Megaherbivore extinctions in Africa Human ancestors have been proposed as drivers of extinctions of Africa's diverse large mammal communities. Faith et al. challenge this view with an analysis of eastern African herbivore communities spanning the past ∼7 million years (see the Perspective by Bobe and Carvalho). Megaherbivores (for example, elephants, rhinos, and hippos) began to decline about 4.6 million years ago, preceding evidence for hominin consumption of animal tissues by more than 1 million years. Instead, megaherbivore decline may have been triggered by declining atmospheric carbon dioxide and expansion of grasslands. Science, this issue p. 938; see also p. 892

Abstract It has long been proposed that pre-modern hominin impacts drove extinctions and shaped the evolutionary history of Africa’s exceptionally diverse large mammal communities, but this hypothesis has yet to be rigorously tested. We analyzed eastern African herbivore communities spanning the past 7 million years—encompassing the entirety of hominin evolutionary history—to test the hypothesis that top-down impacts of tool-bearing, meat-eating hominins contributed to the demise of megaherbivores prior to the emergence of Homo sapiens. We document a steady, long-term decline of megaherbivores beginning ~4.6 million years ago, long before the appearance of hominin species capable of exerting top-down control of large mammal communities and predating evidence for hominin interactions with megaherbivore prey. Expansion of C 4 grasslands can account for the loss of megaherbivore diversity.

Africa is home to more species of large-bodied mammalian herbivores than anywhere else today (1). Because most of the world’s large-bodied vertebrates became extinct toward the end of the Pleistocene (2), present-day African faunas serve as model systems for understanding the ecology of large mammal communities (3) and the impact of massive megaherbivores (>1000 kg) on ecosystems (4). Such knowledge feeds directly into conservation biology on a global scale by highlighting the ecological consequences of ongoing large mammal diversity loss (1) and illustrating the potential consequences of their rewilding (5).

There is a perception that Africa’s exceptional large herbivore diversity is due to the continent being spared the extinctions that occurred elsewhere as modern humans (Homo sapiens) dispersed across the world in the past 100,000 years (2). This anomaly has been thought to reflect coevolution of hominin hunters and their prey (6) or perhaps a long history of extinctions precipitated by pre-modern hominins (7) in Africa. Indeed, for decades it has been suggested that hominins drove extinctions and shifts in the functional structure of large mammal communities throughout the Pleistocene (7–13). Many of these hypotheses posit that top-down control of mammal communities by tool-bearing, meat-eating hominins contributed to the demise of large-bodied herbivores (e.g., the formerly diverse Proboscidea) long before the emergence of Homo sapiens (7, 9, 11, 12). Other versions of the “ancient impacts” hypothesis propose that encroachment of Early Pleistocene Homo into the carnivore guild led to the demise of several carnivoran lineages (8, 10), perhaps leading to environmental changes through relaxed predation pressure on large-bodied herbivores (10). Both scenarios imply that ancient hominins played a key role in shaping African ecosystems, and by extension the environmental settings that influenced our own evolutionary history.

Despite decades of literature asserting ancient hominin impacts on African faunas, there have been few attempts to test this scenario or to explore alternatives. Here, we tested the hypothesis of top-down hominin impacts on mammal communities through the analysis of megaherbivore diversity over the past 7 million years (Ma) in eastern Africa. Our focus on this region reflects its rich and well-dated late Cenozoic fossil record, coupled with the fact that the earliest known members of the hominin clade are from eastern Africa, which therefore provides the longest well-documented history of hominin-mammal community interactions in the world. On the basis of previous hypotheses (7–13), we expect declines in megaherbivore community richness to follow or temporally coincide with hominin expansion into carnivore niche space. Specifically, proponents of the ancient impacts hypothesis typically place the onset of anthropogenic diversity decline between 2 and 1 Ma ago (7, 8, 10–12). This encompasses the earliest evidence for systematic hominin predation upon large-bodied mammals (~2 Ma ago) (14) and megaherbivores (~1.95 Ma ago) (15), as well as the appearance of Homo erectus (~1.9 Ma ago), the first hominin species whose paleobiology is similar to later representatives of our genus and that consumed large amounts of animal tissue (16). These evolutionary changes are thought to account for an unprecedented reduction of megaherbivore diversity coupled with collapse of the large carnivore guild (7, 8, 10–12).

We used present-day and fossil herbivore community data to quantify long-term changes in the richness of eastern African megaherbivores (17). A dataset of more than 200 modern communities from protected areas across Africa allowed us to establish a baseline for present-day variability in megaherbivore community richness (Fig. 1A, table S1, and data S1). In addition, we compiled a fossil dataset that includes the presence of herbivore taxa in 101 eastern African fossil assemblages spanning the past ~7 Ma (table S2 and data S2), a period that encompasses the earliest probable and definitive hominin species in eastern Africa. Our focus on individual fossil assemblages within a single region provides a pertinent spatiotemporal scale for our research question because it allows a more direct assessment of hominin impacts on ancient herbivore communities than is possible from analyses of species occurrences at continental scales [e.g., (9)]. Because hominin impacts need not be the only driver of change in the eastern African megaherbivore community, we also examined trends in megaherbivore community richness relative to independent records of climatic and environmental change. These include global atmospheric partial pressure of CO 2 (pCO 2 ) (18), the percentage of C 4 biomass (e.g., tropical grasses) inferred from the stable carbon isotope (δ13C) composition of soil carbonates in eastern Africa (19), estimates of paleo-aridity derived from the stable oxygen isotopes (δ18O) of eastern African fossil herbivores (20), and the percentage of C 4 grazers among ungulate taxa in eastern African fossil assemblages (20). The eastern African proxy data come from many of the same sites examined in our analysis of megaherbivore diversity.

Fig. 1 Megaherbivore richness in modern and fossil communities. (A) Geographic distribution of the 203 modern (continental map) and 101 fossil (inset map) herbivore communities. (B) Relationship between the total number of herbivore species and the proportion of megaherbivore species in modern African communities and eastern African fossil assemblages. The solid line represents the maximum proportion of megaherbivores that could coexist today, based on the empirical observation of at most five sympatric megaherbivore species. Fossil assemblages falling above the line are non-analog because they include a greater proportion of megaherbivores than is observed today. (C) Megaherbivore richness residuals over the past 7 Ma, illustrating the long-term decline of megaherbivores starting ~4.6 Ma ago. Data points represent residuals from the least-squares regression modeling the relationship of megaherbivore richness as a function of total community richness in the modern communities (fig. S2). The solid gray line represents LOESS (locally estimated scatterplot smoothing) regression with smoothing factor = 0.75; 95% confidence limits are shown in light gray. Horizontal dashed lines encompass the middle 95% range of variation in the modern communities.

Our compilation of the eastern African fossil record reveals substantial megaherbivore extinctions through time. Over the past 7 Ma, 28 megaherbivore lineages became extinct (table S3), leading to present-day communities that are depauperate in megaherbivores. For example, modern African herbivore communities include only up to five sympatric megaherbivores (data S1), including all of the extant species (Giraffa camelopardalis, Hippopotamus amphibius, Ceratotherium simum, Diceros bicornis, and Loxodonta africana). In contrast, the fossil record documents paleocommunities that were considerably richer in megaherbivores, with some assemblages documenting the co-occurrence of as many as 10 megaherbivore species (data S2). Although time-averaging of fossil assemblages can produce associations of species that never spatiotemporally co-occurred, it cannot account for the exceptional richness of megaherbivores here (17) (fig. S1). Controlling for community richness, a variable that increases as a function of time-averaging and sampling effort, many fossil assemblages over the past ~7 Ma fall outside the modern range of variation because they include both a greater proportion and a greater absolute number of megaherbivore species (Fig. 1, B and C).

To illustrate temporal trends (Fig. 1C), we calculated residuals for fossil assemblages as deviations from expected megaherbivore richness modeled as a linear function of herbivore community richness based on our modern community data (fig. S2). Residual analysis highlights the exceptional richness of fossil megaherbivore communities—many are well outside the modern range of variation—and documents a steady and long-term decline in richness beginning in the early Pliocene, with fossil assemblages consistently falling within the modern range of variation only after ~0.7 Ma ago (Fig. 1C). Breakpoint analysis places the onset of the megaherbivore decline at ~4.6 Ma ago (95% confidence interval, 3.3 to 5.9 Ma ago). After the ~4.6 Ma breakpoint, the rate of diversity decline through time does not change following the appearance of Homo erectus (1.9 Ma ago) or at either end of the hypothesized window of accelerated anthropogenic diversity decline, 2 to 1 Ma ago (table S4). Instead, the long-term decline in megaherbivore richness closely tracks global variation in atmospheric pCO 2 as well as the expansion of C 4 grasslands and C 4 grazers in eastern Africa, although there is no association with paleo-aridity (Fig. 2).

Fig. 2 The decline of megaherbivore richness relative to climatic and environmental proxies. (A) Global pCO 2 . (B) Percentage of C 4 vegetation inferred from δ13C of eastern African paleosol carbonates. (C) Estimates of water deficit (aridity) for eastern African fossil sites based on δ18O of herbivore tooth enamel. Error bars represent SE of the mean water deficit estimates. (D) Percentage of C 4 grazers among herbivore taxa (Artiodactyla-Perissodactyla-Proboscidea) from eastern African fossil sites, calculated as the percentage of taxa with mean enamel δ13C values > –1 per mil. The gray line in all panels represents the LOESS regression (95% confidence limits in light gray) for megaherbivore richness residuals, as in Fig. 1C.

The loss of large-bodied mammals is thought to be a hallmark of anthropogenic extinctions (6, 7, 9), in part because large-bodied species are likely to have been preferentially targeted by hominin hunters and because their slower life history profiles (e.g., delayed reproductive maturity, prolonged gestation, low population growth rates) render them more susceptible to extinction. Our analyses show that the diversity of megaherbivores in eastern African fossil assemblages has undergone a steady decline since ~4.6 Ma ago (Fig. 1), beginning long before the proposed timing of anthropogenic impacts (2 to 1 Ma ago) linked to encroachment of Homo erectus into the carnivore guild (Fig. 3). The antiquity of the megaherbivore decline effectively eliminates top-down hominin impacts as a plausible mechanism for setting it in motion, as it would have had to involve small-bodied australopiths or pre-australopiths (e.g., Australopithecus, Ardipithecus), which were functionally equivalent to bipedal apes. Like extant chimpanzees, these hominin taxa may have preyed upon vertebrate species smaller than themselves, but they almost certainly did not hunt megaherbivore prey (21). Although we cannot rule out the possibility that the subsequent appearance of more derived hominin species, new stone-tool technologies, and increased carnivory may have incidentally contributed to the demise of megaherbivores, the steady decline of megaherbivores beginning ~4.6 Ma ago (Fig. 3 and table S4)—in contrast to proposed extinction pulses linked to major shifts in hominin evolution (7)—implies that the primary driver was decoupled from hominin evolution.

Fig. 3 The decline of megaherbivore richness relative to milestones in hominin evolution. These include the appearance of novel technologies and behaviors, as well as the observed temporal ranges of eastern African hominin taxa. The vertical dashed line indicates the breakpoint denoting onset of megaherbivore decline (4.6 Ma ago), with red shading representing the 95% confidence interval (3.3 to 5.9 Ma ago).

We propose that the expansion of C 4 grasslands (Fig. 2B) played a critical role in megaherbivore decline. Analysis of our fossil dataset indicates that the long-term decline of megaherbivores is primarily due to the loss of megaherbivore browsers and mixed feeders that consumed C 3 plants, including trees, shrubs, and herbs (fig. S3). Unlike megaherbivore grazers, temporal declines in the richness of megaherbivore browsers and mixed feeders are in close agreement with the overall megaherbivore diversity loss (fig. S3). Loss of C 3 consumers is also evident in a compilation of δ13C data from tooth enamel of eastern African megaherbivores (fig. S3 and data S3). Their decline in fossil assemblages is likely related to the Plio-Pleistocene expansion of C 4 grasslands (Fig. 2B), which reduced the availability of C 3 forage on the landscape. Because larger-bodied species are more strongly limited by forage availability than smaller-bodied species (4), a decline in megaherbivore species dependent on C 3 forage is expected. At the same time, decreasing atmospheric CO 2 concentrations (Fig. 2A) would have diminished the advantage of massive body size, which allows megaherbivores to consume lower-quality foods than their smaller-bodied counterparts (4). Especially among C 3 plant species, plant tissue grown at lower CO 2 concentrations provides higher-quality forage because such plants have higher N content (lower C:N ratios) and fewer secondary compounds (22). This would allow smaller-bodied species—which are restricted to high-quality forage (3)—to exploit a greater range of increasingly rare C 3 resources, with the outcome being less food available to megaherbivore browsers and mixed feeders. Some or all of these mechanisms are likely to have played a role in driving large herbivore extinctions elsewhere. For example, although the timing of C 4 expansion and the nature of its ecological consequences varied globally as a result of differences in climate and historical contingencies (23), the C 4 expansion in the Siwalik Group (Pakistan) from ~8.5 to 6.0 Ma ago is associated with considerable losses among C 3 consumers and the last appearances of many massive herbivores, including five rhino species, a proboscidean, a chalicothere, and a sivathere (24).

There is a long history of debate concerning the mechanisms responsible for the expansion of C 4 grasslands in eastern Africa (19). This phenomenon is often linked to increased aridity after the onset of Northern Hemisphere Glaciation, ~2.8 Ma ago (25). However, dust flux records from marine sedimentary archives that reflect eastern African climate indicate substantial long-term increases in aridity only after ~1.5 Ma ago (26), long after the onset of C 4 expansion (Fig. 2B). In addition, recent analyses show that terrestrial proxies for aridity and vegetation in eastern Africa vary independently through the Plio-Pleistocene, implying that other abiotic or biotic mechanisms likely underpin habitat change (20). Because C 4 grasses are favored at lower CO 2 concentrations (27), the Plio-Pleistocene CO 2 decline (Fig. 2A) is likely an important abiotic mechanism (19). For example, at high temperatures, such as those inferred from Turkana Basin paleosol carbonates (>30°C) (28), C 4 grasses are expected to expand when atmospheric CO 2 concentrations fall below ~450 parts per million (27). The expansion of C 4 grasslands and associated decline of megaherbivores are consistent with long-term decline of CO 2 (Fig. 2), likely facilitated by episodes of aridity (i.e., positive water deficit) that occurred across the interval (Fig. 2C). The persistent expansion of C 4 grasslands is remarkable in light of the decline of megaherbivore diversity. Megaherbivore browsers and mixed feeders, especially elephants (L. africana) and black rhinoceros (D. bicornis), promote grassland expansion through consumption of woody (C 3 ) vegetation, toppling and ringbarking of trees, and synergistic effects with fire (4, 29). With all other factors held constant, we would expect the considerable decline of such taxa—which implies a reduction in megaherbivore biomass (fig. S4)—to drive an expansion of woody cover through the Plio-Pleistocene. That the exact opposite occurred (Fig. 2B) suggests a dominance of abiotic mechanisms in driving the C 4 expansion.

We note that the CO 2 -driven expansion of C 4 grasslands and the associated extinction of megaherbivores can account for other changes in eastern African mammal communities that have been attributed to ancient hominin impacts. As noted earlier, the loss of richness and functional diversity among eastern African carnivorans through the Pleistocene has been attributed to the encroachment of Homo into the large carnivore guild (8, 10–12). However, some extinct Pleistocene carnivorans lacking modern analogs (e.g., sabertooth felids) are known to have specialized on juvenile megaherbivores (30). Given the close association between large carnivore diversity and herbivore diversity (31), the loss of megaherbivore prey likely contributed directly to the extinction of attendant carnivores. Thus, in the absence of detailed consideration of eastern African herbivores, it is premature to invoke hominin impacts as an important driver of carnivoran diversity loss and associated ecosystem change. Together with our observations indicating that bottom-up processes can account for the loss of megaherbivores, it follows that in the search for anthropogenic impacts on ancient African ecosystems, we must focus our attention on the one species known to be capable of causing them: Homo sapiens over the past 300,000 years.

Supplementary Materials www.sciencemag.org/content/362/6417/938/suppl/DC1 Materials and Methods Figs. S1 to S4 Tables S1 to S4 Data S1 to S3 References (32–149)

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