Corrections

ANTHROPOLOGY; EARTH, ATMOSPHERIC, AND PLANETARY SCIENCES COMMENTARY Correction for “Stable isotope-based diet reconstructions of Correction for “Stable carbon isotopes and human evolution,” by Turkana Basin hominins,” by Thure E. Cerling, Fredrick Kyalo Richard G. Klein, which appeared in issue 26, June 25, 2013, of Manthi, Emma N. Mbua, Louise N. Leakey, Meave G. Leakey, Proc Natl Acad Sci USA (110:10470–10472; first published June 6, Richard E. Leakey, Francis H. Brown, Frederick E. Grine, 2013; 10.1073/pnas.1307308110). John A. Hart, Prince Kaleme, Hélène Roche, Kevin T. Uno, and The author notes that on page 10470, middle column, first Bernard A. Wood, which appeared in issue 26, June 25, 2013, of paragraph, lines 13 and 16, “∂13C ‰” should instead appear Proc Natl Acad Sci USA (110:10501–10506; first published June as “δ13C ‰.” 3, 2013; 10.1073/pnas.1222568110). Also, on page 10471, middle column, first paragraph, line 3 The authors note that on page 10501, left column, line 13 of “65%” should instead appear as “35%.” the abstract, “ca. 35/65 ratio” should instead appear as “ca. 65/35 Both the online article and the print article have been corrected. ratio.” Both the online article and the print article have been corrected. www.pnas.org/cgi/doi/10.1073/pnas.1311057110

www.pnas.org/cgi/doi/10.1073/pnas.1310815110

10878 | PNAS | June 25, 2013 | vol. 110 | no. 26 www.pnas.org Downloaded by guest on September 23, 2021 COMMENTARY Stable carbon isotopes and human evolution

Richard G. Klein1 ratios show that fossil species after 2 Ma di- Department of Biology, Stanford University, Stanford, CA 94305 vide between grazers and browsers exactly as their anatomical resemblances to living spe- cies would predict (6), which confirms that Paleoanthropologists have long relied on skull enamel is by far the most important. This is the grazer/browser ratio in a fossil site can be and tooth morphology to infer fossil hominin because its density promotes survival, and it used to estimate the relative abundance of diets, but from the early 1980s, they have also resists postdepositional chemical alteration grass vs. bush nearby, or more conservatively, looked to microscopic wear traces in dental (diagenesis). It thus retains the antemortem that differences in grazer/browser ratios be- enamel, and since the early 1990s, they have 13C/12C signal. Enamel that is especially en- tween sites can be used to gauge differences in looked increasingly to the stable isotope riched in 13Cnormallyimpliesadietcom- the abundance of grass vs. bush nearby. composition of skeletal tissues. The most posed largely of grasses or animals, including commonly used stable isotopes are varieties of insects, that eat grasses. Enamel that is sig- Stable Carbon Isotopes in Dental Enamel fi 13 the light elements nitrogen and carbon. Nitro- ni cantly depleted in Cimpliesadietthat and the Diet of Early Hominins gen isotope ratios can provide information included mostly nuts, fruits, leaves, or other Fig. 1 presents the time spans and putative about the degree of carnivory vs. herbivory (1), parts of nongrassy plants or of animals that evolutionary relationships of the hominin but nitrogen can be extracted only from fossil eat such plants. Values are usually expressed species mentioned below. 13 13 bones that retain protein, which means speci- as a departure in Cpermil(=δ C ‰) In paleoanthropology, the first application mens mostly younger than 100,000 y in tem- from an accepted standard, and they have of stable carbon isotope analysis was to South perate latitudes and usually much younger been determined for a variety of African African Australopithecus africanus (∼2.8–2.1 13 than 25,000 y closer to the Equator. In contrast, savanna ungulates (3). ∂ C ‰ in the enamel Ma), Paranthropus robustus (∼2–1.2 Ma), antemortem carbon isotope ratios persist in- of species that feed on C4 grasses commonly and early Homo (∼2 Ma). The results in- definitely in dental enamel (2), and the main ranges between 1.7 and 3.9. In the enamel dicated that the dental enamel of each species limitation is that they reflect ancient diets of species that feed on nongrassy plants, it was relatively enriched in 13C and to about mostly in tropical or subtropical settings where typically ranges between −14.9 and −10.2. the same extent (7, 8). This has been inter- the plants divide subequally between ones that preted to mean that, on average, each species Stable Carbon Isotopes in Dental Enamel follow a C4 photosynthetic pathway and others obtained 25–30% of its carbon from grassy and Early Hominin Environments that follow a C3 pathway. This is not a problem (C4) foods even if it obtained the bulk from In general, stable carbon isotopes reveal only for paleoanthropology, because early homi- berries, nuts, fruits. leaves, or other C3 items. nins (humans broadly understood) evolved what a species selected from the surrounding In contrast, it was recently shown that the in tropical and subtropical Africa, and their vegetation and not the overall vegetational 13 12 enamel of the east African australopith, teeth are preserved in numerous African sites. community. However, if the C/ Cratio Paranthropus boisei (2.3–1.2 Ma), is much Four articles in PNAS show how stable carbon shifts over long intervals in the teeth of spe- richer in 13C, and as stressed below, the de- isotopes have illuminated the diets of homi- cies that were almost certainly grazers, a rea- gree of enrichment implies that it obtained sonable inference is that there was a shift – nins that lived in Africa between roughly 4.1 75 80% of its diet from C4 sources (9). and 1.3 Ma. in the nature of the available grass. Thus, an fi 13 Carbon isotopes cannot pinpoint the speci c increase in C enrichment in grazer enamel grass-based foods that the various species Link Between Carbon Isotopes and across multiple lineages implies that C4 consumed, but significant differences in jaw Ancient Diets grasses spread at the expense of C3 plants in and tooth morphology and in microwear (7) In tropical and subtropical environments, the tropical and subtropical latitudes between suggest that the different species exploited tissues of plants that follow a C4 photo- 8 and 3 Ma (4, 5). This is paleoanthropo- different sources. For A. africanus and P. fi synthetic pathway, mainly grasses and some logically signi cant, because it supports the robustus, the principal ones may have been sedges, tend to be enriched in 13C relative to “savanna hypothesis,” according to which 12 grass seeds, grass roots, the underground C. In contrast, the tissues of plants that hominin bipedalism represents an adaptive storage organs (USOs) of sedges, and ter- follow a C3 pathway, mainly trees, shrubs, response to the increasingly patchy distri- mites, whereas for early Homo,theflesh or bushes, and forbs, tend to be much poorer bution of trees or tree stands vs. grasses in marrow of grazing ungulates may also have 13 in C. The tissues of plants that follow the tropical and subtropical Africa beginning been important. For P. boisei, the principal Crassulacean acid metabolism (CAM) pho- roughly 8 Ma. source may have been especially large quan- tosynthetic pathway, mainly succulents, re- By 2 Ma or so, African savannas closely tities of sedge USOs. The great difference in 13 13 semble C4 plants in C enrichment, but they resembled historic ones and fossil ungulates C enrichment between P. boisei and P. were probably rarely important to early mainly anticipated living ones such as equids robustus was unexpected, because the species hominins, because they occur mostly in (zebras), alcelaphine (wildebeest/hartebeest) are remarkably similar in skull and tooth deserts. Dietary reconstruction depends on antelopes, reduncine (waterbuck/reedbuck) the observation that the 13C/12Cratiosin antelopes, and hippotragine (roan/sable) an- Author contributions: R.G.K. wrote the paper. herbivores reflect the ratios in the plants telopes that feed primarily on C4 grasses they eat, and the ratios in carnivores reflect (grazers) and others such as giraffids and The author declares no conflict of interest. the ratios in their prey. tragelaphine (kudu/bushbuck) antelopes that See companion articles on pages 10495, 10501, 10507 and 10513. 13 12 The C/ C ratio is recorded in various feed primarily on the leaves of C3 bushes, See Inner Workings article on page 10466. 13 12 tissues, but from a fossil perspective, dental shrubs, and trees (browsers). Enamel C/ C 1E-mail: [email protected].

10470–10472 | PNAS | June 25, 2013 | vol. 110 | no. 26 www.pnas.org/cgi/doi/10.1073/pnas.1307308110 H. sapiensH. neanderthalensis Denisovan H. erectus inference requires an enlarged sample of COMMENTARY Ma Ma species 0 0 analyzed teeth. Sponheimer et al. (8) review the principles that allow dietary inferences from stable carbon isotopes. They summarize all of the H. heidelbergensis P. boisei available observations, involving 175 teeth 1 1 from multiple early hominin species between 4.4and1.3Ma,andtheyexplorethelikely relationship between inferred diets and the H. habilis P. robustus Au. H. rudolfensis sediba form of early hominin jaws and teeth. They Homo ergaster suggest that the increased interest in C4 foods 2 2 by australopiths after 4 Ma could largely ex- plain a broadly simultaneous expansion in ? the chewing surfaces of the postcanine (pre- Au. garhi ? Au. africanus molar and molar) teeth and in the thickness Burtele Paranthropus of the mandibular body. They also stress that 3 aethiopicus 3 species the trend toward increasing C4 consumption Au. afarensis after 4 Ma is nearly unique to the hominins. Coeval mammal species remain consistently Kenyanthropus platyops oriented toward C4,C3,ormixedC3/C4 diets. fl 4 Australopithecus 4 The trend in hominins is thus likely to re ect ? anamensis fundamental evolutionary change. ? ? Finally, Cerling et al. (16) report on carbon ? Ar. ramidus isotope ratios in enamel of the extinct gelada baboons Theropithecus brumpti (4-2.5 Ma) 5 5 and Theropithecus oswaldi (2.0–0.9 Ma). Fos- Ardipithecus sils of both species frequently accompany kadabba those of hominins in eastern Africa, especially in Kenya from which Cerling et al. obtained Orrorin ? Sahelanthropus tugensis tchadensis their samples. T. oswaldi is thought to have 6 6 descended from Theropithecus darti, a broad contemporary of T. brumpti in southern Fig. 1. Hypothetical phylogeny of the Hominini. Boldface marks species for which stable carbon isotope observa- Africa, and to have replaced T. brumpti in tions are available. Observations for early Homo have thus far been presented without reference to species. Broken – bars indicate probable as opposed to directly established time spans. eastern Africa after 2.5 2 Ma. Isotope ratios for all three fossil Theropithecus species imply they favored grassy C4 foods, but this was morphology. However, they also differ in previously, the degree in P. boisei was ex- especially true for T. oswaldi,forwhichthe their enamel microwear (9), and the impli- ceptional. Cerling et al. estimate that it con- ratios suggest 80% C4 consumption. The fl cation may be that they did not share an sumed 75% C4 items compared with 35% in difference from T. brumpti may re ect a dif- especially close common ancestor but evolved early Homo,althoughHomo increased its C4 ference in surroundings, because associated their craniodental similarities in parallel. consumption toward 1.5 Ma, perhaps be- mammals suggest that T. oswaldi occupied In PNAS, Cerling et al. (10) report on cause it fed increasingly on the flesh of more open savanna settings. In the degree to stable carbon isotopes in the teeth of homi- grazing ungulates. which extinct geladas favored grassy foods, nins that lived between 4.1 and 1.4 Ma in the Wynn et al. (14) report on stable carbon they anticipate their smaller, surviving rela- Lake Turkana basin of northern Kenya. The isotopes in the teeth of later Australopithecus tive, Theropithecus gelada,whichfeedsalmost results indicate that the oldest species, Aus- afarensis (3.4–2.9 Ma) from localities in the exclusively on grass stems and seeds in the tralopithecus anamensis (4.2–4.0 Ma), rarely Hadar region of north-central Ethiopia. A. central Ethiopian highlands. Among other known primates, living or extinct, only P. consumed C4 foods, even though these were afarensis is generally thought to have probably readily available nearby. In its descended from A. anamensis about 3.8 Ma, boisei approximated the geladas in its C4 emphasis. Geladas evolved unusually high- strong C3 preference, A. anamensis recalls its and it is a likely common ancestor for all putative ancestor, Ardipithecus ramidus (11), hominins that postdate 2.6 Ma, including A. crowned postcanine teeth to masticate large and also the common chimpanzee, which africanus, Paranthropus spp., and Homo. quantities of grassy items. P. boisei may have favors C foods almost exclusively even in Carbon isotope ratios show that later A. evolved unusually large postcanine tooth 3 surfaces for the same purpose. relatively open savanna settings where po- afarensis consumed C4 foods to about the tential C4 foods abound (12). In contrast to same extent as most subsequent hominins, Conclusion the results for A. anamensis,thoseforKen- and A. afarensis is thus the oldest species to Twenty years ago, we might have guessed, yanthropus platyops (3.6–3.0 Ma), which was document the conspicuous dietary divide based mainly on the savanna settings in coeval and possibly conspecific with Ethio- between hominins and chimpanzees. Among which early hominins evolved, that they pian Australopithecus afarensis (13), some- later species, only Australopithecus sediba, depended increasingly on grassy foods or fi times indicate signi cant consumption of C4 dated to about 2 Ma at Malapa Cave, South on creatures that ate grasses. The cranio- foods. The results for Paranthropus aethio- Africa, may have resembled chimpanzees in dental morphology of P. boisei might also – picus (2.6 2.3 Ma) and for sympatric P. boisei a strong preference for C3 foods (15). This have led to us to speculate that it relied on and early Homo (2–1.5 Ma), reveal a persis- may mean it was as peculiar in its diet as grassy foods to a particularly great extent, tent interest in C4 foods, but as noted it was in its anatomy, but secure dietary rivaling only gelada baboons among known

Klein PNAS | June 25, 2013 | vol. 110 | no. 26 | 10471 primates. Now, thanks to stable-isotope research will tell us what early A. afarensis whether different diets distinguished the analyses, we no longer have to guess, and (3.8–3.4 Ma) is likely to have eaten, whether three species of early Homo that are now the broad pattern of early hominin dietary the diet of A. sediba was truly chimpan- thought to have coexisted between 2 and evolution is established. Continuing isotope zee-like, and perhaps most interesting, 1.5 Ma (17).

1 Richards MP, Trinkaus E (2009) Out of Africa: Modern human 6 Cerling TE, Levin NE, Passey BH (2011) Stable isotope ecology in 12 Sponheimer M, et al. (2006) Do “savanna” chimpanzees origins special feature: isotopic evidence for the diets of European the Omo-Turkana Basin. Evol Anthropol 20(6):228–237. consume C4 resources? J Hum Evol 51(2):128–133. Neanderthals and early modern humans. Proc Natl Acad Sci USA 106 7 Grine FE, Sponheimer M, Ungar PS, Lee-Thorp J, Teaford MF (2012) 13 White TD (2003) Paleoanthropology. Early hominids—Diversity or (38):16034–16039. Dental microwear and stable isotopes inform the paleoecology of distortion? Science 299(5615):1994–1997. 2 Lee-Thorp JA, van der Merwe NJ, Brain CK (1989) Isotopic extinct hominins. Am J Phys Anthropol 148(2):285–317. 14 Wynn JG, et al. (2013) Diet of Australopithecus afarensis from evidence for dietary differences between two extinct baboon species 8 Sponheimer M, et al. (2013) Isotopic evidence of early hominin the Pliocene Hadar Formation, Ethiopia. Proc Natl Acad Sci USA from Swartkrans. J Hum Evol 18(3):183–189. diets. Proc Natl Acad Sci USA 110:10513–10518. 110:10495–10500. 3 Cerling TE, Harris JM (1999) Carbon isotope fractionation between 9 Cerling TE, et al. (2011) Diet of Paranthropus boisei in the early 15 Henry AG, et al. (2012) The diet of Australopithecus sediba. diet and bioapatite in ungulate mammals and implications for Pleistocene of East Africa. Proc Natl Acad Sci USA 108(23): Nature 487(7405):90–93. ecological and paleoecological studies. Oecologia 120(3):347–363. 9337–9341. 16 Cerling TE, Chritz KL, Jablonski NG, Leakey MG, Manthi FK 4 Cerling TE, et al. (1997) Global vegetation change through the 10 Cerling TE, et al. (2013) Stable isotope-based diet reconstructions (2013) Diet of Theropithecus from 4 to 1 Ma in Kenya. Proc Natl Miocene/Pliocene boundary. Nature 389(6647):153–158. of Turkana Basin hominins. Proc Natl Acad Sci USA Acad Sci USA 110:10507–10512. 5 Uno KT, et al. (2011) Late Miocene to Pliocene carbon isotope 110:10501–10506. 17 Leakey MG, et al. (2012) New fossils from Koobi Fora in northern record of differential diet change among East African herbivores. Proc 11 White TD, et al. (2009) Macrovertebrate paleontology and the Kenya confirm taxonomic diversity in early Homo. Nature 488(7410): Natl Acad Sci USA 108(16):6509–6514. Pliocene habitat of Ardipithecus ramidus. Science 326(5949):87–93. 201–204.

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