<<

Aridity and hominin environments

Scott A. Blumenthala,1, Naomi E. Levinb, Francis H. Brownc, Jean-Philip Brugald, Kendra L. Chritze, John M. Harrisf, Glynis E. Jehlec, and Thure E. Cerlingc

aResearch Laboratory for Archaeology, University of Oxford, Oxford OX1 3QY, United Kingdom; bDepartment of Earth and Environmental Sciences, University of Michigan, Ann Arbor, MI 48109; cDepartment of Geology & Geophysics, University of Utah, Salt Lake City, UT 84112; dAix-Marseille University, CNRS, UMR 7269, Laboratoire Méditerranéen de Préhistoire Afrique, 13094 Aix-en-Provence Cedex 2, France; eNational Museum of Natural , Smithsonian Institution, Washington, DC 20013; and fNatural History Museum of Los Angeles County, Los Angeles, CA 90007

Edited by James O’Connell, University of Utah, Salt Lake City, UT, and approved May 25, 2017 (received for review January 11, 2017) Aridification is often considered a major driver of long-term ecolog- but drivers of environmental change might not be equivalent at ical change and hominin evolution in eastern during the Plio- short vs. long time scales and also may vary over time. ; however, this hypothesis remains inadequately tested Uncertainties in the relationships between climate and hominin owing to difficulties in reconstructing terrestrial paleoclimate. We environments stem in part from difficulties in reconstructing present a revised aridity index for quantifying water deficit (WD) in terrestrial aridity. Terrestrial climate indicators commonly used in terrestrial environments using tooth enamel δ18O values, and use this eastern Africa, including the isotopic composition of pedogenic approach to address paleoaridity over the past 4.4 million in carbonates (21, 27, 30), taxonomy (31–33), and mor- eastern Africa. We find no long-term trend in WD, consistent with phology (34), provide valuable insight into past environments, but other terrestrial climate indicators in the Omo-, and no are sensitive to multiple environmental and evolutionary changes, relationship between paleoaridity and paleodiet structure making it difficult to identify the specific role of aridity. In ad- among collections meeting the criteria for WD estimation. Thus, dition, existing faunal records (31–34) typically combine we suggest that changes in the abundance of C4 grass and from multiple sites and may integrate relatively long (but varying) in eastern Africa during the and Pleistocene may time periods. Other climate proxies, such as the deuterium iso- have been decoupled from aridity. As in modern African , tope composition of leaf wax biomarkers (17) and fossil leaf other factors, such as rainfall seasonality or ecological interactions morphology (35), have not been widely applied in Pliocene- among plants and , may be important for understanding Pleistocene sequences in Africa. the evolution of C4 grass- and grazer-dominated biomes. In the present study, we address paleoaridity using iso- tope ratios (δ18O) in herbivore tooth enamel. Our goal is to in- oxygen | terrestrial paleoclimate | evolution | mammals | vestigate the role of climate in shaping hominin environments over Africa the past 4.4 million years, concentrating on individual stratigraphic horizons associated with hominin fossil and archaeological mate- central challenge of human evolutionary studies is un- rial. We focus on the Omo-Turkana Basin, where sediments pre- Aderstanding the role of climatic change in shaping early serve abundant evidence of early hominin evolution and associated hominin environments and selective pressures (1, 2). Aridity influ- environments throughout the Pliocene and Pleistocene. The envi- ences the distribution and abundance of vegetation in African en- ronmental history of this basin is not necessarily representative of vironments (3), and changes in aridity over both long and short time eastern Africa (1), but nonetheless provides a useful study scales have been suggested to drive changes in hominin environ- for investigating interactions between climate and ecology. A major ments leading to adaptation, dispersal, , and (2, benefit of analyzing herbivore tooth enamel is the possibility of 4, 5). The notion that aridity may have driven certain adaptations comparing paired oxygen and carbon records from the has been fundamental to discussions of hominin evolution since same fossil collections in which hominin specimens or stone tools 1925 (6), and continues to feature prominently in studies addressing have been found, providing indicators of climate and ecology at changes in hominin locomotion, body proportions, thermoregula- ANTHROPOLOGY tion, food acquisition, tool use, and social organization (7–10). Significance Changes in African climate are driven principally by changes in Earth’s orbital geometry, which has been documented in the geo- Oxygen isotopes in modern and fossil mammals can provide in- logic past using marine and continental sedimentary records (4, 11– formation on climate. In this study, we provide a new record of 15). Marine core records of dust, leaf wax biomarkers, pollen, and aridity experienced by early hominins in Africa. We show that past sapropels indicate long-term aridification across Africa since the climates were similar to the climate in eastern Africa today, and late (4, 12, 14, 16–18), which has been linked to global that early hominins experienced highly variable climates over time. EARTH, ATMOSPHERIC,

cooling (19), changes in ocean circulation and temperature gradi- Unexpectedly, our findings suggest that the long-term expansion AND PLANETARY SCIENCES ents (20), high-latitude glaciation (4), low-latitude atmospheric of grasses and grazing herbivores since the Pliocene, a major circulation (14), and tectonic uplift (21). Increasing aridity has been ecological transformation thought to drive aspects of hominin evolution, was not coincident with aridification in northern Kenya. thought to drive the origin and subsequent expansion of C4 plants (grasses and sedges) (22). The long-term increase in the abundance This finding raises the possibility that some aspects of hominin environmental variability might have been uncoupled from aridity, of C4 plants throughout the Pliocene and Pleistocene has been well documented in eastern Africa using carbon isotope ratios in ped- and may instead be related to other factors, such as rainfall sea- ogenic carbonates and leaf wax biomarkers (23, 24) and coincides sonality or ecological interactions among plants and mammals. with an increasing reliance on C4-based resources among mam- Author contributions: S.A.B., N.E.L., F.H.B., and T.E.C. designed research; S.A.B., N.E.L., mals, including hominins and other (25, 26). Variation in F.H.B., J.-P.B., K.L.C., J.M.H., G.E.J., and T.E.C. performed research; S.A.B. and N.E.L. ana- the timing of vegetation change across basins indicates that existing lyzed data; and S.A.B. and N.E.L. wrote the paper. continental- and regional-scale climate records are not sufficient to The authors declare no conflict of interest. understand the drivers of basin- and local-scale ecological change, This article is a PNAS Direct Submission. and do not reflect local hominin environments (23, 27). Evidence 1To whom correspondence should be addressed. Email: [email protected]. for vegetation changes with precession-scale timing suggests direct This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. climate forcing of such changes over thousands of years (28, 29), 1073/pnas.1700597114/-/DCSupplemental.

www.pnas.org/cgi/doi/10.1073/pnas.1700597114 PNAS | July 11, 2017 | vol. 114 | no. 28 | 7331–7336 Downloaded by guest on September 29, 2021 spatial scales directly relevant to hominin environments. We can- A 5 km BC not address short-term orbital scale environmental variability,

however, owing to discontinuous sedimentation associated with KI1 SHUNGURA FM. NC3 KL3&6 NC1 NY4 terrestrial vertebrate fossil collections. KL2&6 NY3 LK FM. NY2 KL1 Our geochemical approach for quantifying aridity in tropical KS1 FwJj20 KS2 KK African ecosystems relies on differing oxygen isotopic effects FxJj82 10°N KG1&2 105-1311 LA1 4°N 105-0208 among taxa that are evaporation-sensitive (ES) or evaporation- FxJj1&3 LO3 104 LO8 NACHUKUI FM. insensitive (EI) (36, 37). This method, which builds on earlier work LO6 LO7 Allia Bay LO4 LO1/2 that focused on oxygen isotope variation among individual taxa KU2 0° LO5 (38–42), relies on a comparison of multiple taxa and simulta- LO10 KU1 KU3 3°N neously accounts for isotopic variation related to changes in both LO7 Lothagam climate and environmental water. This proxy has advantages over Kanapoi previously used paleoaridity indicators because it is largely in- 36°E 37°E 20°E 30°E sensitive to changes in (i) vegetation, which control mammal tax- onomic abundances, diet, and carbon isotopic records from tooth Fig. 1. Map of the study area. (A) Detailed map of fossil exposures (red areas) ii and sites (red circles) and drainages associated with the Nachukui Formation, enamel, soil carbonates, and leaf wax biomarkers; ( ) moisture west of Lake Turkana. (B) Fossil collection sites and formations in the Omo- source, soil temperature, and elevation, which influence oxygen Turkana Basin. (C) Map of Africa with sampling locations for modern teeth isotopic records reflecting meteoric water, such as soil carbonates and meteoric water (white circles) and fossil sites (red circles). and leaf wax biomarkers; and (iii) mammal physiology and be- havior, which affect oxygen isotopic records of individual species. Previous applications of this approach to the African fossil record Nachukui, and Kibish Formations (Fig. 1 and SI Appendix,Fig.S3 have been hampered by uncertainties in the selection of appro- and Tables S2 and S3), that meet the criteria for application of the priate taxa and the unavailability of appropriate fossil collections. aridity index to evaluate long-term changes in paleoaridity in this Aridity is expressed as water deficit (WD), which describes the basin. We also estimate paleoaridity using previously published 18 annual difference (in mm/y) between water loss (evaporation and δ Oenamel values from two eastern African fossil collections out- transpiration) and water gain (precipitation) and is a useful in- side the Turkana Basin that meet the criteria for applying this dicator of water availability in African ecosystems (43, 44). δ18O method, including Aramis, Ethiopia (4.4 Ma), and Kanjera South, values in large mammalian herbivore tooth enamel are in equi- Kenya (2.0 Ma). Finally, we investigate the relationship between librium with body water, which reflects oxygen inputs from food, aridity and structure in eastern Africa using a compi- drinking water, and air, and ultimately relate to meteoric lation of previously published modern mammalian herbivore tis- (precipitation-derived) water (45). In the tropics, the oxygen iso- sue δ13Cvalues(n > 1,600) (25) and a compilation of new and topic composition of meteoric water is related to rainfall amount, previously published fossil tooth enamel δ13Cvalues(n = 658) elevation, and moisture source (46). Evaporation enriches the from fossil collections with paleoaridity estimates. remaining water in the heavy isotope 18O relative to source water, such that aridity can be quantified by comparing one isotopic re- Results and Discussion cord that tracks meteoric water with another that tracks evapora- Terrestrial Aridity Proxy. Across modern localities, WD increases tive enrichment (36, 37). nonlinearly with decreasing mean annual precipitation (logarithmic The aridity index (36) is based on regressions between the WD regression, R2 = 0.7546, P < 0.0001) and increasing mean annual and the oxygen isotopic enrichment between tooth enamel and temperature (quadratic polynomial regression, R2 = 0.6829, P < SI Appendix e local meteoric water (eenamel-mw). Mammalian herbivore taxa for 0.0001) ( ,Fig.S1). enamel-mw values for Hippopot- which eenamel-mw increases with WD are classified as ES, and taxa amidae, Elephantidae, and Rhinocerotidae do not vary with WD, A e for which eenamel-mw does not change with WD are classified as and these taxa are classified as EI (Fig. 2 ). enamel-mw values for EI. Meteoric water cannot be measured directly in the fossil , Hippotragini, and Tragelaphini increase with WD, and record; therefore, these relationships can be extended to the these taxa are classified as ES (Fig. 2B). The slopes of WD-eES-mw fossil record to predict WD by using δ18O values of EI taxa to regressions vary significantly from one another (P < 0.05, F test), P > F represent meteoric water, because eES-EI and eES-mw both track except for Giraffidae and Hippotragini ( 0.05, test). Despite aridity (36). Applying the aridity index to the fossil record re- preliminary observations to the contrary (36), the addition of more quires the assessment of appropriate taxa, geological context, locations in this dataset reveals that Antilopini, , and Neo- diagenetic alteration, and sample size (SI Appendix). tragini should be excluded from the ES category (Fig. 2C). Other To revise the aridity index, we present a compilation of new and sampled bovids, suids, and equids (Fig. 2C) have no significant re- previously published δ18Ovalues(n = 1,224 in 57 species) mea- lationship with WD (P > 0.05), except Cephalophini (P < 0.05), sured on tooth enamel from modern mammalian herbivores from which are not considered further owing to eenamel-mw values that are 37 locations in eastern and central Africa (Fig. 1), along with cli- more variable and/or span a restricted WD range. Additional data 18 mate data and WD estimates for each location and δ Ovaluesin are needed to address the variability in eenamel-mw values across bovid meteoric water (n = 161) from 33 of these locations (SI Appendix, genera, although many bovid fossils are identifiable only to tribe. Table S1 and Datasets S1 and S2). Our compilation significantly We use a body water model to identify possible physiological and 18 expands on a previously published dataset (36) and includes δ O behavioral mechanisms driving the relationship between eenamel-mw data from many more locations and taxa, and also expands the WD andWDamongEIandEStaxa(SI Appendix). A static oxygen scale owing to the correction of a mathematical error in calculating budget, in which body water is influenced solely by changes in the potential evapotranspiration (SI Appendix,Fig.S1). To address isotopic composition of oxygen influxes rather than by changes in paleoaridity in eastern Africa, we present a compilation of new the balance of influxes, is inconsistent with the eenamel-mw values of 18 SI Appendix C D 18 and previously published mammalian herbivore δ Oenamel values either ES or EI taxa ( ,Fig.S2 and ); therefore, O (n = 273) from 26 fossil collections (Fig. 1) ranging in age from enrichment of leaf water in arid environments is insufficient to ∼4.4–0.01 Ma, chosen based on their potential for addressing explain the relationship between eenamel-mw values and WD among paleoaridity and their association with hominin fossil and archaeo- ES taxa. Instead, sensitivity to evaporation is likely related to dif- logical material (SI Appendix, Dataset S3). We use a subset of ferences in drinking behavior and associated changes in the balance 18 δ Oenamel values (n = 160) from 11 fossil collections in the Omo- of oxygen influxes as the environment varies. Predicted eenamel-mw Turkana Basin, including specimens from the Kanapoi, Koobi Fora, values suggest that EI taxa reflect meteoric water as aridity

7332 | www.pnas.org/cgi/doi/10.1073/pnas.1700597114 Blumenthal et al. Downloaded by guest on September 29, 2021 preservation of appropriate ES and EI taxa. Among all fossil col- ABHippopotamidae Elephantidae Giraffidae Tragelaphini 45 45 45 45 lections used to evaluate paleoaridity, we find highly variable condi- 40 40 40 40 tions, including both mesic (WD < 0)andarid(WD> 0) climates 35 35 35 35 that fall within a WD range (∼−550–1,700 mm/y) encompassing enamel-mw enamel-mw 30 30 30 p = 0.002126 p < 0.001 30 r2 = 0.71 r2 = 0.82 ∼61% of the modern range (Fig. 4 and SI Appendix,Fig.S4). The Rhinocerotidae 0 20001000 Hippotragini 0 20001000 mean WD estimated by fossil tooth enamel is 471 mm/y, similar to 45 WD (mm/y) 45 WD (mm/y) the present-day mean WD in eastern and central Africa (251 mm/y; 40 40 P > 0.05) (SI Appendix, Figs. S1 and S4 and Tables S1 and S3). 35 35 enamel-mw enamel-mw p = 0.002041 Among fossil collections from the Omo-Turkana Basin, we detect no 30 30 2 r = 0.71 long-term trend in WD between ∼4.2 and 0.01 Ma (P > 0.05) (Fig. 4). -10000 1000 2000 -10000 1000 2000 WD (mm/y) WD (mm/y) The paleoaridity record (Fig. 4 and SI Appendix,Fig.S4and Tables S2 and S3) begins in the Pliocene with a highly uncertain C estimate of arid conditions associated with ramidus Aepycerotini Alcelaphini Phacochoerus fossilsfromtheLowerAramisMember,SangatoleFormation 45 45 45 45 ∼ 40 40 40 40 ( 4.4 Ma) (47). In the Omo-Turkana Basin, we find arid condi- 35 35 35 35 tions at Kanapoi (∼4.16 Ma) and a highly uncertain estimate of enamel-mw enamel-mw 30 30 30 30 mesic conditions at Allia Bay (∼4.0 Ma), both associated with anamensis (48), and pedogenic carbonate δ13C Antilopini Bovini Hylochoerus 0 20001000 45 45 45 meinertzhageni WD (mm/y) values indicative of vegetation ranging from woodland/bushland/ 40 40 40 shrubland to wooded (49). Mid- to late-Pliocene (∼3.5– 35 35 35 enamel-mw enamel-mw 2.8 Ma) fossil collections in Turkana indicate variable conditions 30 30 30 that include arid (Kangatukuseo KU1) and arid to mesic Cephalophini Neotragini -10000 1000 2000 45 45 (Lomekwi LO4/5) climates, associated with pedogenic carbonate WD (mm/y) 13 40 40 δ C values indicating woody cover, including woodland/bushland/ 35 35 shrubland (Fig. 4) (49). This time interval in Turkana includes

enamel-mw p = 0.04044 30 2 30 r = 0.92 fossils of the hominin genera and .The ∼ – Reduncini 0 20001000 E. burchellii E. grevyi ( 2.5 1.5 Ma) is represented in the Turkana 45 WD (mm/y) 45 45 Basin by fossil assemblages in the upper Burgi Member of the 40 40 40 Koobi Fora Formation as well as the Kaito Member of the 35 35 35 enamel-mw 30 enamel-mw 30 30 Nachukui Formation, which indicate arid (FwJj20 and Kalochoro KL3/6, Naiyena Engol NY2/3), nearly balanced (Kokiselei -10000 1000 2000 -10000 1000 2000 0 20001000 WD (mm/y) WD (mm/y) WD (mm/y) KS2 and Kangatukuseo KU2/3), and mesic (Kokiselei KS1) con- ditions. Pedogenic carbonate δ13C values indicate that relatively e Fig. 2. Isotopic enrichment between enamel and meteoric water ( enamel-mw) open vegetation, including wooded , became more among eastern and central African herbivores. (A) EI taxa. (B) ES taxa. (C)Other prevalent during this time interval in Turkana (49), which includes bovids, equids, and suids. Error bars represent propagated SE of eenamel-mw val- ues. Data are compiled in SI Appendix, Datasets S1 and S2.

Hippopotamidae Elephantidae Rhinocerotidae increases owing to a balance between increasing drinking water and SI Appendix C decreasing food water ( ,Fig.S2 ),andEStaxatrack 15 p = 0.002208 p = 0.05341 p = 0.106 increasing aridity owing to a balance between decreasing drinking r2 = 0.81 10 water and increasing intake of food water and O2, both of which ES-EI are sensitive to evaporation (SI Appendix,Fig.S2D). 5 ANTHROPOLOGY Giraffidae The aridity index reflects the relationship between WD and 0 the enrichment between ES and EI taxa (eES-EI). Significant WD-eES-EI regressions (P < 0.05) that can be used to estimate paleoaridity include e e , p < 0.0001 p < 0.0001 p = 0.0005727 Giraffid-Hippopotamidae, Tragelaphini-Hippopotamidae 15 2 2 2 e , e ,ande r = 0.88 r = 0.8911 r = 0.92 Hippotragini-Hippopotamidae Tragelaphini-Elephantidae Tragelaphini- 10 Rhinocerotidae (Fig. 3 and SI Appendix,TableS4). The SEs of these elaphini ES-EI regression models are relatively low (±193 to ±478.1 mm/y) and 5 g 2 EARTH, ATMOSPHERIC, Tra coefficients of determination are high (R = 0.81–0.92), and thus 0 AND PLANETARY SCIENCES these models have sufficient predictive power to estimate paleo- aridity in the fossil record. Slopes are different among WD-eES-EI P < F p = 0.00711 p = 0.2557 p = 0.188 regressions ( 0.05, test); therefore, a pooled or common 15 r2 = 0.87 ini

slope, as suggested previously (36), is not appropriate. We use the g 10 mean of WD values calculated with WD-eES-EI regressions for all available ES-EI pairs from each fossil collection. Uncertainty in ES-EI 5

WD estimates (∼800 mm/y) corresponds to ∼20% of the WD 0 Hippotra range in modern eastern African environments, sufficient to de- -1000 0 1000 2000 -1000 020001000 -1000 0 1000 2000 tect long-term trends in Turkana (SI Appendix). Other WD-eES-EI regressions are not significant (P > 0.05) and should not be used to WD (mm/y) WD (mm/y) WD (mm/y) estimate paleoaridity. Fig. 3. Isotopic enrichment (eES-EI) between modern ES and EI taxa. eES-EI was 18 calculated using mean δ Oenamel values of sampled ES taxa (rows) and EI taxa Paleoaridity. Our oxygen isotope analyses of fossil tooth enamel (columns) from eastern and central Africa. Dashed lines indicate significant

for paleoaridity estimation were restricted to fossil collections with WD-eES-EI regressions (SI Appendix,TableS4). Error bars represent propagated well-defined stratigraphic and sedimentological context and the SE of eES-EI. Calculated from values provided in SI Appendix, Dataset S2.

Blumenthal et al. PNAS | July 11, 2017 | vol. 114 | no. 28 | 7333 Downloaded by guest on September 29, 2021 A CB D E F

Climate Vegetation Herbivores Hominin behavior and taxa 0 0 sapiens Middle

1 1

Acheulean Paranthropus 2 2 omnivory Age (Ma) early Homo 3 3 Lomekwian butchery? Pliocene australopiths 4 4 habitual bipedality mesic arid closed open 5 5 -2000 0 2000 30 35 40 −10 −5 0 25 50 75 C grazers (%) Water Deficit (mm/y) Temperature (°C) δ13C (‰) 4 pc among APP taxa

Fig. 4. Compilation of data indicating aspects of climate and ecology over the past 5 million years in the Omo-Turkana Basin. (A) Paleoaridity estimates, with error bars indicating age uncertainty and propagated SE of mean WD estimates using all available combinations of ES and EI taxa (SI Appendix, Table S3). (B) 13 Deep lake intervals (62). (C) Paleosol carbonate clumped-isotope temperatures (63). (D) Carbon isotope values of pedogenic carbonates (δ Cpc) (64). There is a 13 2 trend toward increasing δ C values over time (R = 0.2442, P < 0.0001). (E) Percent C4 grazers among Artiodactyla-Perissodactyla- (APP). There is a 2 trend toward including the proportion of C4 grazers over time (R = 0.7391, P < 0.001). (F) Schematic timeline showing the appearance of major hominin behaviors and taxa in eastern Africa (SI Appendix).

an abundant fossil record of Homo and Paranthropus.Mesiccon- case by the scarcity of fossil assemblages meeting the criteria for ditions prevailed at Kanjera South KS-2 in southwestern Kenya, applying the aridity index. We address this problem in three ways. associated with an open grassland ecosystem (50). Archaeological First, we examine the fidelity of long-term environmental records occurrences at Kanjera South, as well as in the Nachukui and derived from the fossil collections used for paleoaridity analy- Koobi Fora Formations in the Turkana Basin, demonstrate that sis. The long-term increase in the proportion of C4 grazers Oldowan tool-making hominins inhabited mesic and arid envi- among Artiodactyla-Perissodactyla-Proboscidea over the ronments. The late Middle Pleistocene to (∼0.2–0.01 Pliocene-Pleistocene in the Omo-Turkana Basin is similar Ma) is represented in the Turkana Basin by fossil assemblages in (P > 0.05, F test) when calculated using tooth enamel δ13C the Kibish Formation, which indicate arid conditions in Member values from paleoaridity fossil collections (R2 = 0.3868, P = 4 and arid to mesic conditions in Member 1. Fossils identified as 0.02324) or from a larger fossil tooth enamel δ13C dataset di- Homo sapiens (Omo I and Omo II) are from Member 1, and other vided into long time bins (>100 ka) (R2 = 0.7391, P = 0.0006911) human specimens are derived from either Member 3 or Member 4. (SI Appendix, Fig. S5). Therefore, it is possible to recover first- WD estimates in Members 1 and 4 are substantially lower than order environmental trends using fossils from these discontinuous those in Turkana today (modern WD = 2,386 mm/y; SI Appendix, depositional intervals. Table S1), consistent with deposition during relatively humid Second, we compare our WD record with previously published periods associated with high lake levels and sapropel formation geological and faunal-based reconstructions of terrestrial paleo- intervals (51). climate in Turkana with varying time representation and analytical biases. There are no trends in paleoclimate based on paleosol Relationships Between Climate and Ecology. To understand the significance of aridity in shaping hominin environments in eastern Africa, we further consider the relationship between climate and ecology in modern African ecosystems. Vegetation in Africa is excluding forests grasslands A all biomes shaped by complex interactions between multiple abiotic (e.g., forests p Modern rainfall amount and seasonality, fire, atmospheric CO2)and 100 100 100 biotic (e.g., herbivory) factors, and the relative importance of these – 80 80 80 factors is contingent on the ecological history of each area (52 54). 60 60 60 Although woody cover is constrained by aridity (55), vegetation 40 40 40 Grazer (%) does not respond in a direct or continuous manner to changes in 20 20 Browser (%) 20 Mixed feeder (%) annual rainfall, and each biome (e.g., forest, , grassland) is 0 0 0 distributed over a wide rainfall range (1,000–3,000 mm/y) (52, 56, 0 2000 0 2000 0 2000 57). We find that among modern eastern and central African 2 WD (mm/y) WD (mm/y) WD (mm/y) ecosystems, the proportion of C4 grazers increases with WD (R = 0.262, P = 0.00536), and the proportion of C3 browsers decreases B Fossil with WD (R2 = 0.1884, P = 0.021) (Fig. 5). These correlations are 100 100 100 weak, however, and during the Pliocene-Pleistocene forests were 80 80 80 rare in the Turkana Basin (25, 27, 49, 58) and elsewhere in eastern 60 60 60 Africa (23). After excluding forests, we find no relationship be- 40 40 40 Grazer (%) 20 20 Browser (%) 20

tween WD and the proportional abundance of each diet guild Mixed feeder (%) 0 0 0 (Fig. 5). Thus, although the abundances of C4 plants and C4 grazing herbivores are often used as an indicators of aridity (21, 30), −2000 0 2000 −2000 0 2000 −2000 0 2000 variation in C4 biomass among nonforest biomes can be decoupled WD (mm/y) WD (mm/y) WD (mm/y) from aridity. 18 Fig. 5. WD (mm/y) and the proportion of C4 grazers, C3-C4 mixed feeders, and Paleoaridity records from δ O of tooth enamel provide a 13 C3 browsers calculated using the average δ C value of each taxon. (A) Modern means to investigate links between climate and ecology in hominin collections in eastern and central Africa. (B) Fossil collections in eastern Africa. environments, but also are highly discontinuous owing to the in- Modern data (51, 65) and fossil data are summarized in SI Appendix,TableS5 completeness of the terrestrial fossil record, compounded in this andcompiledinSI Appendix, Dataset S4.

7334 | www.pnas.org/cgi/doi/10.1073/pnas.1700597114 Blumenthal et al. Downloaded by guest on September 29, 2021 calcic depth, mammal hypsodonty and lophedness (k-nearest- consistent with the notion that biological and behavioral changes in neighbor model), or bovid tribe abundance (SI Appendix,Fig. hominins, including upright posture, hair loss, sweating, and long- S6). Estimated precipitation decreases over time based on mam- distance scavenging or running, may be related to thermophysio- mal community structure (R2 = 0.2295, P = 0.03258) and mammal logical challenges associated with surviving periodically arid con- R2 = hypsodonty and lophedness (linear regression model) ( ditions and high heat loads (58). The relative abundance of C3 0.0583, P = 0.004477), but these trends are weak and based on woody vegetation during the Pliocene (Fig. 4) is consistent with the proxies influenced by evolutionary and dietary changes, re- notion that early bipedal hominins could have relied on areas with spectively, that might not be related to aridity (SI Appendix, shade-providing plants that may have reduced water and heat Fig. S6). Taken together, evidence for marked long-term aridifi- stress. Archaeological occurrences in Turkana during the early cation in the Turkana Basin is weak. Pleistocene (∼2.4–1.4 Ma) are preferentially associated with lower Third, we examine the relationship between WD and ecology in δ13C values of paleosol carbonate compared with those from the fossil record irrespective of time. There are no relationships nonarchaeological deposits, indicating that hominins concentrated (P > 0.05) between WD and the proportion of C4 grazers, C3-C4 SI Appendix their activities in more wooded areas (61). In contrast, archaeo- mixed feeders, or C3 browsers (Fig. 5 and ,TableS4). logical occurrences at Kanjera South in southwestern Kenya Owing to the lack of suitable fossil collections for the application of (2.0 Ma) demonstrate hominins repeatedly using an open grassland our tooth enamel aridity proxy, we do not address climate before (50) when aridity was low (SI Appendix,Fig.S4). Thus, early ∼4 Ma. The appears to have been more humid in hominin land use patterns were likely structured by the interplay Turkana and elsewhere (34), although aridification before ∼4Ma between aridity and vegetation, such that the exploitation of in- predates the long-term increase in C4 vegetation and C4 grazing mammalian herbivore that continued throughout the Pliocene and creasingly open C4-dominated ecosystems may have been limited Pleistocene (25, 27). during periods of high aridity owing to constraints on the availability Despite the coarse time resolution associated with the tooth of water and shade. δ18 enamel O WD calculations, we suggest that the Pliocene- Conclusion Pleistocene expansion in C4 plants and C4 grazing herbivores ap- δ18 pears to not be coincident with significant long-term aridification in Our findings demonstrate how mammal tooth enamel Ovalues the Omo-Turkana Basin (Fig. 4 and SI Appendix,Fig.S6). The can be used to quantify paleoaridity directly associated with the possibility of a smaller long-term increase in aridity, undetected hominin fossil and archaeological record. WD values estimated δ18 owing to uncertainty in WD estimates, cannot be discounted, but from fossil tooth enamel O values suggest that early hominins would not necessarily have been a major environmental driver, experienced highly variable climatic conditions within the range of given that ecological feedback in African biomes inhibits vegeta- present-day environments in the region, and could accommodate tion responses to climate change (52–54). Thus, the cause of the arid conditions as early as ∼4.2 Ma. The modern hyperarid climate major long-term expansion of C4 biomass within Turkana and in Turkana is not a useful analog for paleoaridity in the basin. The elsewhere remains unclear, but may be related to climatic and lack of evidence for marked, long-term aridification, along with the ecological dynamics that are unrelated to annual WD and need not absence of any relationship between aridity and herbivore diet be equivalent across basins or regions (1, 23, 25). Our results do structure, suggest that other abiotic or biotic determinants may not preclude the possibility of climate-driven change in hominin have driven long-term ecological restructuring in the Omo- environments generally, but highlight the need to address possible Turkana Basin. The complex interplay of ecology and behavior variability in the determinants of environmental change in different suggests that disentangling the influence of climate on the evolu- areas, because basins do not necessarily respond in a straightfor- tion of and other mammals remains a significant chal- ward way to continental- and regional-scale aridification. Similarly, lenge. interbasinal and intrabasinal studies are needed to previous paleosol and leaf wax biomarker paleovegetation studies investigate relationships among changing basinal geometry, bio- demonstrate that the timing and magnitude of the expansion of geography, climate, depositional setting, ecology, and evolution. C4 plants is not uniform across eastern and northeastern Africa (23, 27, 59). Thus, climatic and ecological dynamics appear to Materials and Methods ANTHROPOLOGY vary across basins, and regional-scale climate proxies must be Additional details on isotopic and statistical methods, WD calculations, and contextualized by terrestrial, basin-scale environmental records models of leaf water, leaf cellulose, and body water δ18O, along with an ex- most relevant to hominin evolution. panded discussion on criteria for the application of the aridity index, are pro- Our aridity record is consistent with the notion that climate in- vided in SI Appendix. Modern meteoric water samples were compiled from the stability may be an important driver of hominin evolution (2, 30). literature (SI Appendix, Dataset S1). Modern and fossil samples of mammalian Arid conditions were prevalent during two large lake intervals tooth enamel were analyzed for δ18O using standard methods or were com- ∼4.0 and 2.0 Ma (Fig. 4), consistent with climate variability in- piled from the literature (SI Appendix, Datasets S2 and S3). Information on the geological context of fossil specimens is provided in SI Appendix, Dataset S3. cluding periods of increased aridity occurring within generally hu- EARTH, ATMOSPHERIC, mid periods characterized by widespread lake formation (30). AND PLANETARY SCIENCES Orbital-scale environmental change has been demonstrated using ACKNOWLEDGMENTS. This study was made possible by geological and paleontological fieldwork in the Omo-Turkana Basin over the last 50 y. Fossil leaf wax biomarkers from Early Pleistocene lake sediments at collection was done in collaboration with Anna K. Behrensmeyer, David R. Olduvai Gorge, suggesting a direct link between rainfall and Braun, Meave G. Leakey, and the West Turkana Archaeological Project. We changes in the balance of woody and grassy vegetation (28). This thank the National Museums of Kenya, particularly Idle Farah, Emma Mbua, case, and other episodes of climate-driven vegetation change (29, Fredrick Manthi, Purity Kiura, and Mary Muungu, for providing support and 60), are entirely consistent with ecological dynamics in cases where facilitating access to fossil specimens, and other researchers and staff for fossil preparation. We also thank Tom Plummer for reading a previous draft of this woody cover is not constrained by other factors, or when drastic manuscript, and Faysal Bibi and Scott Jasechko for sharing data. Many changes in precipitation, particularly during periods of heightened organizations have offered assistance and access to collections, including the climatic variability, exceed thresholds for stable biome states American Museum of Natural History, the Centre de Recherche en Science otherwise maintained by herbivory, fire, or other factors (44, 53). Naturelles of the Democratic Republic of Congo, the Kenya Wildlife Service, Save the , the Turkana Basin Institute, and the Uganda Wildlife Authority. This research was funded by the Geological Society of America, the Aridity and . Our paleoaridity record demonstrates Leakey Foundation, the National Geographic Society (Grant YEG 9349-13), the that hominins were able to accommodate variable environments National Science Foundation (Grants 0617010, 0621542, and 1260535), Sigma throughout the Pliocene-Pleistocene in eastern Africa, and is Xi, and the Wenner-Gren Foundation (Grant 8694).

Blumenthal et al. PNAS | July 11, 2017 | vol. 114 | no. 28 | 7335 Downloaded by guest on September 29, 2021 1. Levin NE (2015) Environment and climate of early human evolution. Annu Rev Earth 34. Fortelius M, et al. (2016) An ecometric analysis of the fossil mammal record of the Planet Sci 43:405–429. Turkana Basin. Philos Trans R Soc Lond B Biol Sci 371:20150232. 2. Potts R (2013) Hominin evolution in settings of strong environmental variability. Quat 35. Peppe DJ, et al. (2011) Sensitivity of leaf size and shape to climate: Global patterns Sci Rev 73:1–13. and paleoclimatic applications. New Phytol 190:724–739.

3. Bond WJ (2008) What limits trees in C4 grasslands and savannas? Annu Rev Ecol Evol 36. Levin NE, Cerling TE, Passey BH, Harris JM, Ehleringer JR (2006) A stable isotope aridity Syst 39:641–659. index for terrestrial environments. Proc Natl Acad Sci USA 103:11201–11205. 4. deMenocal PB (2004) African climate change and faunal evolution during the Plio- 37. Kohn MJ, Schoeninger MJ, Valley JW (1996) Herbivore tooth oxygen isotope com- cene-Pleistocene. Earth Planet Sci Lett 220:3–24. positions: Effects of diet and physiology. Geochim Cosmochim Acta 60:3889–3896. 5. Shultz S, Maslin M (2013) Early human speciation, brain expansion and dispersal 38. Ayliffe LK, Chivas AR (1990) Oxygen isotope composition of the bone phosphate of influenced by African climate pulses. PLoS One 8:e76750. Australian : Potential as a palaeoenviromental recorder. Geochim Cosmochim 6. Dart RA (1925) Australopithecus africanus: The man- of South Africa. 115: Acta 54:2603–2609. 195–199. 39. Ayliffe LK, Lister A, Chivas AR (1992) The preservation of glacial-interglacial climatic 7. Bramble DM, Lieberman DE (2004) Endurance running and the evolution of Homo. signatures in the oxygen isotopes of skeletal phosphate. Palaeogeogr – Nature 432:345 352. Palaeoclimatol Palaeoecol 99:179–191. 8. Ruxton GD, Wilkinson DM (2011) Avoidance of overheating and selection for both 40. Luz B, Cormie AB, Schwarcz HP (1990) Oxygen isotope variations in phosphate of – hair loss and bipedality in hominins. Proc Natl Acad Sci USA 108:20965 20969. bones. Geochim Cosmochim Acta 54:1723–1728. ’ 9. O Connell JF, Hawkes K, Blurton Jones NG (1999) Grandmothering and the evolution 41. Huertas AD, Iacumin P, Stenni B, Chillión B, Longinelli A (1995) Oxygen isotope var- – of Homo erectus. J Hum Evol 36:461 485. iations of phosphate in mammalian bone and tooth enamel. Geochim Cosmochim 10. Ruff CB (1993) Climatic adaptation and hominid evolution: The thermoregulatory Acta 59:4299–4305. – imperative. Evol Anthropol 2:53 60. 42. Cormie A, Luz B, Schwarcz H (1994) Relationship between the hydrogen and oxygen 11. Tiedemann R, Sarnthein M, Shackleton NJ (1994) Astronomic timescale for the Plio- isotopes of deer bone and their use in the estimation of relative humidity. Geochim δ18 cene O and dust flux records of Ocean Drilling Program Site 659. Cosmochim Acta 58:3439–3449. – Paleoceanography 9:619 638. 43. Thornthwaite CW (1948) An approach toward a rational classification of climate. 12. Larrasoaña JC, Roberts AP, Rohling EJ, Winklhofer M, Wehausen R (2003) Three Geogr Rev 38:55–94. – million years of variability over the northern Sahara. Clim Dyn 21:689 698. 44. Lehmann CER, Archibald SA, Hoffmann WA, Bond WJ (2011) Deciphering the distri- 13. Rossignol-Strick M (1983) African , an immediate climate response to orbital bution of the savanna biome. New Phytol 191:197–209. insolation. Nature 304:46–49. 45. Kohn MJ (1996) Predicting animal δ18O: Accounting for diet and physiological ad- 14. Trauth MH, Larrasoaña JC, Mudelsee M (2009) Trends, rhythms and events in Plio- aptation. Geochim Cosmochim Acta 60:4811–4829. Pleistocene African climate. Quat Sci Rev 28:399–411. 46. Levin NE, Zipser E, Cerling TE (2009) Isotopic composition of waters from Ethiopia and 15. Kingston JD, Deino AL, Edgar RK, Hill A (2007) Astronomically forced climate change Kenya: Insights into moisture sources for eastern Africa. J Geophys Res 114:2–13. in the Kenyan Rift Valley 2.7-2.55 Ma: Implications for the evolution of early hominin 47. White TD, et al. (2009) Macrovertebrate paleontology and the Pliocene habitat of ecosystems. J Hum Evol 53:487–503. Ardipithecus ramidus. Science 326:87–93. 16. Dupont LM, Rommerskirchen F, Mollenhauer G, Schefuß E (2013) Miocene to Pliocene 48. Leakey MG, Feibel CS, McDougall I, Walker A (1995) New four-million--old changes in South African hydrology and vegetation in relation to the expansion of C 4 hominid species from Kanapoi and Allia Bay, Kenya. Nature 376:565–571. plants. Earth Planet Sci Lett 375:408–417. 49. Cerling TE, et al. (2011) Woody cover and hominin environments in the past 6 million 17. Liddy HM, Feakins SJ, Tierney JE (2016) Cooling and drying in northeast Africa across years. Nature 476:51–56. the Pliocene. Earth Planet Sci Lett 449:430–438. 50. Plummer TW, et al. (2009) Oldest evidence of tool-making hominins in a grassland- 18. Bonnefille R (2010) vegetation, climate changes and hominid evolution in dominated ecosystem. PLoS One 4:e7199. tropical Africa. Global Planet Change 72:390–411. 51. Brown FH, McDougall I, Fleagle JG (2012) Correlation of the KHS Tuff of the Kibish 19. Zachos J, Pagani M, Sloan L, Thomas E, Billups K (2001) Trends, rhythms, and aber- Formation to volcanic ash layers at other sites, and the age of early Homo sapiens rations in global climate 65 Ma to present. Science 292:686–693. (Omo I and Omo II). J Hum Evol 63:577–585. 20. Cane MA, Molnar P (2001) Closing of the Indonesian seaway as a precursor to east 52. Staver AC, Archibald S, Levin S (2011) Tree cover in sub-Saharan Africa: Rainfall and African aridification around 3-4 million years ago. Nature 411:157–162. fire constrain forest and savanna as alternative stable states. Ecology 92:1063–1072. 21. Sepulchre P, et al. (2006) Tectonic uplift and Eastern Africa aridification. Science 313: 53. Lehmann CER, et al. (2014) Savanna vegetation-fire-climate relationships differ 1419–1423. – 22. Edwards EJ, et al.; C4 Grasses Consortium (2010) The origins of C grasslands: In- among continents. Science 343:548 552. 4 – tegrating evolutionary and ecosystem science. Science 328:587–591. 54. Oliveras I, Malhi Y (2016) Many shades of green: The dynamic tropical forest savannah 23. Uno KT, Polissar PJ, Jackson KE, deMenocal PB (2016) biomarker record of transition zones. Philos Trans R Soc Lond B Biol Sci 371:20150308. vegetation change in eastern Africa. Proc Natl Acad Sci USA 113:6355–6363. 55. Sankaran M, et al. (2005) Determinants of woody cover in African savannas. Nature – 24. Feakins SJ, Levin NE, Liddy HM, Sieracki A (2013) Northeast African vegetation change 438:846 849. over 12 my. Geology 41:295–298. 56. Guan K, et al. (2014) Terrestrial hydrological controls on land surface phenology of – 25. Cerling TE, et al. (2015) Dietary changes of large herbivores in the Turkana Basin, African savannas and woodlands. J Geophys Res Biogeosci 119:1652 1669. Kenya from 4 to 1 Ma. Proc Natl Acad Sci USA 112:11467–11472. 57. Hirota M, Holmgren M, Van Nes EH, Scheffer M (2011) Global resilience of tropical – 26. Levin NE, Haile-Selassie Y, Frost SR, Saylor BZ (2015) Dietary change among hom- forest and savanna to critical transitions. Science 334:232 235. inins and cercopithecids in Ethiopia during the early Pliocene. Proc Natl Acad Sci 58. Passey BH, Levin NE, Cerling TE, Brown FH, Eiler JM (2010) High-temperature envi- USA 112:12304–12309. ronments of human evolution in based on bond ordering in paleosol 27. Levin NE, Brown FH, Behrensmeyer AK, Bobe R, Cerling TE (2011) Paleosol carbonates carbonates. Proc Natl Acad Sci USA 107:11245–11249. from the Omo Group: Isotopic records of local and regional environmental change in 59. Lüdecke T, et al. (2016) Persistent C3 vegetation accompanied Plio-Pleistocene hom- East Africa. Palaeogeogr Palaeoclimatol Palaeoecol 307:75–89. inin evolution in the Malawi Rift (Chiwondo Beds, Malawi). J Hum Evol 90:163–175. 28. Magill CR, Ashley GM, Freeman KH (2013) Ecosystem variability and early human 60. Bonnefille R, Potts R, Chalié F, Jolly D, Peyron O (2004) High-resolution vegetation habitats in eastern Africa. Proc Natl Acad Sci USA 110:1167–1174. and climate change associated with Pliocene Australopithecus afarensis. Proc Natl 29. Rose C, Polissar PJ, Tierney JE, Filley T, deMenocal PB (2016) Changes in northeast African Acad Sci USA 101:12125–12129. hydrology and vegetation associated with Pliocene–Pleistocene sapropel cycles. Philos 61. Quinn RL, et al. (2013) Pedogenic carbonate stable isotopic evidence for wooded habitat Trans R Soc Lond B Biol Sci 371:20150243. preference of early Pleistocene tool makers in the Turkana Basin. JHumEvol65:65–78. 30. Maslin MA, et al. (2014) East African climate pulses and early human evolution. Quat 62. Lepre CJ, et al. (2011) An earlier origin for the Acheulian. Nature 477:82–85. Sci Rev 101:1–17. 63. Harris JM, Brown FH, Leakey MG, Walker AC, Leakey RE (1988) Pliocene and pleis- 31. Bibi F, Kiessling W (2015) Continuous evolutionary change in Plio-Pleistocene mam- tocene hominid-bearing sites from west of Lake Turkana, Kenya. Science 239:27–33. mals of eastern Africa. Proc Natl Acad Sci USA 112:10623–10628. 64. Robinson JR, Rowan J, Faith JT, Fleagle JG (2016) Paleoenvironmental change in the 32. Bobe R (2006) The evolution of arid ecosystems in eastern Africa. J Arid Environ 66: late middle Pleistocene–Holocene Kibish Formation, southern Ethiopia: Evidence 564–584. from isotopic ecology. Palaeogeogr Palaeoclimatol Palaeoecol 450:50–59. 33. Hernández Fernández M, Vrba ES (2006) Plio-Pleistocene climatic change in the Turkana 65. Brown FH, Fuller CR (2008) Stratigraphy and tephra of the Kibish Formation, south- Basin (East Africa): Evidence from large mammal . J Hum Evol 50:595–626. western Ethiopia. J Hum Evol 55:366–403.

7336 | www.pnas.org/cgi/doi/10.1073/pnas.1700597114 Blumenthal et al. Downloaded by guest on September 29, 2021