Late Miocene to Pliocene carbon isotope record of differential diet change among East African herbivores Kevin T. Unoa,1, Thure E. Cerlinga,b, John M. Harrisc, Yutaka Kunimatsud, Meave G. Leakeye, Masato Nakatsukasad,f, and Hideo Nakayaf aDepartment of Geology and Geophysics, University of Utah, Salt Lake City, UT 84112; bDepartment of Biology, University of Utah, Salt Lake City, UT 84112; cGeorge C. Page Museum, Los Angeles, CA 90036; dLaboratory of Physical Anthropology, Kyoto University, Kyoto 606-8502, Japan; eTurkana Basin Institute, Stony Brook University, Stony Brook, NY 11790; and fDepartment of Earth and Environmental Sciences, Kagoshima University, Kagoshima 890-0065, Japan Edited by David Pilbeam, Harvard University, Cambridge, MA, and approved March 5, 2011 (received for review December 14, 2010) Stable isotope and molecular data suggest that C4 grasses first Lothagam (7). All carbon isotope data from pedogenic carbo- appeared globally in the Oligocene. In East Africa, stable isotope nates older than 9 Ma indicate C3 environments, with the ex- data from pedogenic carbonate and fossil tooth enamel suggest ception of the Tugen Hills (2). No pedogenic carbonates have a first appearance between 15–10 Ma and subsequent expansion been found in the Nakali Formation, and none have been sampled during the Plio-Pleistocene. The fossil enamel record has the po- from the Namurungule Formation in the Samburu Hills. The tential to provide detailed information about the rates of dietary earliest robust evidence for C4 vegetation from pedogenic car- adaptation to this new resource among different herbivore line- bonate is in the Lower Nawata Formation (7.4 Ma) at Lothagam, 13 ages. We present carbon isotope data from 452 fossil teeth that where the δ C values (−9.0 to −2.2‰) indicate C3 to mixed C3/C4 fi record differential rates of diet change from C3 to mixed C3/C4 or environments that included signi cant amounts of C4 grass (7). C4 diets among East African herbivore families at seven different Although isotope records from Late Miocene pedogenic carbo- time periods during the Late Miocene to the Pliocene (9.9–3.2 Ma). nates are rare, abundant records show that C4 grasses became Significant amounts of C4 grasses were present in equid diets be- widespread during the Late Pliocene to Pleistocene throughout ginning at 9.9 Ma and in rhinocerotid diets by 9.6 Ma, although East Africa (ref. 5 and references therein). 13 there is no isotopic evidence for expansive C4 grasslands in this Feakins et al. (4) analyzed the δ Cvaluesofn-alkanoic acids part of the Late Miocene. Bovids and hippopotamids followed suit in sediments from a Gulf of Aden core (Deep Sea Drilling with individuals that had C4-dominated (>65%) diets by 7.4 Ma. Project Site 231) that coincide with two time periods repre- Suids adopted C4-dominated diets between 6.5 and 4.2 Ma. Gom- sented in our record. The biomarker record shows input of photheriids and elephantids had mostly C3-dominated diets predominantly C3-derived leaf waxes at 9.4 Ma and 5–15% C4 through 9.3 Ma, but became dedicated C4 grazers by 6.5 Ma. Dein- vegetation from 3.8 to 3.2 Ma (4). The data from the Gulf of fi otheriids and giraf ds maintained a predominantly C3 diet Aden core record a noncontinuous, regional-scale signal that is throughout the record. The sequence of differential diet change well dated with high temporal resolution. Collectively, the fossil among herbivore lineages provides ecological insight into a key enamel, pedogenic carbonate, and biomarker records from period of hominid evolution and valuable information for future East Africa indicate C3-dominated ecosystems throughout the studies that focus on morphological changes associated with Middle and Late Miocene and an expansion of C4 grasses in the diet change. Late Pliocene and Pleistocene. However, none of these pre- viously published datasets provides a detailed record of the carbon isotopes | herbivore diet | bioapatite | paleodiet | mammal response of the fauna during this period. We use stable carbon isotope ratios from fossil tooth enamel table carbon isotope ratios from fossil tooth enamel, pedo- identified from family to species level (SI Appendix, Table S1) to Sgenic carbonates, and terrestrial plant biomarkers are com- evaluate rates of change in herbivore diets from the Late Mio- cene to the Early Pliocene from three fossil localities in East monly used to determine the relative amounts of C3 and C4 vegetation in ancient habitats (1–4). These paleovegetation Africa (Fig. 1). The sites range in age from 9.9 to 3.2 Ma; lith- proxies integrate over different spatial and temporal scales, and ostratigraphy, radiometric ages, and stratigraphic intervals where each proxy has inherent strengths and weaknesses when used samples were collected are shown in Fig. 2. The stable isotope data address two important issues in the East African fossil re- to reconstruct the relative amounts of C3 and C4 vegetation in ancient habitats (5, 6). cord. First, they illustrate the diverse paleoecological response of Carbon isotopes from fossil enamel of East African herbivores large herbivores to paleoenvironmental change associated with the appearance of C4 grasses during a key period of hominid indicate C3 diets and presumably, C3 environments, in the records from Buluk, Fort Ternan, and the Tugen Hills that range evolution. Paleoenvironmental context is integral to under- standing East African hominid emergence, radiation, and evo- in age from 17 to ∼9 Ma (7–9). An exception is carbon isotope lution from the Late Miocene onward. All sites in this study have data from four equid teeth from Chorora, Ethiopia, dated at yielded important hominid material. Nakali and the Samburu 10.7–10.1 Ma, which indicate a mixed C /C diet (10). Previously 3 4 Hills, located in the Suguta Valley, Kenya, have yielded the Late published isotope data on enamel from the Nakali, Namur- Miocene hominids Nakalipithecus nakayami (18) and Sambur- ungule, Nawata, and Nachukui formations (included and ex- upithecus kiptalami (19), respectively, which likely represent stem panded significantly here) indicate a shift toward C4-dominated EVOLUTION diets between 9.6 and 4.2 Ma (7). The previously published fossil 13 enamel δ C record from East Africa shows that herbivores in- Author contributions: K.T.U., T.E.C., J.M.H., Y.K., M.G.L., M.N., and H.N. designed corporated C4 vegetation into their diets as early as ∼10 Ma and research; K.T.U., T.E.C., J.M.H., Y.K., M.G.L., M.N., and H.N. performed research; K.T.U., is generally consistent with the Late Miocene (8–6 Ma) global T.E.C., J.M.H., and M.G.L. analyzed data; and K.T.U. wrote the paper. fl expansion of C4 vegetation documented in the Siwaliks, North The authors declare no con ict of interest. America, and South America (1, 11–14). This article is a PNAS Direct Submission. Early to early Late Miocene pedogenic carbonate records 1To whom correspondence should be addressed. E-mail: [email protected]. from fossil sites in East Africa include Rusinga Island (15), the This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. ANTHROPOLOGY Lothidok Hills (16), Fort Ternan (17), the Tugen Hills (2), and 1073/pnas.1018435108/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1018435108 PNAS | April 19, 2011 | vol. 108 | no. 16 | 6509–6514 Fig. 1. Map of northern Kenya showing the three fossil localities in the Suguta Valley and the Turkana Basin. hominines (23). With Chororapithecus abyssinicus, these are the only known East African hominids between 11 and 9 Ma (24). The third site, Lothagam, is located west of Lake Turkana in northern Kenya (Fig. 1). The Nawata and Nachukui formations at Lothagam have yielded hominid material dated at ∼5 and 3.5 Ma. The older specimens are attributed to Hominidae indet., whereas the younger specimens are likely Kenyanthropus platyops or, possibly, Australopithecus cf Au. afarensis (25) (SI Appendix, Table S2). Second, the stable isotope record of diet change will allow paleontologists to compare the timing and rate of diet change to morphological changes associated with the dietary shift toward C4 grazing in herbivore lineages. Examples of cra- niodental and postcranial ecomorphic characteristics influenced by the transition from browsing to grazing include tooth mor- phology (i.e., hypsodonty, enamel thickness, and size), jaw structure, and forelimb bone length (26, 27). Results and Discussion Carbon Isotope Data by Age. We use the terms “C3-dominated 13 diet” for δ C values < −8‰, “mixed C3/C4 diet” for −8‰ to −2‰, and “C4-dominated diet” for values > −2‰. These delineations are based on estimated paleoatmospheric δ13C values and an enrichment factor of 14.1‰ between diet and enamel (SI Appendix, Table S3) (28, 29). A Shapiro–Wilk test for normality demonstrates that the data are not distributed nor- mally (SI Appendix, Table S4). Thus, the median and range of 13 δ C values are more appropriate than the mean and SD for Fig. 2. Lithostratigraphy, magnetostratigraphy, and radiometric ages from describing central location and variance. Mann–Whitney U test Nakali, the Samburu Hills, and Lothagam. Geomagnetic Polarity Time Scale results indicate significant shifts (P < 0.05) in the median δ13C (GPTS) changes at the break between 9.0 and 8.0 Ma. The uppermost age value between successive age increments (i.e., 9.9–9.6 Ma) where from the Nakali Formation (10.10 ± 0.12 Ma) is from a pyroclastic flow and there are more than five isotope analyses within a family essentially synchronous with the two slightly younger ages below. Modified – (SI Appendix, Table S5). All isotopic results are reported in SI from refs.