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Dietary Trends in Herbivores from the Shungura Formation, Southwestern Ethiopia

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Dietary Trends in Herbivores from the Shungura Formation, Southwestern Ethiopia Dietary trends in herbivores from the Shungura Formation, southwestern Ethiopia Enquye W. Negasha,1, Zeresenay Alemsegedb, René Bobec,d, Frederick Grinee, Matt Sponheimerf, and Jonathan G. Wynng aCenter for the Advanced Study of Human Paleobiology, George Washington University, Washington, DC 20052; bDepartment of Organismal Biology and Anatomy, University of Chicago, Chicago, IL 60637; cSchool of Anthropology, University of Oxford, Oxford OX2 6PE, United Kingdom; dGorongosa National Park, Sofala, Mozambique; eDepartment of Anthropology, Stony Brook University, Stony Brook, NY 11794; fDepartment of Anthropology, University of Colorado Boulder, Boulder, CO 80302; and gDivision of Earth Sciences, National Science Foundation, Alexandria, VA 22314 Edited by Thure E. Cerling, University of Utah, Salt Lake City, UT, and approved July 27, 2020 (received for review April 14, 2020) Diet provides critical information about the ecology and environ- evolution of our genus. The sedimentological record indicates ment of herbivores. Hence, understanding the dietary strategies of that the lower Omo Valley from Member A (3.6 Ma) through fossil herbivores and the associated temporal changes is one the middle of Member G (2.1 Ma) was dominated by a large aspect of inferring paleoenvironmental conditions. Here, we pre- meandering river (15). This was followed by a shift to lacustrine sent carbon isotope data from more than 1,050 fossil teeth that conditions in middle and upper Member G (2.1 to 1.9 Ma), and a record the dietary patterns of nine herbivore families in the late return to fluvial conditions in Members H through L (1.9 to 1.0 Ma) Pliocene and early Pleistocene (3.6 to 1.05 Ma) from the Shungura (16). Paleosols in the lower part of the Shungura sequence Formation, a hominin-bearing site in southwestern Ethiopia. An (Members A and B) indicate relatively high precipitation and a increasing trend toward C4 herbivory has been observed with at- warm climate, with a shift to more sporadic precipitation and tendant reductions in the proportions of browsers and mixed a generally drier climate in Member C and above (17). Stable feeders through time. A high proportion of mixed feeders has isotopes from pedogenic carbonates suggest that Members B been observed prior to 2.9 Ma followed by a decrease in the pro- through G were dominated by extensive woodlands, with a shift portion of mixed feeders and an increase in grazers between 2.7 to wooded grasslands above Member G, i.e., after 2 Ma (18). The and 1.9 Ma, and a further increase in the proportion of grazers evidence of paleobotanical remains (fossil wood, fruits, and after 1.9 Ma. The collective herbivore fauna shows two major – EARTH, ATMOSPHERIC, AND PLANETARY SCIENCES ∼ ∼ pollen) (19 21) and micromammals (22, 23) corroborates that change points in carbon isotope values at 2.7 and 2.0 Ma. While Members A and B had more extensive woodlands and forests hominin fossils from the sequence older than 2.7 Ma are attributed than later members, and that environmental conditions became to Australopithecus, the shift at ∼2.7 Ma indicating the expansion more open above Member G, after 2 Ma. Previous analyses of of C grasses on the landscape was concurrent with the first ap- 4 large mammals reinforce these interpretations, with shifts in pearance of Paranthropus. The link between the increased C4 her- bivory and more open landscapes suggests that Australopithecus taxonomic abundances at about 2.9 Ma, and higher proportions lived in more wooded landscapes compared to later hominins such of grazing species first around 2.5 to 2.4 Ma (24, 25), then at the as Paranthropus and Homo, and has implications for key morpho- base of Member G at 2.3 Ma (25, 26), and more markedly after ANTHROPOLOGY logical and behavioral adaptations in our lineage. 2 Ma (27). Even though these environmental changes are well documented in the Shungura Formation from 3.6 to 2 Ma, it has stable isotopes | herbivores | fauna | tooth enamel | Shungura Formation been suggested that the Omo remained more wooded than other parts of the Omo-Turkana Basin (West Turkana, East Turkana) nvironmental change in the Pliocene and Pleistocene is Eamong the key drivers thought to have shaped the course of Significance human evolution (1–3). Well-dated hominin-bearing sites that span this critical time period offer a unique opportunity to investigate the Studying the diet of fossil herbivores is a critical aspect of tempo and patterns of paleoenvironmental shifts. This, in turn, understanding past ecology. Here, we present carbon isotope allows us to test hypotheses about the links between environmental data from the collective herbivore fauna in the Shungura For- change and morphological and behavioral adaptations in the homi- mation, Ethiopia, a key sequence for the study of mammalian nin clade (4–6). The Shungura Formation in the lower Omo Valley evolution in eastern Africa. We document temporal patterns in of southwestern Ethiopia is a key site spanning the time from ∼3.6 to the diet of nine mammalian herbivore families in the late Pli- ∼1 Ma, which possesses an exceptionally rich record of fossil verte- ocene and early Pleistocene. The diet of herbivores has signif- icantly changed in the last 3.5 Ma, and major dietary transitions brates including hominins. The formation consists of a stratigraphic are observed in several taxa around ∼2.7 Ma and then at ∼2.0 sequence with a composite thickness of >760 m divided into 12 Ma. These patterns reflect response of the fauna to major members(i.e.,Basal,A,B,C,D,E,F,G,H,J,KandL).Each ecological and environmental changes and provide a compar- member is underlain by a volcanic tuff layer that allows accurate ative framework for the study of hominin diet during this time. radiometric age attribution for the corresponding member (7, 8). Over 50,000 fossil specimens belonging to more than 14 mammalian Author contributions: E.W.N., Z.A., R.B., F.G., M.S., and J.G.W. designed research; E.W.N., families were recovered in the 1960s and 1970s by the International Z.A., R.B., F.G., M.S., and J.G.W. performed research; E.W.N., Z.A., R.B., F.G., M.S., and Omo Research Expedition, and field work has recently been re- J.G.W. analyzed data; and E.W.N., Z.A., R.B., F.G., M.S., and J.G.W. wrote the paper. sumed by the Omo Group Research Expedition (9, 10). The authors declare no competing interest. The hominin taxa from the Shungura Formation include This article is a PNAS Direct Submission. Australopithecus sp., Paranthropus aethiopicus, Paranthropus Published under the PNAS license. boisei, and Homo sp. (11, 12). The hominin fossil record is thus See online for related content such as Commentaries. unique as it spans the time period between 3.0 and 2.0 Ma that 1To whom correspondence may be addressed. Email: [email protected]. Homo Paranthropus coincides with the earliest records of and This article contains supporting information online at https://www.pnas.org/lookup/suppl/ (13, 14). As such, this sedimentary sequence provides the unique doi:10.1073/pnas.2006982117/-/DCSupplemental. opportunity to test the role of the environment in the origin and First published August 24, 2020. www.pnas.org/cgi/doi/10.1073/pnas.2006982117 PNAS | September 8, 2020 | vol. 117 | no. 36 | 21921–21927 Downloaded by guest on September 24, 2021 and provided a partial refugium for woodland species (e.g., Hippopotamidae. A mixed C3–C4 diet and a higher percentage of Tragelaphini) (18, 28, 29). C4 resources at times was observed in hippopotamids (n = 81), Here we use stable isotope data from herbivore tooth enamel to with an overall median value of −3.3‰ with minimum and characterize the diet of large mammals from the Shungura Forma- maximum values of −8.7 and +1.1‰, respectively. tion. The use of stable isotopes is predicated upon our understanding of carbon isotope fractionation during photosynthesis in C3 plants Cercopithecidae. This sample comprises 73 specimens identified (i.e., trees, shrubs, herbs, and temperate and high-altitude grasses) as the genus Theropithecus. The overall median δ13C value for – and C4 plants (mainly tropical grasses and sedges) (30 32). As plants Theropithecus is −2.9‰ with a −9.2 to +0.4‰ range. These are the primary source of carbon for herbivores, the distinct isotopic data indicate a diet dominated by mixed C3–C4 and C4 resources. signature of foods consumed is recorded in body tissues (e.g., bones A statistically significant difference (Wilcoxon rank-sum test, P = and teeth) with a relatively consistent fractionation factor. Thus, the 0.01) in δ13C values was observed between Members B and C carbon isotopic values of tooth enamel reflect the diet of herbivores with the latter having higher δ13C values. and can be used to infer the vegetation available on the landscape (33–35). Although isotopic data have been reported for a few tax- Suidae. This family (n = 258) comprises four genera: Nyanza- onomic groups from the Shungura Formation (25, 36, 37), a detailed choerus, Kolpochoerus, Notochoerous, and Metridiochoerus.An isotopic record of the broader large herbivore fauna is currently overall increase in C resource consumption with time was ob- lacking. Here, we present dietary trends in nine mammalian families 4 served with significant shifts between some members. Among using >1,050 fossil specimens from the Shungura Formation and suids in general, the transition from Member B to C was ac- provide a fresh perspective on the ecological context of hominins in companied by a notable change from a mixed C –C and a C - thelatePlioceneandearlyPleistocene. 3 4 4 dominated diet to a predominantly C4 diet (Wilcoxon rank-sum Results test, P < 0.01), and the change from Member G to Member H also shows a shift toward higher δ13C values within the C diet In this section we report on analyses of carbon isotope values 4 category (Wilcoxon rank-sum test, P < 0.01).
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