resources, whereas P. boisei had a higher fraction of C4-based diet (ca. 25/75 ratio). Homo sp. increased the fraction of C4-based resources in the diet through ca. 1.5 Ma, whereas P. boisei maintained its high dependency on C4-derived resources.

Late Miocene to Pliocene carbon isotope record of differential diet change among East African herbivores.

Stable isotope and molecular data suggest that C4 grasses first appeared globally in the Oligocene. In East Africa, stable isotope data from pedogenic carbonate and fossil tooth enamel suggest a first appearance between 15–10 Ma and subsequent expansion during the Plio-Pleistocene. The fossil enamel record has the potential to provide detailed information about the rates of dietary adaptation to this new resource among different herbivore lineages. We present carbon isotope data from 452 fossil teeth that record differential rates of diet change from C3 to mixed C3/C4 or C4 diets among East African herbivore families at seven different time periods during the Late Miocene to the Pliocene (9.9–3.2 Ma). Significant amounts of C4 grasses were present in equid diets beginning at 9.9 Ma and in rhinocerotid diets by 9.6 Ma, although there is no isotopic evidence for expansive C4 grasslands in this part of the Late Miocene. Bovids and hippopotamids followed suit with individuals that had C4-dominated (>65%) diets by 7.4 Ma. Suids adopted C4-dominated diets between 6.5 and 4.2 Ma. Gomphotheriids and elephantids had mostly C3-dominated diets through 9.3 Ma, but became dedicated C4 grazers by 6.5 Ma. Deinotheriids and giraffids maintained a predominantly C3 diet throughout the record. The sequence of differential diet change among herbivore lineages provides ecological insight into a key period of hominid evolution and valuable information for future studies that focus on morphological changes associated with diet change.

Dietary changes of large herbivores in the Turkana Basin, Kenya from 4 to 1 Ma

Significance Stable carbon isotopes give diet information for both modern and fossil mammals and can be used to classify diets as C4 grazers, C3–C4 mixed, or C3 browsers. We show that diets of some major African herbivore lineages have significantly changed over the past 4 million years by comparing fossils from the Turkana Basin in Kenya with modern mammals from East and Central Africa. Some fossil assemblages have no modern analogues in East and Central Africa, suggesting different ecological functions for some mammals in the past as compared with their modern counterparts. The development of modern tropical grassland ecosystems are products of the coevolution of both grasses and herbivores. A large stable isotope dataset from East and Central Africa from ca. 30 regional collection sites that range from forest to grassland shows that most extant East and Central African large herbivore taxa have diets dominated by C4 grazing or C3 browsing. Comparison with the fossil record shows that faunal assemblages from ca. 4.1–2.35 Ma in the Turkana Basin had a greater diversity of C3–C4 mixed feeding taxa than is presently found in modern East and Central African environments. In contrast, the period from 2.35 to 1.0 Ma had more C4-grazing taxa, especially nonruminant C4-grazing taxa, than are found in modern environments in East and Central Africa. Many nonbovid C4 grazers became extinct in Africa, notably the suid Notochoerus, the hipparion equid Eurygnathohippus, the giraffid Sivatherium, and the elephantid Elephas. Other important nonruminant C4-grazing taxa switched to browsing, including suids in the lineage Kolpochoerus-Hylochoerus and the elephant Loxodonta. Many modern herbivore taxa in Africa have diets that differ significantly from their fossil relatives. Elephants and tragelaphin bovids are two groups often used for paleoecological insight, yet their fossil diets were very different from their modern closest relatives; therefore, their taxonomic presence in a fossil assemblage does not indicate they had a similar ecological function in the past as they do at present. Overall, we find ecological assemblages of C3-browsing, C3–C4-mixed feeding, and C4-grazing taxa in the Turkana Basin fossil record that are different from any modern ecosystem in East or Central Africa.

Bomb-curve radiocarbon measurement of recent biologic tissues and applications to wildlife forensics and stable isotope (paleo)ecology

Above-ground thermonuclear weapons testing from 1952 through 1962 nearly doubled the concentration of radiocarbon (14C) in the atmosphere. As a result, organic material formed during or after this period may be radiocarbon-dated using the abrupt rise and steady fall of the atmospheric 14C concentration known as the bomb-curve. We test the accuracy of accelerator mass spectrometry radiocarbon dating of 29 herbivore and plant tissues collected on known dates between 1905 and 2008 in East Africa. Herbivore samples include teeth, tusks, soft tissue, hair, and horn. Tissues formed after 1955 are dated to within 0.3–1.3 y of formation, depending on the tissue type, whereas tissues older than ca. 1955 have high age uncertainties (>17 y) due to the Suess effect. 14C dating of tissues has applications to stable isotope (paleo)ecology and wildlife forensics. We use data from 41 additional samples to determine growth rates of tusks, molars, and hair, which improve interpretations of serial stable isotope data for (paleo)ecological studies. 14C dating can also be used to calculate the time interval represented in periodic histological structures in dental tissues (i.e., perikymata), which in turn may be used as chronometers in fossil teeth. Bomb-curve 14C dating of confiscated animal tissues (e.g., ivory statues) can be used to determine whether trade of the item is legal, because many Convention of International Trade of Endangered Species restrictions are based on the age of the tissue, and thus can serve as a powerful forensic tool to combat illegal trade in animal parts.

Ecological change in the lower Omo Valley around 2.8 Ma

Late Pliocene climate changes have long been implicated in environmental changes and mammalian evolution in Africa, but high-resolution examinations of the fossil and climatic records have been hampered by poor sampling. By using fossils from the well-dated Shungura Formation (lower Omo Valley, northern Turkana Basin, southern Ethiopia), we investigate palaeodietary changes in one bovid and in one suid lineage from 3 to 2 Ma using stable isotope analysis of tooth enamel. Results show unexpectedly large increases in C4 dietary intake around 2.8 Ma in both the bovid and suid, and possibly in a previously reported hippopotamid species. Enamel δ13C values after 2.8 Ma in the bovid (Tragelaphus nakuae) are higher than recorded for any living tragelaphin, and are not expected given its conservative dental morphology. A shift towards increased C4 feeding at 2.8 Ma in the suid (Kolpochoerus limnetes) appears similarly decoupled from a well-documented record of dental evolution indicating gradual and progressive dietary change. The fact that two, perhaps three, disparate Pliocene herbivore lineages exhibit similar, and contemporaneous changes in dietary behaviour suggests a common environmental driver. Local and regional pollen, palaeosol and faunal records indicate increased aridity but no corresponding large and rapid expansion of grasslands in the Turkana Basin at 2.8 Ma. Our results provide new evidence supporting ecological change in the eastern African record around 2.8 Ma, but raise questions about the resolution at which different ecological proxies may be comparable, the correlation of vegetation and faunal change, and the interpretation of low δ13C values in the African Pliocene.

Fossil mice and rats show isotopic evidence of niche partitioning and change in dental ecomorphology related to dietary shift in Late Miocene of Pakistan.

Stable carbon isotope analysis in tooth enamel is a well-established approach to infer C3 and C4 dietary composition in fossil mammals. The bulk of past work has been conducted on large herbivorous mammals. One important finding is that their dietary habits of fossil large mammals track the late Miocene ecological shift from C3 forest and woodland to C4 savannah. However, few studies on carbon isotopes of fossil small mammals exist due to limitations imposed by the size of rodent teeth, and the isotopic ecological and dietary behaviors of small mammals to climate change remain unknown. Here we evaluate the impact of ecological change on small mammals by fine-scale comparisons of carbon isotope ratios (δ13C) with dental morphology of murine rodents, spanning 13.8 to ∼2.0 Ma, across the C3 to C4 vegetation shift in the Miocene Siwalik sequence of Pakistan. We applied in-situ laser ablation GC-IRMS to lower first molars and measured two grazing indices on upper first molars. Murine rodents yield a distinct, but related, record of past ecological conditions from large herbivorous mammals, reflecting available foods in their much smaller home ranges. In general, larger murine species show more positive δ13C values and have higher grazing indices than smaller species inhabiting the same area at any given age. Two clades of murine rodents experienced different rates of morphological change. In the faster-evolving clade, the timing and trend of morphological innovations are closely tied to consumption of C4 diet during the vegetation shift. This study provides quantitative evidence of linkages among diet, niche partitioning, and dental morphology at a more detailed level than previously possible.

Neogene biomarker record of vegetation change in eastern Africa.

The evolution of C4 grassland ecosystems in eastern Africa has been intensely studied because of the potential influence of vegetation on mammalian evolution, including that of our own lineage, hominins. Although a handful of sparse vegetation records exists from middle and early Miocene terrestrial fossil sites, there is no comprehensive record of vegetation through the Neogene. Here we present a vegetation record spanning the Neogene and Quaternary Periods that documents the appearance and subsequent expansion of C4 grasslands in eastern Africa. Carbon isotope ratios from terrestrial plant wax biomarkers deposited in marine sediments indicate constant C3 vegetation from ∼24 Ma to 10 Ma, when C4 grasses first appeared. From this time forward, C4 vegetation increases monotonically to present, with a coherent signal between marine core sites located in the Somali Basin and the Red Sea. The response of mammalian herbivores to the appearance of C4 grasses at 10 Ma is immediate, as evidenced from existing records of mammalian diets from isotopic analyses of tooth enamel. The expansion of C4 vegetation in eastern Africa is broadly mirrored by increasing proportions of C4-based foods in hominin diets, beginning at 3.8 Ma in Australopithecus and, slightly later, Kenyanthropus. This continues into the late Pleistocene in Paranthropus, whereas Homo maintains a flexible diet. The biomarker vegetation record suggests the increase in open, C4 grassland ecosystems over the last 10 Ma may have operated as a selection pressure for traits and behaviors in Homo such as bipedalism, flexible diets, and complex social structure.

Radiocarbon dating of seized ivory confirms rapid decline in African elephant populations and provides insight into illegal trade

Significance C-14 dating methods can be used to determine the time of death of wildlife products. We evaluate poaching patterns of elephants in Africa by using 14C to determine lag time between elephant death and recovery of ivory by law enforcement officials. Most ivory in recent seizures has lag times of less than 3 y. Lag times for ivory originating in East Africa are shorter, on average, than the lag times for ivory originating in the Tridom region (Cameroon–Gabon–Congo). The 14C data show little or no evidence that large-scale ivory shipments contained ivory stockpiled over long time periods. Little, if any, “old” ivory (i.e., >10 y) seems to contribute to large ivory shipments. Carbon-14 measurements on 231 elephant ivory specimens from 14 large ivory seizures (≥0.5 ton) made between 2002 and 2014 show that most ivory (ca. 90%) was derived from animals that had died less than 3 y before ivory was confiscated. This indicates that the assumption of recent elephant death for mortality estimates of African elephants is correct: Very little “old” ivory is included in large ivory shipments from Africa. We found only one specimen of the 231 analyzed to have a lag time longer than 6 y. Patterns of trade differ by regions: East African ivory, based on genetic assignments of geographic origin, has a much higher fraction of “rapid” transit than ivory originating in the Tridom region of Cameroon–Gabon–Congo. Carbon-14 is an important tool in understanding patterns of movement of illegal wildlife products.

A Pleistocene palaeovegetation record from plant wax biomarkers from the Nachukui Formation, West Turkana, Kenya

Reconstructing vegetation at hominin fossil sites provides us critical information about hominin palaeoenvironments and the potential role of climate in their evolution. Here we reconstruct vegetation from carbon isotopes of plant wax biomarkers in sediments of the Nachukui Formation in the Turkana Basin. Plant wax biomarkers were extracted from samples from a wide range of lithologies that include fluvial–lacustrine sediments and palaeosols, and therefore provide a record of vegetation from diverse depositional environments. Carbon isotope ratios from biomarkers indicate a highly dynamic vegetation structure (ca 5–100% C4 vegetation) from 2.3 to 1.7 Ma, with an overall shift towards more C4 vegetation on the landscape after about 2.1 Ma. The biomarker isotope data indicate ca 25–30% more C4 vegetation on the landscape than carbon isotope data of pedogenic carbonates from the same sequence. Our data show that the environments of early Paranthropus and Homo in this part of the Turkana Basin were primarily mixed C3–C4 to C4-dominated ecosystems. The proportion of C4-based foods in the diet of Paranthropus increases through time, broadly paralleling the increase in C4 vegetation on the landscape, whereas the diet of Homo remains unchanged. Biomarker isotope data associated with the Kokiselei archaeological site complex, which includes the site where the oldest Acheulean stone tools to date were recovered, indicate 61–97% C4 vegetation on the landscape. This article is part of the themed issue ‘Major transitions in human evolution’.