ARTICLE Received 30 Jul 2015 | Accepted 16 Dec 2015 | Published 29 Jan 2016 DOI: 10.1038/ncomms10496 OPEN Human predation contributed to the extinction of the Australian megafaunal bird Genyornis newtoni B47 ka Gifford Miller1,2,3, John Magee4, Mike Smith5, Nigel Spooner6,7, Alexander Baynes8, Scott Lehman1, Marilyn Fogel9, Harvey Johnston10, Doug Williams11, Peter Clark12,z, Christopher Florian1,2, Richard Holst13 & Stephen DeVogel1 Although the temporal overlap between human dispersal across Australia and the disappearance of its largest animals is well established, the lack of unambiguous evidence for human–megafauna interactions has led some to question a human role in megafaunal extinction. Here we show that diagnostic burn patterns on eggshell fragments of the megafaunal bird Genyornis newtoni, found at 4200 sites across Australia, were created by humans discarding eggshell in and around transient fires, presumably made to cook the eggs. Dating by three methods restricts their occurrence to between 53.9 and 43.4 ka, and likely before 47 ka. Dromaius (emu) eggshell occur frequently in deposits from 4100 ka to present; burnt Dromaius eggshell first appear in deposits the same age as those with burnt Genyornis eggshell, and then continually to modern time. Harvesting of their eggs by humans would have decreased Genyornis reproductive success, contributing to the bird’s extinction by B47 ka. 1 Institute of Arctic and Alpine Research, University of Colorado, Boulder, Colorado 80309-0450, USA. 2 Department of Geological Sciences, University of Colorado, Boulder, Colorado 80309-0399, USA. 3 Department of Environment and Agriculture, Curtin University, Perth, Western Australia 6102, Australia. 4 Research School Earth Sciences, Australian National University, Canberra, Australian Capital Territory 2601, Australia. 5 National Museum Australia, GPO Box 1901, Canberra, Australian Capital Territory 2601, Australia. 6 Institute for Photonics and Advanced Sensing and School of Physical Sciences, University of Adelaide, Adelaide,, South Australia 5005, Australia. 7 Defence Science and Technology Group, Edinburgh, South Australia 5111, Australia. 8 Western Australian Museum, Locked Bag 49, Welshpool DC, Western Australia 6986, Australia. 9 School of Natural Sciences, University of California, Merced, 95343 California, USA. 10 Office Environment and Heritage, Box 318, Buronga, New South Wales 2739, Australia. 11 Access Archaeology & Heritage, Box 816, Moruya, New South Wales 2537, Australia. 12 Infrastructure Planning and Natural Resources, Box 363, Buronga, New South Wales 2739, Australia. 13 289 Churchill Avenue, Subiaco, Western Australia 6008, Australia. Correspondence and requests for materials should be addressed to G.M. (email: [email protected]). zDeceased. NATURE COMMUNICATIONS | 7:10496 | DOI: 10.1038/ncomms10496 | www.nature.com/naturecommunications 1 ARTICLE NATURE COMMUNICATIONS | DOI: 10.1038/ncomms10496 ore than 170 years after the discovery of skeletal remains of giant vertebrates preserved in Australian Mcaves1,andlaterindrylakebeds2, the cause of their demise is still debated. Most scientific studies are directed at 0 1,000 2,000 evaluating the two dominant explanations for extinction: human km 3 impact or climate change . As dating methods have improved, B chronologies for human dispersal across Australia and for the GN W Q last surviving megafauna have become more accurate and more E precise4–6. Although the date of initial human arrival on P mainland Australia remains uncertain, populations were PB GA established over most of the continent by at least 47 ka WL D A (refs 6,7). Although many elements of the Australian megafauna (those animals 445 kg body mass) lack firm extinction timelines, last appearance dates for taxa that occur most frequently in the fossil record are between 50 and 40 ka (refs 4,5,8), indicating a temporal overlap between Figure 1 | Regions across Australia from which diagnostic burnt 9 humans and megafauna . The climate of Australia was drying Genyornis eggshell were collected. Map of Australia showing the ten gradually between 60 and 40 ka, but neither the rate nor regions from which burnt Genyornis eggshell fragments have been collected magnitudeofchangeweremoreseverethanduringearlier (solid circles) and one other region where other key samples were collected 10,11 Pleistocene climate shifts . The lack of evidence for (open circle). A: Arumpo Station, NSW; GA: Garnpung Station, NSW; D: unprecedented climate change between 60 and 40 ka and Lower Darling River, NSW; WL: Wallaroo, SA; PB: Port Broughton, SA; P: Port survival of megafauna during earlier more extreme climate Augusta region, SA; E: Lake Eyre, SA; Q: Sites on and around Quobba Station, 12 fluctuations implies that climate change is unlikely to be the WA; GN: Sites on and around Gnaraloo Station, WA; W: Sites on and around sole cause of megafaunal extinction, leaving human agency more Warroora Station, WA; B: Bullara, Ningaloo, and Cardabia stations, WA. likely to have been the decisive factor, with modest additional stress from increasing aridity potentially a contributing factor13,14. Human colonizers may stress megafaunal Diagnostic patterned burning. To test whether blackened egg- populations by predation or by altering habitats so that shell is diagnostic of high temperatures, we sub-sampled partially dietary resources are reduced, with recent studies emphasizing blackened fragments for amino-acid analysis. We found that the the impacts of even modest hunting, especially for long-lived blackened ends had been heated sufficiently to decompose all large vertebrates with low reproductive rates15,16.Althoughthe amino acids, with decreasing decomposition away from the burnt argument for human predation contributing to widespread end, eventually reaching amino-acid concentrations similar to those extinction in Australia is on firm grounds from ecological in unburnt fragments (Fig. 2). Such a strong decomposition gra- theory, little supporting evidence is available in the form of kill dient can only be accomplished if the blackened end was briefly in sites or unambiguous human modification of skeletal remains contact with a localized high-heat-source, likely an ember; rapid despite 50 years of systematic archaeological fieldwork. This lack amino-acid decomposition requires temperatures Z500 °C of evidence has been used to argue against human predation as a (ref. 21). Graded amino-acid decomposition is apparent in transects cause of megafaunal extinction17.Theabsenceofkill across other variably blackened fragments, whereas fully blackened sites in Australia compared with the Americas has been eggshell are devoid of amino acids, consistent with sustained high postulated to be a consequence of the much earlier date for heat over the entire fragment (Supplementary Figs 1 and 2). Australian extinctions, diminishing the probability of their In most collections with burnt eggshell, we found examples preservation4,18,19. Here we provide direct evidence from sites of partially and wholly burnt fragments, some burnt so across most of the continent that humans preyed on at least one severely that their natural curvature was flattened, and element of the Australian megafauna, harvesting eggs of occasionally reversed, as well as many visually unburnt Genyornis newtoni,anextinct,200kgflightlessbird,and fragments. These collections often form a tight cluster o3m leaving diagnostic burnt eggshell fragments as evidence of in diameter without other eggshell nearby, suggesting the source their activities. In the largest series of dates collated for was a single, or small number of eggs. We conclude that natural any Australian megafaunal species, we demonstrate that wildfire could not produce such steep thermal gradients within burnt Genyornis eggshell only occur during a window between and between nearby eggshell fragments, as it requires an 53.9 and 43.4 ka, and likely before 47 ka, documenting untenable combination of circumstances. Rather, these megafaunal predation by humans as they dispersed across the characteristics are most consistent with humans harvesting continent. one or more eggs from a nest, making a fire and presumably cooking the egg. For the same reason that it is possible to boil water in a paper cup over a fire without burning the Results cup, cooking an egg in a manner that does not cause the Genyornis eggshell. Fragments of Genyornis eggshell are found in egg to explode, will not char the eggshell. Records of traditional recently deflated sand dunes where the birds nested, with mor- Aboriginal cooking of emu eggs describe a relatively slow phological features differentiating Genyornis eggshell from those cooking of the eggs, either wrapped in vegetation or in hot ashes of Dromaius (emu)20. We analysed Genyornis eggshell from in a hole dug in the ground for that purpose, from which the egg nearly 2,000 localities across Australia; none is clearly younger would be removed and rotated or shaken frequently, then than 50±5 ka, whereas Dromaius eggshell are commonly found repositioned22. After cooking, we presume that eggshell in the same regions from 4100 ka to the present8. Field studies in fragments were discarded randomly in and around the fire. ten regions across the continent (Fig. 1) yielded 4200 collections We find similarly burnt Dromaius eggshell in unambiguous late that contain variably blackened Genyornis eggshell, frequently Holocene archaeological contexts along with other burnt food blackened at only one end of the fragment, suggestive