COMMENTARY Four million years of African herbivory

Anna K. Behrensmeyer1 community and provide direct evidence for Department of Paleobiology, National Museum of Natural History, Smithsonian Institution, ecological change operating over large tem- Washington, DC 20013 poral and spatial scales. Ecosystem structure is defined in this pa- perastheproportionsofC browsers, C +C The vast African continent is an ecological formation. If the individual is a selective C 3 3 4 3 mixed diets, and C grazers. The authors stage with ever-changing scenery and casts of or C feeder, the enamel records this faith- 4 4 convincingly show that there were many characters that included human ancestors. fully; if it eats a mix of leaves and grass, then C +C mixed feeders in the Turkana Basin The mammals that came and went upon this the isotopic ratio falls in an intermediate 3 4 between 4.3 and 2.3 Ma, a pattern that per- stage have been enlisted to help answer a range. The δ13C data points are compiled sisted for 2 million y. What does this compelling question relevant to our own by taxonomic group and averaged over space imply about the vegetation? Herbivores as evolutionary story: How do land animals (modern ecosystems) or time (fossil-bearing primary consumers depend on plant pro- respond to long-term environmental change? intervals, ∼105 y in this case) to represent ductivity, and more C +C feeders should ThepaperbyCerlingetal.(1)isamilestone larger-scale patterns of G:M:B. The number 3 4 indicate abundant mixes of browse (i.e., di- in this quest. It synthesizes a huge amount of of isotopic values per time interval from the cots) and grass that provided opportunities information on stable carbon isotopes to re- 919 Turkana Basin fossil teeth is variable but for mixed feeding strategies. This suggests a construct the dietary history of three major provides a sound basis for inferring general vegetation structure different from any today herbivore groups over the last 4.3 million y. and raises the question of what could have The study focuses on Kenya’s Turkana Basin, Stable isotope research generated habitats with mixed C and C a prime source of vertebrate fossils and geo- 3 4 is opening up new pos- vegetation but reduced them later (2.3–1.0 Ma) logical information relating to human evolu- and in modern ecosystems. tion. Results from the fossil record are sibilities for ecologists, Causes of past and present ecological interpreted using an even larger sample of isotope geochemists, difference could relate to physical (including isotopic data from modern eastern and cen- and paleontologists to climatic) factors. The Turkana Basin’sfossil tral Africa ecosystems, making this study a record is derived from fluvial, deltaic, and unique comparison of past and present her- collaborate in recon- lake margin environments in a low-altitude bivore adaptations on a changing continent. structing an ancient rift setting. Over the past 4 million y, the The power of carbon isotopes is that they basin has alternated between riverine and can record what an individual animal ate Africa. 12 lacustrine deposition, modulated by drainage during its lifetime via differing ratios of C dietary trends. Taxa previously established as 13 from the Ethiopian highlands (4). Tempera- and C in their tissues, providing informa- dedicated browsers or grazers (2, 3) have tures in the past were similar to those today tion on trophic links between primary pro- consistent C or C isotopic values. There is 3 4 (5), but rainfall was generally higher (6). The ducers and consumers. This insight on no known diagenetic process that would 30 modern tropical ecosystems represented ancient diets is possible because of a rapidly mimic these patterns. The δ13Cdatathus in this study range from mountane to low- expanding collaboration between geochemists, provide a highly credible macroscale view of land and wet to dry, but none matches the ecologists, and paleobiologists. Although herbivore diets over more than 4 million y as Turkana Basin in terms of scale and phys- organic molecules are not well preserved in well as across tropical Africa today. iographic complexity. Physical conditions in most vertebrate fossils, decades of research this basin between 4.3 and 1.0 Ma could have have established that the original biochemical Carbon Isotopes Reveal Nonanalog 13 promoted unique habitats with nonanalog signal is retained in the δ Cvaluesofpre- Herbivore Diets combinations of grass, bush, and trees. This served tooth enamel. The method presented Theimportanceofthisresearchliesnotonly is consistent with soil carbonate δ13C, which in this paper focuses on Artiodactyla (Cetar- in novel interpretations based on massive records woodland and wooded grassland tiodactyla), Perissodactyla, and Proboscidea data compilation and analysis, but also in the vegetation trending toward increased C (APP) and classifies modern and fossil her- ecological and evolutionary questions that 4 13 through time but no pure C grasslands (6). bivores in these groups using δ Cratiosthat emerge from these findings. The authors 4 Of course, biological processes interact with signal a diet of grass (C ), dicots (C ), or a demonstrate that (i) dietary ecology repre- 4 3 physical ones to determine ecosystem struc- mix of the two, expressed as a ratio of grazers: sented by the target groups was different in ture, and diverse mammalian herbivores, es- mixed feeders:browsers (G:M:B). This ratio the past, with more mixed feeders followed pecially larger-bodied APP species, would is examined through time in the Turkana by more nonruminant grazers than occur in have helped shape and sustain mixed C –C Basin and compared with G:M:B for the same African ecosystems today, (ii) some herbi- 3 4 habitats of the Turkana Basin. After 2.3 Ma, groups in modern Central and East Africa. vore lineages shifted their diet over time Before discussing the implications of the whereas others did not, and (iii) the diversity paper by Cerling et al. (1), it is worth consid- of APP taxa was higher in the Turkana Basin Author contributions: A.K.B. wrote the paper. ering how stable isotopes record animal diet of the late Pliocene–Pleistocene than in pre- The author declares no conflict of interest. 13 at different scales. The δ C ratios represent sent-day mammal faunas. These findings See companion article on page 11467. an individual’s diet during the time of tooth record major shifts in the African herbivore 1Email: [email protected].

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climate-driven grassland expansion could have This gives us a new way to view both should take note of this research the wealth COMMENTARY increased competition among mixed feeders, modern and ancient herbivore communities of new isotopic data on herbivore diets + leading to greater segregation of C3 and C4 as an assemblage of C3,C4,ormixedC3 C4 should be seriously considered in light of + vegetation and driving C3 C4 herbivores ex- herbivores and flexible feeders capable of ongoing debates about community dynamics – tinction or greater specialization as browsers major dietary shifts along the C3 C4 spec- and assembly rules. Although these data or grazers. trum over time, presumably as an opportu- may not tell us about population abundances, The extinction of a number of large non- nistic response to changing ecological species of plants consumed, or competitive ruminant grazers between 2.0 and 1.0 Ma conditions. A flexible diet clearly is not the interactions at any given time or place, the indicates a different change in ecosystem only effective survival strategy because spe- paper’s macroscale analysis shows that care- structure. Pedogenic isotope values record cialist C3 and C4 feeders also have many fully constructed datasets open new windows the continuing presence of grasslands (6), long-term success stories. Perhaps it is the on longer-term processes in ecology and but competition with ruminant grazers, combination of these strategies that helped evolution. Many questions emerge from this more extreme seasonality, and changes in the Turkana Basin (and other) species as- work that can stimulate future research. predation pressure could have been operat- semblages persist in the face of ecological What should we make of the apparent dis- ing to limit resources for dedicated grazers. change. The flexible taxa include modern connect between dental morphology and diet A missing piece to this puzzle is what hap- examples that changed from C4 to C3 diets pened with the continuing story of changing during the past million years, hinting at in some herbivore lineages? If these denti- vegetation between 1.0 Ma and today. The times of significantly reduced grassland pro- tions are not indicative of specific diets, how authors suggest that the shift to the modern ductivity or increasing dominance of grazing did natural selection shape them in the first herbivore fauna was abrupt, but a million specialists (including numerous modern place? How can we explain the ability of years is a long time, and faunas from this ruminants) that pushed other APP lineages some taxa to shift their diets whereas others period are still poorly known in East Africa. toward C3 diets or extinction. remain unchanged over time? What hap- There is tantalizing evidence for hyper- The paper in PNAS (1) also draws at- pened to the G:M:B in mammalian faunal hypsodont grazers (7), and it is likely that tention to the lower diversity of APP taxa in assemblages in the last million years as hu- there were multiple shifts between C3-and modern ecosystems. Modern parks in mans became a more effective predator and C4-dominated ecosystems throughout this Kenya, using the best available compila- habitat changer while the amplitude of cli- time, subjecting surviving lineages to ever- tions of mammal richness (10), have 15–16 mate cycles increased (11)? changing pressures for dietary flexibility APP taxa (counting genera and tribes, as in Cerling et al. (1) also are helping to remove or specialization. ref. 1), whereas the total in the Turkana Basin a conceptual roadblock in the search for clues A remarkable aspect of this study is the record reaches a maximum of 20 in the time about the ecology of our ancestors. Hominin isotopic evidence that some APP herbivore interval from 1.9–1.5 Ma. Proboscidea, fossils typically occur in fossil assemblages lineages could adopt different dietary strate- equids, and giraffes show losses at the with grazers, browsers, and mixed feeders, gies over time. Readers should not miss fig- genericlevel,butothergroupsarelittle and this is taken as evidence for mosaic ure S5 in Cerling et al. (1), which provides a changed. The grazing Elephas was the habitats of C3 and C4 vegetation similar to compelling summary of stable vs. changing dominant African proboscidean for millions modern wooded grasslands and woodlands. diets for 20 APP taxa. Previous research of years but went extinct, whereas the sur- Based on the new evidence in this paper, we has shown dietary changes within lineages viving Loxodonta is a flexible feeder that now should question whether modern Africa adapting to the Miocene expansion of C eats mostly C plants but also can incorporate 4 3 provides adequate models for past vegetation vegetation (2, 8), but Cerling et al.’s(1) large amounts of C (e.g., Amboseli National 4 and mammal community structure. Stable findings are the first to offer a detailed Park in ref. 1, dataset S1). This example isotope research is opening up new possibil- analysis of multiple African lineages. No suggests one case in which dietary flexibility longer can we assume that African large may have trumped specialization. ities for ecologists, isotope geochemists, and herbivore diets, at the level of tribes or gen- paleontologists to collaborate in reconstruct- era, have remained constant over time, even New Interdisciplinary Perspectives From ing an ancient Africa with different stage when dental morphology shows little change. Fossil Herbivores sets and roles for herbivores, and perhaps Bovid tribes such as tragelaphines (kudus, Ecologists who question the quality of eco- even different ecological rules, than we see bongo, etc.) were thought to be browsers in logical information from the fossil record operating today. the past, as they are today (1). Elephants with simpler, lower-crowned teeth were regarded Loxodonta 1 Cerling TE, et al. (2015) Dietary changes of large herbivores in the 7 Faith JT, et al. (2012) New perspectives on middle Pleistocene as mixed feeders to browsers ( )as Turkana Basin, Kenya from 4 to 1 Ma. Proc Natl Acad Sci USA change in the large mammal faunas of East Africa: Damaliscus was the brachyodont suid Kolpochoerus,a 112:11467–11472. hypsodon sp. nov. (Mammalia, Artiodactyla) from Lainyamok, Kenya. relative of the modern giant forest hog (9). 2 Uno KT, et al. (2011) Late Miocene to Pliocene carbon isotope Palaeogeogr Palaeoclimatol Palaeoecol 361–362:84–93. δ13 record of differential diet change among East African herbivores. Proc 8 Badgley C, et al. (2008) Ecological changes in Miocene The C isotope research has upended many Natl Acad Sci USA 108(16):6509–6514. mammalian record show impact of prolonged climatic forcing. Proc of these assumptions by showing that the 3 Cerling TE, Levin NE, Passey BH (2011) Stable isotope ecology in Natl Acad Sci USA 105(34):12145–12149. same tooth morphology can work with very the Omo-Turkana Basin. Evol Anthropol 20(6):228–237. 9 Behrensmeyer AK, Bobe R, Alemseged Z (2007) Approaches 4 Feibel CS (2011) A geological history of the Turkana Basin. Evol to the analysis of faunal change during the East African Pliocene. different diets, even over millions of years. Anthropol 20(6):206–216. Hominin Environments in the East African Pliocene: An Dietary flexibility with respect to C3 and C4 5 Passey BH, Levin NE, Cerling TE, Brown FH, Eiler JM (2010) High- Assessment of the Faunal Evidence, eds Bobe R, Alemseged Z, temperature environments of human evolution in East Africa based Behrensmeyer AK (Springer, Dordrecht, The Netherlands), forage was (and is) an important strategy for on bond ordering in paleosol carbonates. Proc Natl Acad Sci USA pp 1–24. large herbivores dealing with habitat change, 107(25):11245–11249. 10 Tóth AB, Lyons SK, Behrensmeyer AK (2014) Mammals whether caused by climate, biological pro- 6 Levin NH, Brown FH, Behrensmeyer AK, Bobe R, Cerling TE (2011) of Kenya’s protected areas from 1888 to 2013. Ecology Paleosol carbonates from the Omo Group: Isotopic records of local 95(6):1711. cesses (e.g., competition), or accelerating and regional environmental change in East Africa. Palaeogeogr 11 deMenocal PB (2011) Anthropology. Climate and human impact. Palaeoclimatol Palaeoecol 307:75–89. human evolution. Science 331(6017):540–542.

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