Dietary trends in herbivores from the Shungura Formation, southwestern Ethiopia

Edited by Thure E. Cerling, University of Utah, Salt Lake City, UT, and approved July 27, 2020 (received for review April 14, 2020)
August 24, 2020
117 (36) 21921-21927
Research Article
Isotopic evidence for the timing of the dietary shift toward C4 foods in eastern African Paranthropus
Jonathan G. Wynn, Zeresenay Alemseged [...] Matt Sponheimer
Commentary
Paranthropus through the looking glass
Bernard A. Wood, David B. Patterson

Significance

Studying the diet of fossil herbivores is a critical aspect of understanding past ecology. Here, we present carbon isotope data from the collective herbivore fauna in the Shungura Formation, Ethiopia, a key sequence for the study of mammalian evolution in eastern Africa. We document temporal patterns in the diet of nine mammalian herbivore families in the late Pliocene and early Pleistocene. The diet of herbivores has significantly changed in the last 3.5 Ma, and major dietary transitions are observed in several taxa around ∼2.7 Ma and then at ∼2.0 Ma. These patterns reflect response of the fauna to major ecological and environmental changes and provide a comparative framework for the study of hominin diet during this time.

Abstract

Diet provides critical information about the ecology and environment of herbivores. Hence, understanding the dietary strategies of fossil herbivores and the associated temporal changes is one aspect of inferring paleoenvironmental conditions. Here, we present carbon isotope data from more than 1,050 fossil teeth that record the dietary patterns of nine herbivore families in the late Pliocene and early Pleistocene (3.6 to 1.05 Ma) from the Shungura Formation, a hominin-bearing site in southwestern Ethiopia. An increasing trend toward C4 herbivory has been observed with attendant reductions in the proportions of browsers and mixed feeders through time. A high proportion of mixed feeders has been observed prior to 2.9 Ma followed by a decrease in the proportion of mixed feeders and an increase in grazers between 2.7 and 1.9 Ma, and a further increase in the proportion of grazers after 1.9 Ma. The collective herbivore fauna shows two major change points in carbon isotope values at ∼2.7 and ∼2.0 Ma. While hominin fossils from the sequence older than 2.7 Ma are attributed to Australopithecus, the shift at ∼2.7 Ma indicating the expansion of C4 grasses on the landscape was concurrent with the first appearance of Paranthropus. The link between the increased C4 herbivory and more open landscapes suggests that Australopithecus lived in more wooded landscapes compared to later hominins such as Paranthropus and Homo, and has implications for key morphological and behavioral adaptations in our lineage.
Environmental change in the Pliocene and Pleistocene is among the key drivers thought to have shaped the course of human evolution (13). Well-dated hominin-bearing sites that span this critical time period offer a unique opportunity to investigate the tempo and patterns of paleoenvironmental shifts. This, in turn, allows us to test hypotheses about the links between environmental change and morphological and behavioral adaptations in the hominin clade (46). The Shungura Formation in the lower Omo Valley of southwestern Ethiopia is a key site spanning the time from ∼3.6 to ∼1 Ma, which possesses an exceptionally rich record of fossil vertebrates including hominins. The formation consists of a stratigraphic sequence with a composite thickness of >760 m divided into 12 members (i.e., Basal, A, B, C, D, E, F, G, H, J, K and L). Each member is underlain by a volcanic tuff layer that allows accurate radiometric age attribution for the corresponding member (7, 8). Over 50,000 fossil specimens belonging to more than 14 mammalian families were recovered in the 1960s and 1970s by the International Omo Research Expedition, and field work has recently been resumed by the Omo Group Research Expedition (9, 10).
The hominin taxa from the Shungura Formation include Australopithecus sp., Paranthropus aethiopicus, Paranthropus boisei, and Homo sp. (11, 12). The hominin fossil record is thus unique as it spans the time period between 3.0 and 2.0 Ma that coincides with the earliest records of Homo and Paranthropus (13, 14). As such, this sedimentary sequence provides the unique opportunity to test the role of the environment in the origin and evolution of our genus. The sedimentological record indicates that the lower Omo Valley from Member A (3.6 Ma) through the middle of Member G (2.1 Ma) was dominated by a large meandering river (15). This was followed by a shift to lacustrine conditions in middle and upper Member G (2.1 to 1.9 Ma), and a return to fluvial conditions in Members H through L (1.9 to 1.0 Ma) (16). Paleosols in the lower part of the Shungura sequence (Members A and B) indicate relatively high precipitation and a warm climate, with a shift to more sporadic precipitation and a generally drier climate in Member C and above (17). Stable isotopes from pedogenic carbonates suggest that Members B through G were dominated by extensive woodlands, with a shift to wooded grasslands above Member G, i.e., after 2 Ma (18). The evidence of paleobotanical remains (fossil wood, fruits, and pollen) (1921) and micromammals (22, 23) corroborates that Members A and B had more extensive woodlands and forests than later members, and that environmental conditions became more open above Member G, after 2 Ma. Previous analyses of large mammals reinforce these interpretations, with shifts in taxonomic abundances at about 2.9 Ma, and higher proportions of grazing species first around 2.5 to 2.4 Ma (24, 25), then at the base of Member G at 2.3 Ma (25, 26), and more markedly after 2 Ma (27). Even though these environmental changes are well documented in the Shungura Formation from 3.6 to 2 Ma, it has been suggested that the Omo remained more wooded than other parts of the Omo-Turkana Basin (West Turkana, East Turkana) and provided a partial refugium for woodland species (e.g., Tragelaphini) (18, 28, 29).
Here we use stable isotope data from herbivore tooth enamel to characterize the diet of large mammals from the Shungura Formation. The use of stable isotopes is predicated upon our understanding of carbon isotope fractionation during photosynthesis in C3 plants (i.e., trees, shrubs, herbs, and temperate and high-altitude grasses) and C4 plants (mainly tropical grasses and sedges) (3032). As plants are the primary source of carbon for herbivores, the distinct isotopic signature of foods consumed is recorded in body tissues (e.g., bones and teeth) with a relatively consistent fractionation factor. Thus, the carbon isotopic values of tooth enamel reflect the diet of herbivores and can be used to infer the vegetation available on the landscape (3335). Although isotopic data have been reported for a few taxonomic groups from the Shungura Formation (25, 36, 37), a detailed isotopic record of the broader large herbivore fauna is currently lacking. Here, we present dietary trends in nine mammalian families using >1,050 fossil specimens from the Shungura Formation and provide a fresh perspective on the ecological context of hominins in the late Pliocene and early Pleistocene.

Results

In this section we report on analyses of carbon isotope values from each mammalian family binned at the stratigraphic level of members (Fig. 1 and Dataset S1). Mammalian families are presented in the order of their abundance (i.e., from the most to the least abundant in terms of number of identified specimens) with median δ13C values and ranges provided for each taxon. It should be noted that, overall, the relative abundance of browsers decreases through time as noted in previous work (2426).
Fig. 1.
Box and whisker plots of δ13C values for the fossil tooth enamel data from Shungura Formation across nine mammalian families. Median values are marked by a vertical line within the box, the edges of the boxes represent the lower and upper quartile values, the whiskers extend from the edge of the box to the largest and smallest value no farther than 1.5 * interquartile range, and outliers are plotted as black dots. Green, white, and yellow shades indicate C3 browsers, C3–C4 mixed feeders, and C4 grazers, respectively.

Bovidae.

The bovids analyzed comprise 414 specimens belonging to five tribes: Reduncini, Tragelaphini, Aepycerotini, Alcelaphini, and Bovini. Collectively, the bovids show a trend toward increasing C4 resource consumption through time, with statistically significant differences in δ13C values between some members. While the transition from Member A to B shows a shift from C3 and mixed C3–C4 diets to a broader dietary spectrum of C3, mixed C3–C4, and C4 diets (Wilcoxon rank-sum test, P = 0.02), a shift toward higher δ13C values and more C4-dominated diets was observed between Members B and C (t test, P < 0.01).

Reduncini.

Samples from Reduncini have a median δ13C value of −0.7‰, with values ranging from −13.4 to +2.6‰ (although the minimum values are driven by two outliers) (n = 90). The data indicate that reduncins had a predominantly mixed C3–C4 diet during the earlier members of the formation (i.e., Member B) and shifted to a C4-dominated diet during later periods.

Aepycerotini.

Samples of Aepycerotini have a median δ13C value of −2.2‰, with values ranging from −9.2 to +2.5‰ (n = 96). The overall dietary pattern for Aepyceros indicates a mixed C3–C4 diet in the earlier members (Members A and B) followed by a shift to a C4-dominated diet in Members C through F, and a slight change back to a diet dominated by mixed C3–C4 resources in the upper Members G through L.

Tragelaphini.

The median δ13C value for tragelaphin bovids (n = 104) is −5.2‰ with δ13C values ranging from −11.6 to +3.0‰. This indicates a diet dominated by mixed C3–C4 resources.

Alcelaphini.

Samples from alcelaphin bovids (n = 67) have a median δ13C value of +1.0‰ with values ranging from −6.9 to +3.9‰, indicating a relatively consistent C4 diet. A shift toward higher δ13C values within the C4 diet category was observed between Members B and C (Wilcoxon rank sum test, P < 0.01).

Bovini.

The median δ13C value of bovin specimens (n = 57) is +0.6‰ with values ranging from −10.6 to +4.4‰. Except for Member A, in which values indicative of a mixed C3–C4 diet are displayed, the dietary pattern throughout the remainder of the sequence is a relatively consistent C4-dominated diet.

Hippopotamidae.

A mixed C3–C4 diet and a higher percentage of C4 resources at times was observed in hippopotamids (n = 81), with an overall median value of −3.3‰ with minimum and maximum values of −8.7 and +1.1‰, respectively.

Cercopithecidae.

This sample comprises 73 specimens identified as the genus Theropithecus. The overall median δ13C value for Theropithecus is −2.9‰ with a −9.2 to +0.4‰ range. These data indicate a diet dominated by mixed C3–C4 and C4 resources. A statistically significant difference (Wilcoxon rank-sum test, P = 0.01) in δ13C values was observed between Members B and C with the latter having higher δ13C values.

Suidae.

This family (n = 258) comprises four genera: Nyanzachoerus, Kolpochoerus, Notochoerous, and Metridiochoerus. An overall increase in C4 resource consumption with time was observed with significant shifts between some members. Among suids in general, the transition from Member B to C was accompanied by a notable change from a mixed C3–C4 and a C4-dominated diet to a predominantly C4 diet (Wilcoxon rank-sum test, P < 0.01), and the change from Member G to Member H also shows a shift toward higher δ13C values within the C4 diet category (Wilcoxon rank-sum test, P < 0.01).

Nyanzachoerus.

Known from a small sample size (n = 12) in the lower members only, Nyazachoerus has an overall median δ13C value of −3.6‰, indicating a diet of mixed C3–C4 resources.

Notochoerus.

Specimens of Notochoerus (n = 87) have an overall median δ13C value of −1.2‰ with a range between −7 and +0.3‰. Apart from some samples in Members A and B that show a mixed C3–C4 diet, the δ13C results indicate that Notochoerus had a diet dominated by C4 resources. A shift toward higher δ13C values within the C4 diet category was observed between Members G and H (Wilcoxon rank-sum test, P = 0.01).

Metridiochoerus.

The median δ13C value for Metridiochoerus (n = 78) is −0.9‰ with a range between −8.1 and +1.6‰. Throughout the formation, Metridiochoerus maintained a relatively consistent C4-dominated diet, with the transition from Member G to H marked by a significant shift (Wilcoxon rank-sum test, P = 0.01) toward higher δ13C values.

Kolpochoerus.

The median δ13C value for samples from Kolpochoerus throughout the Shungura Formation (n = 81) is −0.8‰, with values ranging from −8.9 to +0.9‰. It appears that initially (i.e., Members A and B) Kolpochoerus was a mixed feeder but there was a later shift (with a statistically significant difference between Members B and C, Wilcoxon rank-sum test, P < 0.01) to a C4-dominated diet in the upper members. Similarly, the transition from Member G to H was marked by a significant shift (Wilcoxon rank-sum test, P = 0.01) toward higher δ13C values.

Elephantidae.

The overall median δ13C value of samples of elephantids (n = 86) is −1.8‰ with values ranging from −12.4 to +0.8‰. A mixed C3–C4-dominated diet was observed in the lower members of the formation (i.e., Members A to E) that changed to predominantly C4 resource consumption in the upper members (Members F through L). Across the members, a statistically significant shift to a higher incorporation of C4 resources was observed between Members B and C (Wilcoxon rank-sum test, P = 0.02).

Giraffidae.

A consistently C3 (browse)-dominated diet was observed in the giraffes throughout the sequence. The sample has a median δ13C value of −12.4‰ and a narrow range between −14.9 and −10.4‰ (n = 23).

Equidae.

Except for the mixed C3–C4 diet observed in some individual samples in Member B (which is significantly different from Member C, Wilcoxon rank-sum test, P < 0.01), the equids show a consistent C4 diet with a median value of +0.1‰ and values ranging from −5.2 to +2.2‰ (n = 68).

Deinotheriidae.

Throughout the formation, the deinotheres were consistent C3 browsers, showing no change in their diet with a median δ13C value of −14.0‰ and a range between −15.7 and −11.5‰ (n = 65). This is a narrow range compared to other taxa.

Rhinocerotidae.

The 17 specimens assigned to the genus Ceratotherium show an overall median δ13C value of −0.9‰ with values ranging from −13.7 to +0.8‰. Although there are specimens that indicate a mixed C3–C4 diet in some members (and a few outliers showing a C3-dominated diet), the genus overall has a clear C4 diet. Moreover, it may also be that the few outliers belong to Diceros (a C3 browser), misidentified as Ceratotherium, as the distinction between the two genera is considered problematic based solely on fragmentary dental remains (38).

Discussion

Herbivore Diet in the Pliocene and Pleistocene.

In general, based on the grazer–mixed feeder–browser ternary classification (3941) at the member level (Fig. 2A), three major periods are evident with differing ecological groupings: 1) herbivore fauna dominated by mixed feeders occurs in Members A, B, and D; 2) faunas with abundant mixed feeders and grazers in Members C, E, F, and G; and 3) grazer-dominated faunas in Members H, J, K, and L. The first and second groups also have statistically significant differences in δ13C values between Members B and C, which is evident in multiple lineages (i.e., bovids, suids, cercopithecids, elephantids, and equids) that show an increase in C4 food intake.
Fig. 2.
Ternary diagram showing proportions of C3 browsers, C3–C4 mixed feeders, and C4 grazers at the member level (A) and for 200 kyr time bins (B). Each point in the figure represents the respective proportions in the specified time units. Triangle represents regions where >50% of the taxa are browsers, mixed feeders, or grazers in each category. Browser, mixed feeder, and grazer categories are adopted from ref. 39.
Because member-level stratigraphic units of the Shungura Formation do not represent equivalent temporal durations, this analysis of the grazer–mixed feeder–browser ternary diet classification was also calculated for 200 kyr time bins (Fig. 2B). Similarly, these finer timescale temporal bins show a high proportion of mixed feeders prior to ∼2.9 Ma, a decrease in the proportion of mixed feeders and an increase in grazers from ∼2.7 to 1.9 Ma followed by a high proportion of grazers after 1.9 Ma. The outlying high proportion of browsers from 2.9 to 2.7 Ma likely results from the small sample size in this time period with relatively abundant deinotheres and giraffes. This supports the argument that the faunal composition changed after 2.9 Ma and again after 1.9 Ma, based on the member-level analysis. Similar patterns have been reported from the Turkana Basin where C3–C4 mixed-feeder herbivores dominated the ecosystem prior to 2.5 Ma, to be replaced by dominantly grazing taxa after 2.5 Ma (39). Despite these similarities, there are slight differences in the timing of shifts toward grazing-dominated fauna at the expense of mixed feeders, which occurs later (i.e., after 1.9 Ma) in the Shungura Formation compared to after 2.3 Ma in the southern portion of the Omo-Turkana Basin. This indicates the consistent presence of C3 resources and further supports previous notions that the paleo Omo River provided broad gallery forests that served as a refugium for C3-browsing fauna under relatively stable hydrological conditions in an otherwise increasingly seasonal and arid basin (42, 43).

Temporal Patterns in the Diet of Herbivores.

We used a nonparametric change-point analysis to detect distributional changes in the δ13C values in the Shungura mammalian fauna. First, the analysis was conducted using the complete faunal isotopic dataset including the nine mammalian families (Fig. 3) and then replicated for each family that shows a significant change in distribution (Fig. 4). Considering the herbivore fauna as a whole, there are two major change points, first at ∼2.7 Ma and then at ∼2.0 Ma. The first change point occurs in lower Member C (C-4), where the δ13C values change to a mixed C3–C4-and C4-dominated distribution. The second change point occurs at upper Member G (G-28), where there is a change to a C4-dominated distribution. These change points are more or less congruent with the patterns portrayed by the ternary diagrams shown in Fig. 2. Assessing the mammalian families individually, five taxa show significant changes in the distribution of δ13C values. The bovids show two major change points at ∼2.7 and ∼2.3 Ma. The first change point occurs at the same time as the ∼2.7-Ma change observed for the composite fauna (Member C unit 4). Even though significant differences are observed between the bovids in Members B (∼3.4 to 2.8 Ma) and C (∼2.8 to 2.5 Ma) (Fig. 1), this analysis indicates that a change in distribution occurred within Member C. Closer examination of the faunal composition between 2.8 and 2.7 Ma indicates a very small sample size for bovids during this time, which might have resulted in this later change point. The second change point occurs at ∼2.3 Ma (at the base of Member F). These results are consistent with previous studies that reported changes in the abundance, species composition, morphology, and diet in the bovids at these two time periods (2426, 36). The suids also show two major change points at ∼2.6 and ∼2.0 Ma. Similar to the bovids, despite the significant difference between Members B and C at the member-level analysis, the later change point at 2.6 Ma results from a small sample size of suids between 2.8 and 2.6 Ma. The second change point at ∼2.0 Ma is also consistent with the significant difference observed between Members G and H in this taxon. It also coincides with one of the two major change points observed for the herbivore fauna as a whole. These timings are also congruent with changes in dental morphology previously reported for this lineage (44). Likewise, the elephants show a change at 2.3 Ma consistent with previously reported dental morphology changes (45) and congruent with the change point observed in bovids. The hippopotamids, on the other hand, show a change at 2.55 Ma, slightly later than the change point in the bovids and suids. However, a close inspection of the isotope dataset shows a very small sample size of hippopotamids between 2.8 and 2.55 Ma, which might have resulted in this later change point. Theropithecus shows a change at ∼2.4 Ma (Member E unit 2), which is similar to what has been observed in the hominins from the Shungura Formation (46). Apart from Theropithecus and the hominins, the other herbivores show changes in the distribution of δ13C values that coincide with previously reported paleoecological changes in the Shungura Formation between Members B and C (24, 36), between Members F and G (26), and after Member G (27). While these previous studies analyzed selected taxa or different components of the fossil collections (e.g., collections from the French vs. American expeditions), this comprehensive study includes the collective herbivore fauna from both the French and American collections and further confirms that real ecological changes indeed occurred in the Shungura Formation between 2.9 and 2.0 Ma.
Fig. 3.
Significant change points in the distribution of δ13C values across herbivore mammalian lineages in the Shungura Formation (shown as red dashed line). The histograms (Right) show distribution of δ13C values in each category before and after the major change points. Green, white, and yellow shades indicate C3 browsers, C3–C4 mixed feeders, and C4 grazers, respectively.
Fig. 4.
Change points in mammalian families that show significant changes in the distribution of δ13C values (shown as red dashed line). The histograms show distribution of δ13C values for each taxa before and after the major change points. Green, white, and yellow shades indicate C3 browsers, C3–C4 mixed feeders, and C4 grazers, respectively.

Conclusion

Stable carbon isotope data from herbivores in the Shungura Formation indicate a trend toward increasing C4 herbivory with attendant reductions in the proportions of browsers and mixed feeders. This is similar to other Pliocene and Pleistocene sites in eastern Africa (39). However, despite this increasing trend toward C4 diets, the higher proportion of mixed feeders indicates relative environmental stability, compared to contemporaneous sites elsewhere in eastern Africa. Thus, more wooded habitats (i.e., C3 resources) were available to hominins in the Shungura Formation compared to contemporaneous sites south of the basin on a landscape that was gradually becoming more open and dominated by C4 resources. Among the major dietary shifts observed in herbivores, the shift at ∼2.7 Ma, which indicates the expansion of C4 grasses on the landscape, was concurrent with the first appearance of Paranthropus in the Shungura Formation (47). The hominin fossils from the sequence older than 2.7 Ma are attributed to Australopithecus or Hominini gen. et sp. indet, and these appear to have lived in more wooded landscapes compared to later hominins such as Paranthropus and Homo. These results are also congruent with other studies that indicate Australopithecus lived in more wooded settings compared to later hominins such as early Homo (48, 49). Overall, the increasing expansion of C4 grasses on the landscape at the expense of wooded habitats across depositional basins has further implications for key adaptations in our lineage such as morphological changes (e.g., loss of features that attest to arboreal adaptations) or behavioral changes (e.g., increased reliance on C4 dietary resources by consuming either plant or animal resources) (27, 50, 51).

Materials and Methods

Fossil teeth were sampled at the National Museum of Ethiopia. Taxonomic assignments are based on a printed version of faunal databases in the National Museum of Ethiopia and updated electronic versions provided by R.B. and Z.A. The specimens were cleaned before sampling, and powdered enamel samples were extracted. The samples were pretreated with hydrogen peroxide and acetic acid–calcium acetate buffer, and isotopic ratios were measured on a Thermo Fisher Scientific (Finnigan) Delta V Isotope Ratio Mass Spectrometer at the University of South Florida. Age estimates for fossil samples are based on a well-established chronology of stratigraphic units using radiometric dates and magnetostratigraphy (8, 16, 52). All statistical analyses including the nonparametric change point analysis (53) were performed using R statistical software.

Data Availability

All study data are included in the article and SI Appendix.

Acknowledgments

We thank the Authority for Research and Conservation of Cultural Heritage, the National Museum of Ethiopia, and the Ethiopian Ministry of Culture and Tourism for research permission. We also thank Tomas Getachew and Sahle Melaku for help in accessing the fossil specimens; Jennifer Leichliter and Oliver Paine for their assistance in isotope sampling; Jessica Wilson for aid with isotopic analytical work; and Bernard Wood, Anna K. Behrensmeyer, and two anonymous reviewers for their comments on earlier versions of this manuscript. This research was supported by National Science Foundation Award 1252157.

Supporting Information

Appendix (PDF)
Dataset_S01 (XLSX)
Dataset_S02 (XLSX)

References

1
R. Potts, Evolution and environmental change in early human prehistory. Annu. Rev. Anthropol. 41, 151–167 (2012).
2
P. B. deMenocal, Anthropology. Climate and human evolution. Science 331, 540–542 (2011).
3
N. E. Levin, Environment and climate of early human evolution. Annu. Rev. Earth Planet. Sci. 43, 405–429 (2015).
4
A. K. Behrensmeyer, Atmosphere. Climate change and human evolution. Science 311, 476–478 (2006).
5
National Research Council, Understanding Climate’s Influence on Human Evolution, (National Academies Press, 2010).
6
M. A. Maslin, S. Shultz, M. H. Trauth, A synthesis of the theories and concepts of early human evolution. Philos. Trans. R Soc. B: Biol. Sci. 370, 20140064 (2015).
7
C. S. Feibel, F. H. Brown, I. McDougall, Stratigraphic context of fossil hominids from the Omo group deposits: Northern Turkana Basin, Kenya and Ethiopia. Am. J. Phys. Anthropol. 78, 595–622 (1989).
8
I. McDougall et al., New single crystal 40Ar/39Ar ages improve time scale for deposition of the Omo group, Omo–Turkana Basin, East Africa. J. Geol. Soc. London 169, 213–226 (2012).
9
J. R. Boisserie et al., New palaeoanthropological research in the Plio-Pleistocene Omo group, lower Omo Valley, SNNPR (southern nations, nationalities and people regions), Ethiopia. C. R. Palevol 7, 429–439 (2008).
10
Z. Alemseged, R. Bobe, D. Geraads, “Comparability of fossil data and its significance for the interpretation of hominin environments” in Hominin Environments in the East African Pliocene: An Assessment of the Faunal Evidence, A. K. Behrensmeyer, R. Bobe, Z. Alemseged, Eds. (Springer, Dordrecht, The Netherlands, 2007), pp. 159–181.
11
G. Suwa, T. D. White, F. C. Howell, Mandibular postcanine dentition from the Shungura formation, Ethiopia: Crown morphology, taxonomic allocations, and Plio-Pleistocene hominid evolution. Am. J. Phys. Anthropol. 101, 247–282 (1996).
12
B. Wood, M. Leakey, The Omo-Turkana basin fossil hominins and their contribution to our understanding of human evolution in Africa. Evol. Anthropol. 20, 264–292 (2011).
13
B. Villmoare et al., Paleoanthropology. Early Homo at 2.8 Ma from Ledi-Geraru, Afar, Ethiopia. Science 347, 1352–1355 (2015).
14
B. Wood, P. Constantino, Paranthropus boisei: Fifty years of evidence and analysis. Am. J. Phys. Anthropol. 134 (suppl. 45), 106–132 (2007).
15
J. de Heinzelin, P. Haesaerts, F. C. Howell, “Plio-Pleistocene formations of the lower Omo basin with particular reference to the Shungura Formation” in Earliest Man and Environments in the Lake Rudolf Basin, Y. Coppens, F. C. Howell, G. L. Isaac, R. E. Leakey, Eds. (University of Chicago Press, 1976), pp. 24–49.
16
J. de Heinzelin, P. Haesaerts, “The Shungura formation” in The Omo Group, J. de Heinzelin, Ed. (Musée Royale de l’Afrique Central, Tervuren, Belgium, 1983), pp. 25–127.
17
P. Haesaerts, G. Stoops, B. Van Vliet-Lanoë, “Data on sediments and fossil soils” in The Omo Group, J. de Heinzelin, Ed. (Musée Royale de l’Afrique Central, Tervuren, Belgium, 1983), pp. 149–185.
18
N. E. Levin, F. H. Brown, A. K. Behrensmeyer, R. Bobe, T. E. Cerling, Paleosol carbonates from the Omo Group: Isotopic records of local and regional environmental change in East Africa. Palaeogeogr. Palaeoclimatol. Palaeoecol. 307, 75–89 (2011).
19
R. Bonnefille, R. Dechamps, “Data on fossil flora” in The Omo Group, J. de Heinzelin, Ed. (Musée Royale de l’Afrique Central, Tervuren, Belgium, 1983), pp. 191–207.
20
R. Bonnefille, R. Letouzey, Fruits fossiles d’Antrocaryon dans la vallée de l’Omo (Éthiopie). Adansonia, Ser. 2 16, 65–82 (1976).
21
R. Dechamps, F. Maes, “Essai de reconstitution des climats et des végétations de la basse vallée de l’Omo au Plio-Pléistocène à l’aide de bois fossiles” in L’Environnement des Hominidés au Plio-Pléistocène, Y. Coppens, Ed. (Masson, Paris, 1985), pp. 175–222.
22
H. B. Wesselman, The Omo micromammals: Systematics and paleoecology of early man sites from Ethiopia. Contrib. Vertebr. Evol. 7, 1–219 (1984).
23
H. B. Wesselman, “Of mice and almost-men: Regional paleoecology and human evolution in the Turkana Basin” in Paleoclimate and Evolution with Emphasis on Human Origins, E. S. Vrba, G. H. Denton, T. C. Partridge, L. H. Burckle, Eds. (Yale University Press, New Haven, CT, 1995), pp. 356–368.
24
R. Bobe, G. G. Eck, Responses of African bovids to Pliocene climatic change. Paleobiology memoirs. Paleobiology 27, 1–48 (2001).
25
E. W. Negash, Z. Alemseged, J. G. Wynn, Z. K. Bedaso, Paleodietary reconstruction using stable isotopes and abundance analysis of bovids from the Shungura formation of South Omo, Ethiopia. J. Hum. Evol. 88, 127–136 (2015).
26
Z. Alemseged, An integrated approach to taphonomy and faunal change in the Shungura formation (Ethiopia) and its implication for hominid evolution. J. Hum. Evol. 44, 451–478 (2003).
27
R. Bobe, A. K. Behrensmeyer, The expansion of grassland ecosystems in Africa in relation to mammalian evolution and the origin of the genus Homo. Palaeogeogr. Palaeoclimatol. Palaeoecol. 207, 399–420 (2004).
28
R. Bobe, Fossil mammals and paleoenvironments in the Omo-Turkana Basin. Evol. Anthropol. 20, 254–263 (2011).
29
T. W. Plummer et al., Bovid ecomorphology and hominin paleoenvironments of the Shungura formation, lower Omo River Valley, Ethiopia. J. Hum. Evol. 88, 108–126 (2015).
30
B. N. Smith, S. Epstein, Two categories of c/c ratios for higher plants. Plant Physiol. 47, 380–384 (1971).
31
M. H. O’Leary, Carbon isotopes in photosynthesis. Bioscience 38, 328–336 (1988).
32
L. L. Tieszen, M. M. Senyimba, S. K. Imbamba, J. H. Troughton, The distribution of C3 and C4 grasses and carbon isotope discrimination along an altitudinal and moisture gradient in Kenya. Oecologia 37, 337–350 (1979).
33
M. J. DeNiro, S. Epstein, Influence of diet on the distribution of carbon isotopes in animals. Geochim. Cosmochim. Acta 42, 495–506 (1978).
34
S. H. Ambrose, M. J. DeNiro, The isotopic ecology of East African mammals. Oecologia 69, 395–406 (1986).
35
T. E. Cerling, J. M. Harris, Carbon isotope fractionation between diet and bioapatite in ungulate mammals and implications for ecological and paleoecological studies. Oecologia 120, 347–363 (1999).
36
F. Bibi, A. Souron, H. Bocherens, K. Uno, J. R. Boisserie, Ecological change in the lower Omo Valley around 2.8 Ma. Biol. Lett. 9, 20120890 (2012).
37
A. Souron, M. Balasse, J. R. Boisserie, Intra-tooth isotopic profiles of canines from extant Hippopotamus amphibius and late Pliocene hippopotamids (Shungura formation, Ethiopia): Insights into the seasonality of diet and climate. Palaeogeogr. Palaeoclimatol. Palaeoecol. 342, 97–110 (2012).
38
D. Geraads, Z. Alemseged, D. Reed, J. Wynn, D. C. Roman, The Pleistocene fauna (other than Primates) from Asbole, lower Awash Valley, Ethiopia, and its environmental and biochronological implications. Geobios 37, 697–718 (2004).
39
T. E. Cerling et al., Dietary changes of large herbivores in the Turkana Basin, Kenya from 4 to 1 Ma. Proc. Natl. Acad. Sci. U.S.A. 112, 11467–11472 (2015).
40
M. Sponheimer, J. A. Lee-Thorp, Using carbon isotope data of fossil bovid communities for palaeoenvironmental reconstruction: Research articles: Human origins research in South Africa. S. Afr. J. Sci. 99, 273–275 (2003).
41
J. A. Lee-Thorp, M. Sponheimer, J. Luyt, Tracking changing environments using stable carbon isotopes in fossil tooth enamel: An example from the South African hominin sites. J. Hum. Evol. 53, 595–601 (2007).
42
Vrba, “Late Pliocene climatic events and hominid evolution” in Evolutionary History of the “Robust” Australopithecines, F. E. Grine, Ed. (Aldine de Gruyter, New York, 1988), pp. 405–426.
43
R. Bobe, The evolution of arid ecosystems in eastern Africa. J. Arid Environ. 66, 564–584 (2006).
44
H. B. S. Cooke, “Stratigraphic variation in Suidae from the Shungura formation and some coeval deposits” in Hominin Environments in the East African Pliocene: An Assessment of the Faunal Evidence, A. K. Behrensmeyer, R. Bobe, Z. Alemseged, Eds. (Springer, Dordrecht, The Netherlands, 2007), pp. 107–127.
45
M. Beden, “Les Proboscidiens des grands gisements à Hominidés plio-pléistocènes d’Afrique orientale” in L’Environment des Hominidés au Plio-Pléistocène, Y. Coppens, Ed. (Masson, 1985), pp. 21–44.
46
J. G. Wynn et al., Isotopic evidence for the timing of the dietary shift toward C4 foods in eastern African Paranthropus. Proc. Nat. Acad. Sci. U.S.A. 117, 21978–21984 (2020).
47
C. Arambourg, Y. Coppens, Découverte d’un australopithécien nouveau dans les gisements de l’Omo (Éthiopie). S. Afr. J. Sci. 64, 58–59 (1968).
48
E. N. DiMaggio et al., Paleoanthropology. Late Pliocene fossiliferous sedimentary record and the environmental context of early Homo from Afar, Ethiopia. Science 347, 1355–1359 (2015).
49
J. R. Robinson, J. Rowan, C. J. Campisano, J. G. Wynn, K. E. Reed, Late Pliocene environmental change during the transition from Australopithecus to Homo. Nat. Ecol. & Evol. 1, 0159 (2017).
50
B. G. Richmond, D. R. Begun, D. S. Strait, Origin of human bipedalism: The knuckle-walking hypothesis revisited. Am. J. Phys. Anthropol. 116 (suppl. 33), 70–105 (2001).
51
T. E. Cerling et al., Woody cover and hominin environments in the past 6 million years. Nature 476, 51–56 (2011).
52
T. Kidane, F. H. Brown, C. Kidney, Magnetostratigraphy of the fossil-rich Shungura formation, southwest Ethiopia. J. Afr. Earth Sci. 97, 207–223 (2014).
53
D. S. Matteson, N. A. James, A nonparametric approach for multiple change point analysis of multivariate data. J. Am. Stat. Assoc. 109, 334–345 (2014).

Information & Authors

Information

Published in

Go to Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences
Vol. 117 | No. 36
September 8, 2020
PubMed: 32839326

Classifications

Data Availability

All study data are included in the article and SI Appendix.

Submission history

Published online: August 24, 2020
Published in issue: September 8, 2020

Keywords

  1. stable isotopes
  2. herbivores
  3. fauna
  4. tooth enamel
  5. Shungura Formation

Acknowledgments

We thank the Authority for Research and Conservation of Cultural Heritage, the National Museum of Ethiopia, and the Ethiopian Ministry of Culture and Tourism for research permission. We also thank Tomas Getachew and Sahle Melaku for help in accessing the fossil specimens; Jennifer Leichliter and Oliver Paine for their assistance in isotope sampling; Jessica Wilson for aid with isotopic analytical work; and Bernard Wood, Anna K. Behrensmeyer, and two anonymous reviewers for their comments on earlier versions of this manuscript. This research was supported by National Science Foundation Award 1252157.

Notes

This article is a PNAS Direct Submission.
See online for related content such as Commentaries.

Authors

Affiliations

Center for the Advanced Study of Human Paleobiology, George Washington University, Washington, DC 20052;
Department of Organismal Biology and Anatomy, University of Chicago, Chicago, IL 60637;
School of Anthropology, University of Oxford, Oxford OX2 6PE, United Kingdom;
Gorongosa National Park, Sofala, Mozambique;
Department of Anthropology, Stony Brook University, Stony Brook, NY 11794;
Department of Anthropology, University of Colorado Boulder, Boulder, CO 80302;
Division of Earth Sciences, National Science Foundation, Alexandria, VA 22314

Notes

1
To whom correspondence may be addressed. Email: [email protected].
Author contributions: E.W.N., Z.A., R.B., F.G., M.S., and J.G.W. designed research; E.W.N., 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 J.G.W. analyzed data; and E.W.N., Z.A., R.B., F.G., M.S., and J.G.W. wrote the paper.

Competing Interests

The authors declare no competing interest.

Metrics & Citations

Metrics

Note: The article usage is presented with a three- to four-day delay and will update daily once available. Due to ths delay, usage data will not appear immediately following publication. Citation information is sourced from Crossref Cited-by service.


Citation statements




Altmetrics

Citations

If you have the appropriate software installed, you can download article citation data to the citation manager of your choice. Simply select your manager software from the list below and click Download.

Cited by

    Loading...

    View Options

    View options

    PDF format

    Download this article as a PDF file

    DOWNLOAD PDF

    Get Access

    Login options

    Check if you have access through your login credentials or your institution to get full access on this article.

    Personal login Institutional Login

    Recommend to a librarian

    Recommend PNAS to a Librarian

    Purchase options

    Purchase this article to access the full text.

    Single Article Purchase

    Dietary trends in herbivores from the Shungura Formation, southwestern Ethiopia
    Proceedings of the National Academy of Sciences
    • Vol. 117
    • No. 36
    • pp. 21825-22604

    Media

    Figures

    Tables

    Other

    Share

    Share

    Share article link

    Share on social media