Toward a Cenozoic history of atmospheric CO2.

The geological record encodes the relationship between climate and atmospheric carbon dioxide (CO2) over long and short timescales, as well as potential drivers of evolutionary transitions. However, reconstructing CO2 beyond direct measurements requires the use of paleoproxies and herein lies the challenge, as proxies differ in their assumptions, degree of understanding, and even reconstructed values. In this study, we critically evaluated, categorized, and integrated available proxies to create a high-fidelity and transparently constructed atmospheric CO2 record spanning the past 66 million years. This newly constructed record provides clearer evidence for higher Earth system sensitivity in the past and for the role of CO2 thresholds in biological and cryosphere evolution.

Pliocene hominins from East Turkana were associated with mesic environments in a semiarid basin.

During the middle Pliocene (∼3.8-3.2 Ma), both Australopithecus afarensis and Kenyanthropus platyops are known from the Turkana Basin, but between 3.60 and 3.44 Ma, most hominin fossils are found on the west side of Lake Turkana. Here, we describe a new hominin locality (ET03-166/168, Area 129) from the east side of the lake, in the Lokochot Member of the Koobi Fora Formation (3.60-3.44 Ma). To reconstruct the paleoecology of the locality and its surroundings, we combine information from sedimentology, the relative abundance of associated mammalian fauna, phytoliths, and stable isotopes from plant wax biomarkers, pedogenic carbonates, and fossil tooth enamel. The combined evidence provides a detailed view of the local paleoenvironment occupied by these Pliocene hominins, where a biodiverse community of primates, including hominins, and other mammals inhabited humid, grassy woodlands in a fluvial floodplain setting. Between <3.596 and 3.44 Ma, increases in woody vegetation were, at times, associated with increases in arid-adapted grasses. This suggests that Pliocene vegetation included woody species that were resilient to periods of prolonged aridity, resembling vegetation structure in the Turkana Basin today, where arid-adapted woody plants are a significant component of the ecosystem. Pedogenic carbonates indicate more woody vegetation than other vegetation proxies, possibly due to differences in temporospatial scale and ecological biases in preservation that should be accounted for in future studies. These new hominin fossils and associated multiproxy paleoenvironmental indicators from a single locale through time suggest that early hominin species occupied a wide range of habitats, possibly including wetlands within semiarid landscapes. Local-scale paleoecological evidence from East Turkana supports regional evidence that middle Pliocene eastern Africa may have experienced large-scale, climate-driven periods of aridity. This information extends our understanding of hominin environments beyond the limits of simple wooded, grassy, or mosaic environmental descriptions.

Oldest evidence of abundant C4 grasses and habitat heterogeneity in eastern Africa.

The assembly of Africa's iconic C4 grassland ecosystems is central to evolutionary interpretations of many mammal lineages, including hominins. C4 grasses are thought to have become ecologically dominant in Africa only after 10 million years ago (Ma). However, paleobotanical records older than 10 Ma are sparse, limiting assessment of the timing and nature of C4 biomass expansion. This study uses a multiproxy design to document vegetation structure from nine Early Miocene mammal site complexes across eastern Africa. Results demonstrate that between ~21 and 16 Ma, C4 grasses were locally abundant, contributing to heterogeneous habitats ranging from forests to wooded grasslands. These data push back the oldest evidence of C4 grass-dominated habitats in Africa-and globally-by more than 10 million years, calling for revised paleoecological interpretations of mammalian evolution.

The evolution of hominoid locomotor versatility: Evidence from Moroto, a 21 Ma site in Uganda.

Living hominoids are distinguished by upright torsos and versatile locomotion. It is hypothesized that these features evolved for feeding on fruit from terminal branches in forests. To investigate the evolutionary context of hominoid adaptive origins, we analyzed multiple paleoenvironmental proxies in conjunction with hominoid fossils from the Moroto II site in Uganda. The data indicate seasonally dry woodlands with the earliest evidence of abundant C4 grasses in Africa based on a confirmed age of 21 million years ago (Ma). We demonstrate that the leaf-eating hominoid Morotopithecus consumed water-stressed vegetation, and postcrania from the site indicate ape-like locomotor adaptations. These findings suggest that the origin of hominoid locomotor versatility is associated with foraging on leaves in heterogeneous, open woodlands rather than forests.

Eastern African environmental variation and its role in the evolution and cultural change of Homo over the last 1 million years.

Characterizing eastern African environmental variability on orbital timescales is crucial to evaluating the hominin evolutionary response to past climate changes. However, there is a dearth of high-resolution, well-dated records of ecosystem dynamics from eastern Africa that cover long time intervals. In the last 1 Myr, there were significant anatomical and cultural developments in Homo, including the origin of Homo sapiens. There were also major changes in global climatic boundary conditions that may have affected eastern African environments, yet potential linkages remain poorly understood. We developed carbon isotopic records from plant waxes (δ13Cwax) and bulk organic matter (δ13COM) from a well-dated sediment core spanning the last ∼1 Myr extracted from the Koora Basin, located south of the Olorgesailie Basin, in the southern Kenya rift. Our record characterizes the climatic and environmental context for evolutionary events and technological advances recorded in the adjacent Olorgesailie Basin, such as the transition from Acheulean to Middle Stone Age tools by 320 ka. A significant shift toward more C4-dominated ecosystems and arid conditions occurred near the end of the mid-Pleistocene Transition, which indicates a link between equatorial eastern African and high-latitude northern hemisphere climate. Environmental variability increases throughout the mid- to late-Pleistocene, superimposed by precession-paced packets of variability modulated by eccentricity. An interval of particularly high-amplitude climate and environmental variability occurred from ∼275 ka to ∼180 ka, synchronous with evidence for the first H. sapiens fossils in eastern Africa. These results support the 'variability selection hypothesis' that increased environmental variability selected for adaptable traits, behaviors, and technology in our hominin ancestors.

New hominin remains and revised context from the earliest Homo erectus locality in East Turkana, Kenya.

The KNM-ER 2598 occipital is among the oldest fossils attributed to Homo erectus but questions have been raised about whether it may derive from a younger horizon. Here we report on efforts to relocate the KNM-ER 2598 locality and investigate its paleontological and geological context. Although located in a different East Turkana collection area (Area 13) than initially reported, the locality is stratigraphically positioned below the KBS Tuff and the outcrops show no evidence of deflation of a younger unit, supporting an age of >1.855 Ma. Newly recovered faunal material consists primarily of C4 grazers, further confirmed by enamel isotope data. A hominin proximal 3rd metatarsal and partial ilium were discovered <50 m from the reconstructed location where KNM-ER 2598 was originally found but these cannot be associated directly with the occipital. The postcrania are consistent with fossil Homo and may represent the earliest postcrania attributable to Homo erectus.

Large mammal diets and paleoecology across the Oldowan-Acheulean transition at Olduvai Gorge, Tanzania from stable isotope and tooth wear analyses.

The well-dated Pleistocene sediments at Olduvai Gorge have yielded a rich record of hominin fossils, stone tools, and vertebrate faunal remains that, taken together, provide insight to hominin behavior and paleoecology. Since 2008, the Olduvai Geochronology and Archaeology Project (OGAP) has undertaken extensive excavations in Bed II that have yielded a large collection of early Pleistocene stone tools and fossils. The strata of Lower, Middle and Upper Bed II at Olduvai Gorge capture the critical transition from Oldowan to Acheulean technology and therefore provide an opportunity to explore the possible role of biotic and abiotic change during the transition. Here, we analyze newly discovered and existing fossil teeth from Bed II sites using stable isotope and tooth wear methods to investigate the diets of large mammals. We reconstruct the dietary ecology of Bed II mammals and evaluate whether vegetation or hydroclimate shifts are associated with the technological change. Combined isotope and tooth wear data suggest most mammals were C4 grazers or mixed feeders. Carbon isotope data from bulk enamel samples indicate that a large majority of Bed II large mammals analyzed had diets comprising mostly C4 vegetation (>75% of diet), whereas only a small number of individuals had either mixed C3-C4 or mostly C3 diets (<25% C4). Mesowear generally indicates an increase of the abrasiveness of the diet between intervals IIA and IIB (∼1.66 Ma), probably reflecting increased grazing. Microwear indicates more abrasive diets in interval IIA suggesting stronger seasonal differences at the time of death during this interval. This is also supported by the intratooth isotope profiles from Equus oldowayensis molars, which suggest a possible decrease in seasonality across the transition. Neither stable isotope nor tooth wear analyses indicate major vegetation or hydrological change across the Oldowan-Acheulean transition.

Dietary traits of the ungulates from the HWK EE site at Olduvai Gorge (Tanzania): Diachronic changes and seasonality.

The Oldowan site HWK EE (Olduvai Gorge, Tanzania) has yielded a large fossil and stone tool assemblage at the transition from Lower to Middle Bed II, ∼1.7 Ma. Integrated tooth wear and stable isotope analyses were performed on the three most abundant ungulate taxa from HWK EE, namely Alcelaphini, cf. Antidorcas recki (Antilopini) and Equus oldowayensis (Equini), to infer dietary traits in each taxon. Some paleodietary changes were observed for cf. A. recki and E. oldowayensis based on tooth wear at the transition from the Lemuta to the Lower Augitic Sandstone (LAS) interval within the HWK EE sequence. Stable carbon and oxygen isotope data show no significant changes in bulk diet or hydroclimate between the Lemuta and LAS intervals. The combined tooth wear and stable isotope data suggest similar paleoecological conditions across the two HWK EE intervals, but that differences in vegetation consumed among ungulates may have resulted in changes in dietary niches. Integrating tooth wear and stable isotope analyses permits the characterization of ungulate diets and habitats at HWK EE where C4 dominated and minor mixed C3 and C4 habitats were present. Our results provide a better understanding of the paleoenvironmental conditions of the Lemuta and LAS intervals. The LAS assemblage was mostly accumulated during relatively dry periods at Olduvai Gorge when grasses were not as readily available and grazing animals may have been more nutritionally-stressed than during the formation of the Lemuta assemblage. This helps to contextualize variations in hominin and carnivore feeding behavior observed from the faunal assemblages produced during the two main occupations of the site.

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

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.

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.

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'.

Carbon isotope ratios of human tooth enamel record the evidence of terrestrial resource consumption during the Jomon period, Japan.

OBJECTIVE: Archaeological remains strongly suggest that the Holocene Japanese hunter-gatherers, the Jomon people, utilized terrestrial plants as their primary food source. However, carbon and nitrogen isotope analysis of bone collagen indicates that they primarily exploited marine resources. We hypothesize that this inconsistency stems from the route of protein synthesis and the different proportions of protein-derived carbon in tooth enamel versus bone collagen. Carbon isotope ratios from bone collagen reflect that of dietary protein and may provide a biased signal of diet, whereas isotope ratios from tooth enamel reflect the integrated diet from all macronutrients (carbohydrates, lipids, and proteins). METHODS: In order to evaluate the differences in inferred diet between the archaeological evidence and bone collagen isotope data, this study investigated carbon isotopes in Jomon tooth enamel from four coastal sites of the Middle to Late-Final Jomon period (5,000-2,300 years BP). RESULTS: Carbon isotope ratios of human teeth are as depleted as coeval terrestrial mammals, suggesting that C3 plants and terrestrial mammals were major dietary resources for the Jomon people. Dietary dependence on marine resources calculated from enamel was significantly lower than that calculated from bone collagen. The discrepancy in isotopic ratios between enamel and collagen and the nitrogen isotope ratio in collagen shows a negative correlation on individual and population levels, suggesting diets with variable proportions of terrestrial and marine resources. CONCLUSION: This study highlights the usefulness of coupling tooth enamel and bone collagen in carbon isotopic studies to reconstruct prehistoric human diet. Am J Phys Anthropol 158:300-311, 2015. © 2015 Wiley Periodicals, Inc.

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

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.

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 (δ(13)C) 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 δ(13)C 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.

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 ((14)C) 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 (14)C 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. (14)C 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. (14)C 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 (14)C 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.

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.

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 C(4) biomass such as grasses or sedges. Its diet included more C(4) 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.

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

Stable isotope and molecular data suggest that C(4) 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 C(3) to mixed C(3)/C(4) or C(4) 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 C(4) 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 C(4) grasslands in this part of the Late Miocene. Bovids and hippopotamids followed suit with individuals that had C(4)-dominated (>65%) diets by 7.4 Ma. Suids adopted C(4)-dominated diets between 6.5 and 4.2 Ma. Gomphotheriids and elephantids had mostly C(3)-dominated diets through 9.3 Ma, but became dedicated C(4) grazers by 6.5 Ma. Deinotheriids and giraffids maintained a predominantly C(3) 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.