Climate Change Frames Debate Over the Extinction of Megafauna in Sahul (Pleistocene Australia-New Guinea) Stephen Wroea,B, Judith H

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PERSPECTIVE PERSPECTIVE Climate change frames debate over the extinction of megafauna in Sahul (Pleistocene Australia-New Guinea) Stephen Wroea,b, Judith H. Fielda,1, Michael Archera, Donald K. Graysonc, Gilbert J. Priced, Julien Louysd, J. Tyler Faithe, Gregory E. Webbd, Iain Davidsonf, and Scott D. Mooneya aSchool of Biological, Earth, and Environmental Sciences, University of New South Wales, Sydney, NSW 2052, Australia; bSchool of Engineering, University of Newcastle, NSW 2308, Australia; cDepartment of Anthropology and Quaternary Research Center, University of Washington, Seattle, WA 98195; dSchool of Earth Sciences, The University of Queensland, St. Lucia, QLD 4072, Australia; eSchool of Social Science, The University of Queensland, St. Lucia, QLD 4072, Australia; and fSchool of Humanities, University of New England, Armidale, NSW 2351, Australia

Edited by James O’Connell, University of Utah, Salt Lake City, UT, and approved April 9, 2013 (received for review February 12, 2013)

Around 88 large vertebrate taxa disappeared from Sahul sometime during the Pleistocene, with the majority of losses (54 taxa) clearly taking place within the last 400,000 years. The largest was the 2.8-ton browsing Diprotodon optatum, whereas the ∼100- to 130-kg marsupial lion, Thylacoleo carnifex, the world’s most specialized mammalian carnivore, and Varanus priscus, the largest lizard known, were formidable predators. Explanations for these extinctions have centered on climatic change or human activities. Here, we review the evidence and arguments for both. Human involvement in the disappearance of some species remains possible but unproven. Mounting evidence points to the loss of most species before the peopling of Sahul (circa 50–45 ka) and a signiﬁcant role for climate change in the disappearance of the continent’s megafauna.

megafauna extinction | Pleistocene extinctions | archaeology | human colonization | faunal turnover

Explaining Pleistocene faunal extinctions 2], ∼28–19 ka, that the first people crossed bandicoots, dasyurids, and rodents (27), also remains one of the most challenging prob- the biogeographic divide (Wallacea) to enter occurred. Furthermore, a range of medium- lems in the prehistory of Sahul (1–3). The Sahul at ∼50–45 ka (15, 16). It seems likely and small-bodied species disappeared or vast majority of extinctions across geological that the size, distribution, and density of hu- underwent major geographic range shifts on time are wholly attributable to climate- man populations in pre-LGM times have time frames similar to those of larger taxa related factors (4), but claims that some, or been overestimated (17), although these (28–33). Also notable is the fact that not all even all, Pleistocene extinctions of large- were evidently behaviorally modern people megafauna went extinct: Some underwent gigantic vertebrates (Fig. 1) in Sahul were the (18, 19). dwarfing, whereas others appear to have consequence of human activity have gen- survived relatively unchanged, such as emus, Late Pleistocene Fauna and Extinction erated particularly robust debate. Polarized cassowaries, wombats, salt-water crocodiles, views have emerged to account for the mode Chronologies and many species of large kangaroos, in- As commonly used in the context of extinc- and timing of these events (2, 5–11). A pau- cluding reds (Macropus rufus), grays (Mac- tions in Sahul, the term megafauna refers to city of empirical data; shortfalls in radiomet- ropus giganteus and Macropus fuliginosus), an arbitrary compilation of relatively large ric dating; and, until recently, a limited and wallaroos (Macropus robustus, Macropus mammalian, reptilian, and avian taxa, rang- appreciation of the paleoenvironmental re- antilopinus,andMacropus bernardus). Taxa ing in size from ∼10 kg or less up to >2,000 kg fromthewholegamutofbodysizedis- cord (7, 12) have placed considerable con- (20–23). In addition to Diprotodon opta- tributions, not just the largest, were affected straints on the ability to resolve “who or tum and Thylacoleo carnifex (Fig. 1), other by extrinsic factors during the Pleistocene. what” was responsible for these extinctions. well-known marsupial “giants” included the Only some of these factors led to extinctions. Given these limitations, assertions such as “... 230-kg kangaroo Procoptodon goliah (24), There is no reason to assume that all species the question is no longer if, but rather how, the tapir-like Palorchestes azael,andthe lumped together as extinct megafauna were humans induced this prehistoric extinction bull-sized Zygomaturus trilobus.Among ” event (ref. 13, p. 563) are premature. nonmammalian megafaunal species were — Author contributions: S.W. and J.H.F. designed research; S.W., J.H.F., Sahul mainland Australia, Tasmania, the massively built flightless bird Genyornis — ∼ G.J.P., and J.L. performed research; G.J.P., J.L., J.T.F., and S.D.M. and New Guinea comprised up to 11 mil- newtoni (25), the anaconda-like madtsoiid 2 analyzed data; and S.W., J.H.F., M.A., D.K.G., J.T.F., G.E.W., I.D., lion km at glacial maxima. Although domi- snake Wonambi naracoortensis,andthe and S.D.M. wrote the paper. nated by an expansive desert core (14), 5-m-long mekosuchine crocodile Pallim- The authors declare no conflict of interest.

environments ranged from periglacial in Tas- narchus pollens (26). This article is a PNAS Direct Submission. mania to tropical in New Guinea (Fig. 2). It It is important to note that extinctions in 1To whom correspondence should be addressed. E-mail: judith. was against a backdrop of deteriorating con- Pleistocene Sahul were not restricted to the ﬁ[email protected]. ditions leading up to the Last Glacial Maxi- large-bodied species described above. Extinc- This article contains supporting information online at www.pnas.org/ mum [LGM; in Marine Isotope Stage (MIS) tions of small-bodied species, including frogs, lookup/suppl/doi:10.1073/pnas.1302698110/-/DCSupplemental.

www.pnas.org/cgi/doi/10.1073/pnas.1302698110 PNAS | May 28, 2013 | vol. 110 | no. 22 | 8777–8781 Downloaded by guest on September 26, 2021 explanation of the data are that the extinc- megafauna disappeared (6). Modeling studies tions were indeed staggered over a period based on the same dataset suggested that that began long before human arrival. A human activities could have accounted for staggered extinction event is further sup- the decline and disappearance of all mega- ported by recent rigorous statistical tests of fauna within 600 y (39). Various publications stratigraphically intact prehuman fossil se- before and since have offered proxy data to quences (Fig. 4) that show progressive support the notion of a primary human role losses of diversity over time (12), strongly (8, 40). suggesting that temporally progressive mid- Human activities as a primary extinction dle to late Pleistocene declines in diversity driver are not, however, supported by the are not sampling artifacts. paleontology or the archeology. The com- Extinctions of a comparable magnitude to plete lack of evidence for predation on, or Fig. 1. Thylacoleo carnifex, the 100- to 130-kg mar- those of megafauna have been observed for even consumption of, megafauna by people supial lion with massive “bolt cutter-like” cheek teeth and small-bodied species in a range of specific aside, the extinction window noted above is the most powerful bite for its size of any mammalian localized studies. For example, small-sized based on a statistical analysis of just seven carnivore, was a formidable predator of large animals. < (Drawing by Peter Schouten.) species ( 3 kg) from Mount Etna in north- sites(7).Fourofthesehavenopublisheddata eastern Australia (Fig. 2) experienced a 50% and cannot be scrutinized. A fifth site, reduction in species richness (from 28 to 35 Menindee Lake (Fig. 2), is 10,000 y younger sufficiently similar ecologically or entangled species to 16 to 12 species) over the course than originally proposed but still 10,000 y (or contemporaneous, see below) to enable of the middle to late Pleistocene (35). These older than the archeological materials from one simultaneous event to account for all losses track progressive environmental change thesamesite(7).Theremainingtwolocali- > these extinctions. from rainforest to less mesic habitats. Like- ties are 100 ka in age (7), and thus earlier ThelastappearancedatesinSahulforthe wise, the eastern Darling Downs records than the arrival of people by at least 50,000 y. suite of taxa traditionally referred to as mega- middle to late Pleistocene extinctions among Only two sites in Sahul have secure exca- fauna are consistent with a staggered extinc- both small- and large-bodied species con- vated contexts with co-occurrence of extinct tion process that was in train well before comitant with progressively drying envi- megafauna and people: Cuddie Springs in the arrival of humans (3, 10, 12) (Fig. 3). In- ronments (30–33). southeastern Australia and Nombe Rock- cluding new middle Pleistocene species re- shelter in the New Guinea highlands (7, 34) corded from south-central Australia (2), as Human-Mediated Extinction Processes (Fig. 2). Two other sites have yielded evi- many as 50 of the 88 known extinct mega- The argument for a primary human role in dence for single instances of megafauna faunal taxa are absent from fossil records the extinction of megafauna has been based persisting after the LGM. These fauna were postdating the Penultimate Glacial Maxi- on the presumption that the arrival of identified in archeological sites but were re- mum (PGM; MIS6) (3) at ∼130ka(Fig.3and humans on Sahul was synchronous with the covered from noncultural (prehuman) hori- Table S1). Additional taxa disappeared at disappearance of all now-extinct megafauna zons (Cloggs Cave and Seton Rockshelter) ∼85–80ka(3,6,12).Thereisfirm evidence (36). A link between the two seemed obvious (7). No kill-sites are known (3, 7). Although for only ∼8–14 now-extinct megafaunal spe- to advocates of a human-driven process (37), megafauna are known from Tasmania, most cies overlapping with human presence on the and a role for climate change was subse- extinct species had vanished before humans continent. Nearly half of these late-surviving quently discounted. The case for a human arrived. There is a single example of a short species are from New Guinea (3, 34), and role was buttressed by claims that MIS3 (60– most are identified from single occurrences. 28ka)wasatimeofrelativelystableclimatic The uncertainty that currently exists conditions (13). As such, human activities around establishing accurate chronologies for were therefore the only credible explanation megafaunal decline and extinction, particu- for the extinctions (2, 11, 38). larly the paucity of securely dated fossil ma- Proponents of early human-mediated terial (5), has been one of the major obstacles extinctions in Sahul have based their argu- to resolving the question of what caused these ments and conclusions on a number of as- extinctions. The absence of so many of the sumptions. Key among these are that all or species in question following the MIS6 glacial most now-extinct megafauna survived the maximum, a time of undoubtedly severe PGM and the ensuing 80,000 y to be present climate, with further attenuation through when people arrived, that the extinctions MIS5–MIS3 is consistent with a staggered could largely or wholly be attributed to a sin- extinction chronology. However, it has been gle cause within a relatively narrow time suggested that this appearance of staggered frame, and that climate changes within the loss could be a sampling artifact, referred to as last two glacial cycles were unremarkable the Signor–Lipps effect (13). Technically, this relative to those of previous cycles (3, 9). is conceivable, because the last occurrences in The case for a human role was bolstered the fossil record are unlikely to document following the observation of a broad overlap precisely the actual time of extinction. How- between human arrival and terminal dates for Fig. 2. Sites mentioned in the main text. The continental ever, given the actual record and the fact that a small number of late-surviving megafaunal limits of Sahul are defined by the −130-m bathymetry line, so many of the extinct taxa are not known species. A hypothetical “extinction window” and Sahul incorporates Australia, New Guinea, and Tas- – mania. The Nullarbor Plain caves contain middle Pleisto- to have existed within tens of thousands of at 51 39 ka was proposed during which, it cene fossil deposits. Kings Creek is located in the eastern years of human arrival, the most parsimonious was argued, all or most species of now-extinct Darling Downs region.

8778 | www.pnas.org/cgi/doi/10.1073/pnas.1302698110 Wroe et al. Downloaded by guest on September 26, 2021 temporal overlap between people and Pro- PERSPECTIVE temnodon anak, but the bones of P. anak have never been identiﬁed in the rich faunal assemblages recovered from the numerous Pleistocene archeological sites inves- tigated (41).

Climate Change and Megafauna Middle to late Pleistocene faunal extinctions and human arrival in Sahul occurred against abackdropofsignificant climatic change. Until recently, our capacity to unravel the potential impacts of climatic flux on plants and animals, including humans, has been limited by the relatively coarse resolution of the fossil records. Numerous independent studies, including analyses based on high- resolution Antarctic ice core data, now allow us to reevaluate the climatic record, the long- term trends spanning some 800 ka, and the more detailed shorter term fluctuations at critical periods through time. There is a growing consensus that Sahul was subject to stepwise and progressive drying beginning as early as 700 ka (42), and notably within the last 350–400 ka (43–46). In recent years, Antarctic ice core records (47–49) have revealed a distinct change in glacial-interglacial cycles after ∼450 ka. The last five interglacial stages (MIS11.3, MIS9.3, MIS7.5, MIS5.5, and MIS1) were, on average, warmer than preceding interglacial stages, as indicated by Deuterium (δD), a proxy for temperature, in the European Project for Ice Coring in Antarctica (EPICA) Dome C (EDC) record. Concurrently, from ∼450 ka, the isotopic minima, representing the coldest or full glacial stages in the EDC δD record, show an obvious downward trend. These trends mean that isotopic changes recorded for the last glacial cycle (from MIS5.5–MIS2) are almost double the amplitude of the interglacial-glacial maximum cycles between 800and500ka(Fig.5).Inaddition,δD (hence, temperature) is conspicuously low in the EDC ice core data from ∼70–63 ka and during MIS2. Importantly, the occurrence of two extended and severe cold periods in the one glacial cycle is unprecedented in the 800,000 y Antarctic ice core record (48). The high-resolution EDC record also documents considerable millennial-scale variability. There are four distinct Antarctic Isotopic Maxima between 60 ka and 35 ka, Fig. 3. Extinction chronology of Pleistocene megafaunal taxa in Sahul (88 species). For many species, terminal anditisnowclearthattherewasmarked dates are debated, as is the definition of a “secure” date. If the selection criteria of Roberts et al. (9) are applied, as fi ∼ – few as 8 species clearly survived to the time of human colonization of Sahul. Species reported to overlap with aridi cation from 50 45 ka (50, 51), the humans but lacking contextual information linking the dates to the taxa in question are illustrated in gray. The interval during which the first humans ar- majority of taxa cannot be placed within the time frame of human arrival, and many lack reliable radiometric dates rived in Sahul. altogether, with some of the taxa claimed to have been the victims of human-mediated extinction known only from In short, the temperature swings of the last the Pliocene (e.g., Euryzygoma dunense). Of those taxa known to overlap with people, some persist well beyond a previously proposed 51- to 39-ka “extinction window” (9), whereas most of those falling within this window are few glacial cycles were without precedent and not securely linked to the dates (six of nine taxa). Of those taxa potentially surviving until more recently than ∼50 ka, the last glacial cycle exhibits unusual vari- almost half are from New Guinea. ability. The climate patterns in the 100,000 y

Wroe et al. PNAS | May 28, 2013 | vol. 110 | no. 22 | 8779 Downloaded by guest on September 26, 2021 people arrived (10). A recent comprehen- sive overview of charcoal work in Austral- asia (55) determined that fire histories more strongly correlate with climate than human activities. Other proxies include dung-fungus (Spor- ormiella). In a recent study, also located at Lynch’s Crater, declining Sporormiella spores (a proxy for megaherbivores) at ∼41 ka were interpreted as evidence for human-mediated extinction of megafauna (40). Subsequent peaks in Sporormiella were attributed to extant kangaroos. The authors did not explore other equally plausible scenarios. Variation in Sporormiella peaks could as easily be attributed to changes in spore abundance correlated with changes in climate, especially moisture availability. Furthermore, significant contributions to all the Sporormiella peaks, not Fig. 4. Late Pleistocene temporal occurrences of megafauna from the intensively sampled Kings Creek Catchment, just those after 41 ka, could have been made Darling Downs, southeastern Queensland (13), in relation to the hypothesized continental megafaunal extinction by still-extant kangaroos or cassowaries. window and earliest evidence of human colonization. Rarefaction, bootstrapping, and associated statistical analyses Paleontological and isotopic data from demonstrate that the apparent temporally progressive loss of megafauna was a real phenomenon and cannot simply middle Pleistocene fossil deposits in southern be explained as a result of taphonomic or sampling biases (14). Importantly, the data clearly point to prehuman climate changes as a driver of the losses and do not support the hypothesis that there was a local mass extinction of all central Australia (2) have demonstrated arid megafauna at or around the hypothesized extinction window. adaptations in some now-extinct fauna. The implication is that subsequent increased aridity was unlikely to have led to late Pleis- preceding the LGM were anything but be- tivity in arguments for a human role in the tocene extinctions (2). A human role was nign. Rather than MIS3 being a mild and extinctions. For example, increases in fire inferred based on the unproven assumption perhaps humid interstadial in Sahul (e.g., ref. activity reconstructed from charcoal analy- that the extinctions occurred after people 13), paleoenvironmental records demonstrate ses of sediment samples recovered from arrived in the region at ∼40 ka. However, as significant climatic inconstancy. For example, Lynch’s Crater (northeast Queensland) have already noted, there is no evidence that many it has recently been shown that climatic var- been assumed to be a proxy for human of these species survived the middle Pleisto- iability was a key factor in the extinction of activities in particular (54). However, other cene. Paleoenvironmental data show that the the large flightless bird G. newtoni near Lake records show increased burning long before middle to late Pleistocene was particularly Eyre by ∼50 ka (51), and the small mammals from Tight Entrance Cave show a marked increase in turnover at this time (10). With an increasing number of reports presenting high-resolution data through critical periods, further correlations between the disappearance of other megafauna and climate change seem likely to emerge. Further support for a climatically driven process comes from analyses demonstrating that small-bodied species were susceptible to significant impacts resulting from climate change during the middle to late Pleistocene, before human arrival. Bottom-up, ecosystem- changing processes triggered by the disappearance of particular small-bodied species are increasingly being described for North American and Eurasian ecosystems (52, 53). Given trophic interdependencies, ecosystem changes of this kind in small keystone species could have reduced the resilience of larger- bodied species in those same ecosystems. Fig. 5. The EDC δD(‰) record over the last 900 ka (45–47) illustrates the trend toward increasingly warm inter- Paleoenvironmental Proxies and the glacials (red line) and increasingly cold glacial maxima (blue line) beginning at around 400 ka. (Upper) Graphic depicts > Role of Humans the number of species that are not represented thereafter in the fossil record in the following temporal bins: 400 ka or undated, 400–126 ka, 126–51 ka, 51–39 ka, and <39 ka. Species with last appearance dates before human arrival Paleoenvironmental records have also been (50–45 ka) are highlighted in green, and those with last appearance dates after this are highlighted in blue. There is used as important proxies for human ac- little evidence for any extinction pulse associated with human arrival.

8780 | www.pnas.org/cgi/doi/10.1073/pnas.1302698110 Wroe et al. Downloaded by guest on September 26, 2021 arid and variable and, as noted above, that Conclusion primary driver of Pleistocene faunal extinc- PERSPECTIVE climate deteriorated markedly from ∼50–45 Many questions remain. As we work toward tions. Many species of megafauna did not ka (42–45, 48, 50, 51). It is clear that at least a better understanding of the biology and persist into the late Pleistocene, and other some arid-adapted species can be insulated distribution of extinct species, a complex subsequent extinctions postdated the PGM against aridity. They are advantaged in times pattern of faunal extinctions across time and but were completed before humans arrived. of water stress by increased mobility and Sahul’s diverse landscape is emerging. Importantly, a role for humans in the dis- water conservation strategies. However, there Tracking individual histories of faunal species appearance of any surviving taxa, although is a tradeoff. Large species must exist at lower (56), although possible in many northern possible, is yet to be demonstrated. Extinct densities and, of necessity, require greater hemisphere contexts, is severely constrained species that persisted until or beyond ∼50–45 home ranges to maintain viable populations. in Sahul by the patchy fossil record (5), yet it ka ﬁnally disappeared within the context of Further, adaptation to aridity does not in- is one area that would certainly help to re- a rapidly deteriorating climate. sulate against hyperaridity (5). Even the solve the nature of faunal turnover through ACKNOWLEDGMENTS. We thank Jim Allen for incisive surviving red kangaroo (M. rufus), superbly time. Advances in our knowledge of pale- and constructive comments on an early draft of the manu- adapted as it is to arid conditions, has suffered oclimates are steadily improving our un- script. This work was funded by the University of New massive population crashes during rela- derstanding of the complexities of the South Wales and the Australian Research Council: Grants DP0666374 and DP0987985 (to S.W.), Grant DP0557923 tively benign climate intervals within his- extinction processes. Mounting evidence in- (to J.T.F.), Grants DE120101533 and DP120101752 (to toric times (23). creasingly points to climate change as the G.J.P.), and Grants LP100200486 and LP0989969 (to M.A.).

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