Linking African herbivore community enamel isotopes and environments: challenges, opportunities, and paleoecological implications.

Paleoenvironmental reconstructions of fossil sites based on isotopic analyses of enamel typically rely on data from multiple herbivore taxa, with the assumption that this dietary spectrum represents the community's isotopic range and provides insights into local or regional vegetation patterns. However, it remains unclear how representative the sampled taxa are of the broader herbivore community and how well these data correspond to specific ecosystems. Verifying these underlying assumptions is essential to refining the utility of enamel isotopic values for paleoenvironmental reconstructions. This study explores potential links between modern herbivore community carbon isotopic enamel spectra, biome types, and climate in sub-Saharan Africa. This region is one of the most comprehensively isotopically sampled areas globally and is of particular relevance to hominin evolution. Our extensive data compilation reveals that published enamel isotopic data from sub-Saharan Africa typically sample only a small percentage of the taxa documented at most localities and that some biome types (e.g., subtropical savannas) are dramatically overrepresented relative to others (e.g., forests) in these modern data sets. Multiple statistical analyses, including linear models and cluster analyses, revealed weak relationships of associated mammalian herbivore enamel isotopic values, biome type, and climate parameters. These results confound any simple assumptions about how community isotopic profiles map onto specific environments, highlighting the need for more precise strategic approaches in extending isotopic frameworks into the past for paleoecological reconstructions. Developing more refined modern analogs will ultimately allow us to more accurately characterize the isotopic spectra of paleo-communities and link isotopic dietary signatures to specific ecosystems.

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.

Plio-Pleistocene environmental variability in Africa and its implications for mammalian evolution.

Understanding the climatic drivers of environmental variability (EV) during the Plio-Pleistocene and EV's influence on mammalian macroevolution are two outstanding foci of research in African paleoclimatology and evolutionary biology. The potential effects of EV are especially relevant for testing the variability selection hypothesis, which predicts a positive relationship between EV and speciation and extinction rates in fossil mammals. Addressing these questions is stymied, however, by 1) a lack of multiple comparable EV records of sufficient temporal resolution and duration, and 2) the incompleteness of the mammalian fossil record. Here, we first compile a composite history of Pan-African EV spanning the Plio-Pleistocene, which allows us to explore which climatic variables influenced EV. We find that EV exhibits 1) a long-term trend of increasing variability since ∼3.7 Ma, coincident with rising variability in global ice volume and sea surface temperatures around Africa, and 2) a 400-ky frequency correlated with seasonal insolation variability. We then estimate speciation and extinction rates for fossil mammals from eastern Africa using a method that accounts for sampling variation. We find no statistically significant relationship between EV and estimated speciation or extinction rates across multiple spatial scales. These findings are inconsistent with the variability selection hypothesis as applied to macroevolutionary processes.

A chimpanzee enamel-diet δ13C enrichment factor and a refined enamel sampling strategy: Implications for dietary reconstructions.

Reconstructing diets from stable carbon isotopic signals in enamel bioapatite requires the application of a δ13C enamel-diet enrichment factor, or the isotopic offset between diet and enamel, which has not been empirically determined for any primate. In this study, an enamel-diet enrichment factor (ε∗enamel-diet) of 11.8 ± 0.3‰ is calculated for chimpanzees (Pan troglodytes) at Ngogo in Kibale National Park, Uganda, based on a comprehensive isotopic assessment of previously analyzed dietary plant data and new isotopic analyses of enamel apatite. Different enamel sampling methods are evaluated to determine the potential influence of weaning on isotopic enamel values and dietary interpretations. The new chimpanzee enrichment factor and a sampling strategy that excludes teeth that formed before weaning completion are applied to all known chimpanzee δ13Cenamel data, either previously published or newly derived in this study, resulting in a dietary range of almost 6‰ across all chimpanzees sampled. This new chimpanzee enamel-diet enrichment factor is then used to reassess dietary reconstructions of 12 fossil hominin species whose isotopic enamel signatures have been determined. Results reveal hominin diets that are isotopically more positive than previously reconstructed, highlighting the widespread contribution of 13C-enriched C4/crassulacean acid metabolism (CAM) resources in fossil hominin diets and emphasizing the broad use of these resources during human evolution. These findings stress the importance of ascertaining and employing an appropriate enrichment factor for dietary reconstructions of specific taxa as well as standardizing the sampling protocol for tooth enamel in isotopic paleodietary reconstructions.

Chimpanzee isotopic ecology: a closed canopy C3 template for hominin dietary reconstruction.

The most significant hominin adaptations, including features used to distinguish and/or classify taxa, are critically tied to the dietary environment. Stable isotopic analyses of tooth enamel from hominin fossils have provided intriguing evidence for significant C4/CAM (crassulacean acid metabolism) resource consumption in a number of Plio-Pleistocene hominin taxa. Relating isotopic tooth signatures to specific dietary items or proportions of C3 versus C4/CAM plants, however, remains difficult as there is an ongoing need to document and quantify isotopic variability in modern ecosystems. This study investigates the ecological variables responsible for carbon isotopic discrimination and variability within the C3-dominated dietary niche of a closed canopy East African hominoid, Pan troglodytes, from Ngogo, Kibale National Park, Uganda. δ(13)C values among C3 resources utilized by Ngogo chimpanzees were highly variable, ranging over 13‰. Infrequent foraging on papyrus (the only C4 plant consumed by chimpanzees at the site) further extended this isotopic range. Variation was ultimately most attributable to mode of photosynthesis (C3 versus C4), food type, and elevation, which together accounted for approximately 78% of the total sample variation. Among C3 food types, bulk carbon values ranged from -24.2‰ to -31.1‰ with intra-plant variability up to 12.1‰. Pith and sapling leaves were statistically more (13)C depleted than pulp, seeds, flowers, cambium, roots, leaf buds, and leaves from mature trees. The effect of elevation on carbon variation was highly significant and equivalent to an approximately 1‰ increase in δ(13)C for every 150 m of elevation gain, likely reflecting habitat variability associated with topography. These results indicate significant δ(13)C variation attributable to food type and elevation among C3 resources and provide important data for hominin dietary interpretations based on carbon isotopic analyses.

The origin and antiquity of syphilis revisited: an appraisal of Old World pre-Columbian evidence for treponemal infection.

For nearly 500 years, scholars have argued about the origin and antiquity of syphilis. Did Columbus bring the disease from the New World to the Old World? Or did syphilis exist in the Old World before 1493? Here, we evaluate all 54 published reports of pre-Columbian, Old World treponemal disease using a standardized, systematic approach. The certainty of diagnosis and dating of each case is considered, and novel information pertinent to the dating of these cases, including radiocarbon dates, is presented. Among the reports, we did not find a single case of Old World treponemal disease that has both a certain diagnosis and a secure pre-Columbian date. We also demonstrate that many of the reports use nonspecific indicators to diagnose treponemal disease, do not provide adequate information about the methods used to date specimens, and do not include high-quality photographs of the lesions of interest. Thus, despite an increasing number of published reports of pre-Columbian treponemal infection, it appears that solid evidence supporting an Old World origin for the disease remains absent.

Partial skeleton of Theropithecus brumpti (Primates, Cercopithecidae) from the Chemeron Formation of the Tugen Hills, Kenya.

Here we describe a complete skull and partial skeleton of a large cercopithecoid monkey (KNM-TH 46700) discovered in the Chemeron Formation of the Tugen Hills at BPRP Site #152 (2.63 Ma). Associated with the skeleton was a mandible of an infant cercopithecoid (KNM-TH 48364), also described here. KNM-TH 46700 represents an aged adult female of Theropithecus brumpti, a successful Pliocene papionin taxon better known from the Omo Shungura Formation in Ethiopia and sites east and west of Lake Turkana, Kenya. While the morphology of male T. brumpti is well-documented, including a partial skeleton with both cranial and postcranial material, the female T. brumpti morphotype is not well-known. This skeleton represents some of the first associated evidence of cranial and postcranial female T. brumpti remains. In addition to the complete skull, postcranial material includes elements of the axial skeleton and lower limb. While aspects of the skeleton conform to those of specimens previously assigned to T. brumpti, other features on the femur and tibia appear to differ from those previously described for this species. It is unclear whether these differences represent general variation within the T. brumpti population, variation between the sexes in T. brumpti, or the incorrect assignment of previous isolated hindlimb specimens. In total, the observable morphological features of the hindlimb suggest that KNM-TH 46700 was a terrestrial quadruped similar to modern savannah baboons (Papio). From the available evidence, it is difficult to assess whether or not KNM-TH 46700 frequently engaged in the specialized squatting and shuffling behavior observed in extant geladas (Theropithecus gelada).

Comment on the paleoenvironment of Ardipithecus ramidus.

White and colleagues (Research Articles, 2 October 2009, pp. 65-67 and www.sciencemag.org/ardipithecus) characterized the paleoenvironment of Ardipithecus ramidus at Aramis, Ethiopia, which they described as containing habitats ranging from woodland to forest patches. In contrast, we find the environmental context of Ar. ramidus at Aramis to be represented by what is commonly referred to as tree- or bush-savanna, with 25% or less woody canopy cover.

Oldest evidence of tool making hominins in a grassland-dominated ecosystem.

BACKGROUND: Major biological and cultural innovations in late Pliocene hominin evolution are frequently linked to the spread or fluctuating presence of C(4) grass in African ecosystems. Whereas the deep sea record of global climatic change provides indirect evidence for an increase in C(4) vegetation with a shift towards a cooler, drier and more variable global climatic regime beginning approximately 3 million years ago (Ma), evidence for grassland-dominated ecosystems in continental Africa and hominin activities within such ecosystems have been lacking. METHODOLOGY/PRINCIPAL FINDINGS: We report stable isotopic analyses of pedogenic carbonates and ungulate enamel, as well as faunal data from approximately 2.0 Ma archeological occurrences at Kanjera South, Kenya. These document repeated hominin activities within a grassland-dominated ecosystem. CONCLUSIONS/SIGNIFICANCE: These data demonstrate what hitherto had been speculated based on indirect evidence: that grassland-dominated ecosystems did in fact exist during the Plio-Pleistocene, and that early Homo was active in open settings. Comparison with other Oldowan occurrences indicates that by 2.0 Ma hominins, almost certainly of the genus Homo, used a broad spectrum of habitats in East Africa, from open grassland to riparian forest. This strongly contrasts with the habitat usage of Australopithecus, and may signal an important shift in hominin landscape usage.

Shifting adaptive landscapes: progress and challenges in reconstructing early hominid environments.

Since Darwin situated humans in an evolutionary framework, much discussion has focused on environmental factors that may have shaped or influenced the course of human evolution. Developing adaptive or causal perspectives on the morphological and behavioral variability documented in the human fossil record requires establishing a comprehensive paleoenvironmental context. Reconstructing environments in the past, however, is a complex undertaking, requiring assimilation of diverse datasets of varying quality, scale, and relevance. In response to these difficulties, human evolution has traditionally been interpreted in a somewhat generalized framework, characterized primarily by increasing aridity and seasonality periodically punctuated by pulses or intervals of environmental change, inferred largely from global climatic records. Although these broad paradigms provide useful heuristic approaches for interpreting human evolution, the spatiotemporal resolution remains far too coarse to develop unambiguous causal links. This challenge has become more acute as the emerging paleoenvironmental evidence from equatorial Africa is revealing a complex pattern of habitat heterogeneity and persistent ecological flux throughout the interval of human evolution. In addition, recent discoveries have revealed significant taxonomic diversity and substantially increased the geographic and temporal range of early hominids. These findings raise further questions regarding the role of the environment in mediating or directing the course of human evolution. As a consequence, it is imperative to critically assess the environmental criteria on which many theories and hypotheses of human evolution hinge. The goals here are to 1) compile, review, and evaluate relevant paleoecological datasets from equatorial Africa spanning the last 10 Ma, 2) develop a hierarchical perspective for developing and evaluating hypotheses linking paleoecology to patterns and processes in early hominid evolution, and 3) suggest a conceptual framework for modeling and interpreting environmental data relevant to human evolution in equatorial Africa.

Astronomically forced climate change in the Kenyan Rift Valley 2.7-2.55 Ma: implications for the evolution of early hominin ecosystems.

Global climate change, linked to astronomical forcing factors, has been implicated in faunal evolutionary change in equatorial Africa, including the origin and diversification of hominin lineages. Empirical terrestrial data demonstrating that orbital forcing has a significant effect, or is detectable, at early hominin sites in equatorial continental interiors during the Pliocene, however, remain limited. Sedimentation patterns in the Baringo Basin within the Central Kenyan Rift Valley between ca. 2.7 and 2.55 Ma, controlled by climatic factors, provide a detailed paleoenvironmental record spanning 35 fossil vertebrate localities, including three hominin sites. The succession includes a sequence of diatomites that record rhythmic cycling of major freshwater lake systems consistent with approximately 23-kyr Milankovitch precessional periodicity. The temporal framework of shifting precipitation patterns, relative to Pliocene insolation curves, implicate African monsoonal climatic control and indicate that climatic fluctuations in Rift Valley ecosystems were paced by global climatic change documented in marine cores. These data provide direct evidence of orbitally mediated environmental change at Pliocene Rift Valley hominin fossil localities, providing a unique opportunity to assess the evolutionary effect of short-term climatic flux on late Pliocene East African terrestrial communities.

Docosahexaenoic acid biosynthesis and dietary contingency: Encephalization without aquatic constraint.

Reconstructing evolutionary processes in the distant past is necessarily an inductive endeavor, typically appealing to numerous considerations thought to be relevant to the veracity of a particular conclusion. In this respect, it is essential that the considerations invoked to support hypotheses are in turn well-established truths. It is with these concerns that we sought to examine the nutritional, physiological, and archeological premises underlying the perspective that access to an aquatic diet rich in docosahexaenoic acid (DHA, 22:6n-3) was critical to human brain evolution (Carlson and Kingston [2007]: Am J Hum Biol 19:132-141). In our report investigating links between omega-3 (n-3) fatty acids and hominin encephalization, we concluded that the regular consumption of aquatic resources rich in preformed DHA may not have been essential given a varied diet of wild terrestrial foods (Carlson and Kingston [2007]). This assessment was based primarily on evidence of potential physiological adaptations in modern humans to ensure sufficient availability of DHA during critical periods of brain growth. While modern human physiology provides critical information regarding DHA as a constraint in evolving a large brain, it is also important to consistently contextualize interpretations within a framework of eclectic foraging diets rather than nutritionally limited modern agricultural populations or even modern foragers. We contend that current interpretations of Pleistocene hominin nutritional ecology do not uniquely support a shore-based foraging niche as claimed by Cunnane et al. ([2007]: Am J Hum Biol, 19:578-581). Specific issues raised in response to our article by Cunnane et al. and Joordens et al. ([2007]: Am J Hum Biol, 19:582-584) are addressed here.

Docosahexaenoic acid, the aquatic diet, and hominin encephalization: difficulties in establishing evolutionary links.

Distinctive characteristics of modern humans, including language, tool manufacture and use, culture, and behavioral plasticity, are linked to changes in the organization and size of the brain during hominin evolution. As brain tissue is metabolically and nutritionally costly to develop and maintain, early hominin encephalization has been linked to a release of energetic and nutritional constraints. One such nutrient-based approach has focused on the n-3 long-chained polyunsaturated fatty acid docosahexaenoic acid (DHA), which is a primary constituent of membrane phospholipids within the synaptic networks of the brain essential for optimal cognitive functioning. As biosynthesis of DHA from n-3 dietary precursors (alpha-linolenic acid, LNA) is relatively inefficient, it has been suggested that preformed DHA must have been an integral dietary constituent during evolution of the genus Homo to facilitate the growth and development of an encephalizing brain. Furthermore, preformed DHA has only been identified to an appreciable extent within aquatic resources (marine and freshwater), leading to speculation that hominin encephalization is linked specifically to access and consumption of aquatic resources. The key premise of this perspective is that biosynthesis of DHA from LNA is not only inefficient but also insufficient for the growth and maturation demands of an encephalized brain. However, this assumption is not well-supported, and much evidence instead suggests that consumption of LNA, available in a wider variety of sources within a number of terrestrial ecosystems, is sufficient for normal brain development and maintenance in modern humans and presumably our ancestors.

Geology and geochronology of the middle Miocene Kipsaramon site complex, Muruyur Beds, Tugen Hills, Kenya.

The Muruyur Beds are a substantial sedimentary deposit within a middle Miocene sequence of mafic volcanic flows associated with early stages of rifting in the central Kenyan Rift Valley. They are best represented in the Muruyur region, near Bartabwa, north of Kipsaramon, where dates range from 16.0 to 13.4 Ma. At Kipsaramon, located about 10 km south of Muruyur along the crest of the Tugen Hills, the upper Muruyur Beds are absent and the lower part can be divided into three members. Important fossil sites within Member 1 are dated between 15.8 and 15.6 Ma, and within Member 3 between 15.6 and 15.4 Ma. BPRP#89, in Member 1, is a bonebed at least 2500 m(2)in areal extent and up to 30 cm thick, which constitutes one of the richest concentrations of in situ fossil vertebrate bones in eastern Africa. BPRP#91, at approximately the same level at BPRP#89, is the source of a hominoid talus and other mammal and bird fossils. In Member 3, BPRP#122 has produced specimens of at least five individuals of the hominoid Equatorius, including a partial skeleton. The Muyuyur Beds were deposited near the western margin of a lake that was formed during the early stages of faulting and volcanism in the African Rift system. The bonebed in Member 1 appears to represent the influx of fluvially transported vertebrate and plant remains into a shallow portion of the lake. Elements of the fauna as well as stable isotopes that indicate both forest and more open environments occurred in proximity to the lake during the time of deposition of Member 1.

New cercopithecoids and a hominoid from 12.5 Ma in the Tugen Hills succession, Kenya.

The early evolutionary history of the cercopithecoids is poorly understood, primarily due to a lack of fossil material from between 15 and about 9 Ma. Cercopithecoid primate specimens from a fossil site in the Ngorora Formation of the Tugen Hills, Kenya, belong to the genus Victoriapithecus, possibly a new species. These fossils are associated with a hominoid specimen that resembles Proconsul, and another tooth of a catarrhine, also probably hominoid. The locality is BPRP#38, in the Kabasero type section of the Ngorora Formation, and well dated at 12.5 Ma. If the hominoid specimen is confirmed as Proconsul, it would be one of the most recent recorded. The relatively diverse mammal fauna from the site in some ways resembles that of Fort Ternan. The site is underlain, and not far removed in time, from one of the best fossil macro-floras in Africa, which indicates lowland rainforest conditions in this portion of the Rift Valley at 12.6 Ma.

Stratigraphy, age and environments of the late Miocene Mpesida Beds, Tugen Hills, Kenya.

Interpretations of faunal assemblages from the late Miocene Mpesida Beds in the Tugen Hills of the Central Kenyan Rift Valley have figured prominently in discussions of faunal turnover and establishment of the modern East African communities. These faunal changes have important implications for the divergence of the human lineage from the African apes ca. 8-5 Ma. While fossil material recovered from the Mpesida Beds has traditionally been analyzed collectively, accumulating evidence indicates that Mpesida facies span the 7-6 Ma interval and are scattered more than 25 km along the eastern flanks of the Tugen Hills. Stratigraphic distinctions between Mpesida facies and younger sediments in the sequence, such as the Lukeino Formation, are not yet fully resolved, further complicating temporal assessments and stratigraphic context of Mpesida facies. These issues are discussed with specific reference to exposures of Mpesida facies at Rurmoch, where large fossil tree fragments were swept up in an ancient ash flow. Preserved anatomical features of the fossil wood as well as estimated tree heights suggest a wet, lowland rainforest in this portion of the rift valley. Stable isotopic analyses of fossil enamel and paleosol components indicate the presence of more open habitats locally. Overlying air-fall tuffs and epiclastic debris, possibly associated with the ash flow, have yielded an assemblage of vertebrate fossils including two teeth belonging to one of the earliest colombines of typical body size known from Africa, after the rather small Microcolobus. Single-crystal, laser-fusion,(40)Ar/(39)Ar dates from a capping trachyte flow as well as tuffs just below the lava contact indicate an age of greater than 6.37 Ma for the fossil material.