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Variable impact of late-Quaternary megafaunal

extinction in causing ecological state shifts in


North and South America
Anthony D. Barnoskya,b,c,1, Emily L. Lindseya,b, Natalia A. Villavicencioa,b, Enrique Bostelmannd,2, Elizabeth A. Hadlye,
James Wanketf, and Charles R. Marshalla,b
a
Department of Integrative Biology, University of California, Berkeley, CA 94720; bMuseum of Paleontology, University of California, Berkeley, CA 94720;
c
Museum of Vertebrate Zoology, University of California, Berkeley, CA 94720; dRed Paleontolgica U-Chile, Laboratoria de Ontogenia, Departamento de
Biologa, Facultad de Ciencias, Universidad de Chile, Chile; eDepartment of Biology, Stanford University, Stanford, CA 94305; and fDepartment of
Geography, California State University, Sacramento, CA 95819

Edited by John W. Terborgh, Duke University, Durham, NC, and approved August 5, 2015 (received for review March 16, 2015)

Loss of megafauna, an aspect of defaunation, can precipitate many megafauna loss, and if so, what does this loss imply for the future
ecological changes over short time scales. We examine whether of ecosystems at risk for losing their megafauna today?
megafauna loss can also explain features of lasting ecological state
shifts that occurred as the Pleistocene gave way to the Holocene. We Approach
compare ecological impacts of late-Quaternary megafauna extinction The late-Quaternary impact of losing 7080% of the megafauna
in five American regions: southwestern Patagonia, the Pampas, genera in the Americas (19) would be expected to trigger biotic
northeastern United States, northwestern United States, and Berin- transitions that would be recognizable in the fossil record in at
gia. We find that major ecological state shifts were consistent with least two respects. First, vegetation should change noticeably,
expectations of defaunation in North American sites but not in South consistent with ecological release from browsing, grazing, and
American ones. The differential responses highlight two factors trampling; such changes should be apparent in fossil-pollen time
necessary for defaunation to trigger lasting ecological state shifts series (17, 25, 29) and possibly also in charcoal (fire-frequency)
discernable in the fossil record: (i) lost megafauna need to have been records (1517, 36). Second, surviving mammal communities
effective ecosystem engineers, like proboscideans; and (ii) historical should demonstrate changes in species composition, richness, and
contingencies must have provided the ecosystem with plant species evenness (32). Testing for such impacts requires fossil sites with the
likely to respond to megafaunal loss. These findings help in identi- following: (i) good records of extinct megafauna; (ii) proximal and
fying modern ecosystems that are most at risk for disappearing temporally overlapping records of vegetation change and fire fre-
should current pressures on the ecosystems large animals continue quency; (iii) associated records of species that allow assessment of
and highlight the critical role of both individual species ecologies and mammalian diversity; (iv) robust dating of megafauna population
ecosystem context in predicting the lasting impacts of defaunation crashes and extinction and vegetation, fire, and diversity changes;
currently underway.
Significance
megafauna | extinction | Quaternary | North America | South America
Removing megafauna from contemporary ecosystems changes

D efaunation is occurring at a rapid pace presently (13).


Losses are particularly severe for megafauna (1) (consid-
ered here as animals with an average body size 44 kg), whose
vegetation and small mammal communities over ecological
time scales. We show that similar dynamics seem to operate
over millennial time scales but only if the megafaunal loss in-
removal can trigger the following: changes in vegetation struc- cludes ecosystem engineers in settings that also contain plant
ture and species composition; reductions in environmental het- species susceptible to ecological release. Under such conditions,
erogeneity, species richness, evenness, seed dispersal, nutrient megafauna extinction can initiate changes that quickly lead to
cycling and distribution, and ecosystem services; coextinction of new, lasting ecological states. This implies that should some
dependent species; and increases in disease-transmitting organ- megafauna currently at risk for extinction actually become
isms (1, 414) and fire frequency and/or intensity (1517). extinct, their characteristic ecosystemsfor example, mosaics
Most work on defaunation has been in contemporary ecosys- of savannah and forestwould also disappear, rapidly trans-
tems. Much less is known about how it manifests over millennial forming into novel systems with respect to what is considered
time scales. A natural experiment to assess lasting effects of normal in todays world.
megafauna loss is provided by the extinctions of late-Quaternary
Author contributions: A.D.B., E.L.L., N.A.V., E.A.H., and C.R.M. designed research; A.D.B.,
megafauna in the Americas, part of global-scale ecological state E.L.L., N.A.V., E.B., E.A.H., J.W., and C.R.M. performed research; A.D.B. provided labora-
shift (18), during which about half of the worlds large-bodied tory facilities; E.L.L. acquired data (especially Pampas); N.A.V. acquired data (especially
mammal species (19, 20) disappeared. In North America, 60 southern Patagonia); E.A.H. acquired data (especially northwestern United States); A.D.B.
and E.B. compiled data; A.D.B. synthesized data; N.A.V. performed computation of con-
megafaunal species died out, with the youngest occurrences of fidence intervals; A.D.B., E.L.L., N.A.V., E.B., E.A.H., J.W., and C.R.M. analyzed data; A.D.B.,
dated species typically falling between 13,000 and 11,000 y ago E.L.L., and E.A.H. interpreted data; N.A.V. interpreted data (especially southern Patago-
(19). In South America, 66 species were lost over a longer time nia); E.B. interpreted data (Pampas and southern Patagonia); J.W. interpreted palynology
and vegetation for northern California; C.R.M. interpreted data (especially confidence
span (2123). intervals); and A.D.B., E.L.L., N.A.V., E.A.H., and C.R.M. wrote the paper.
With a few important exceptions (6, 17, 2429), the major The authors declare no conflict of interest.
changes in vegetation and mammalian community structure that This article is a PNAS Direct Submission.
accompanied Quaternary extinctions have been interpreted as 1
To whom correspondence should be addressed. Email: barnosky@berkeley.edu.
responses to changing climate (1719, 21, 23, 2527, 2935). 2
Present address: Instituto de Ciencias de la Tierra, Facultad de Ciencias, Universidad
Here, we build on recent work of paleoecologists (17, 25, 28, 29, Austral de Chile, Valdivia, Chile.
32, 36) and ecologists (1, 37, 9, 10, 15, 16, 37) who have been This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.
asking instead: Are the observed biotic responses consistent with 1073/pnas.1505295112/-/DCSupplemental.

856861 | PNAS | January 26, 2016 | vol. 113 | no. 4 www.pnas.org/cgi/doi/10.1073/pnas.1505295112


SPECIAL FEATURE
and (v) a fossil record that temporally samples before and after later, respectively, occurred just after the Antarctic Cold Re-
the extinctions. versal, during the beginning of climatic warming that apparently
Here, we examine evidence from five regions where paleonto- initiated a shift from cold grassland vegetation to Nothofagus
logical records are adequate in at least most of these respects: forest (23, 39) (Fig. S4). Hippidion saldiasi and a llama (Lama
southwestern Patagonia, the Pampas, northeastern United States, cf. L. owenii of past publications) disappeared 2,400 y later, as
northwestern United States, and the Alaska/Yukon area (Beringia) transition to Nothofagus continued. At about the same time, fire
(Fig. 1). Each region featured different megafauna and/or vege- frequency also increased, consistent with warming temperatures
tation, and each provides relatively rich datasets within constrained and increased fuel provided by the encroachment of trees. It may
biogeographic settings (see Supporting Information for the South be that extinction of the equid and llama also helped to increase
American sites). If defaunation triggers ecological state shifts uni- fire fuels (Fig. S4) and promote expansion of the Nothofagus
versally, in all areas, we would expect to see as megafauna go ex- forests, which had arrived in the region at least 500 y earlier
tinct: (i) increases in understory and forest plants susceptible to (Figs. S2S4). By 11,000 y ago, Nothofagus forests were firmly
ecological release in the absence of herbivory, trampling, and re- established, and it is only after that (most likely near 10,100 y
lated pressures, potentially with increased fire frequency; and (ii) ago) that Mylodon darwini goes extinct. The overall pattern of
predictable changes in surviving communities of mammal species, herbivore extinction (Fig. S4) is equivocal with respect to
such as adjustments in geographic range, species density, and di- defaunation triggering some of the observed vegetation and fire
versity. Disentangling defaunation impacts from those triggered by changes (23). Although loss of Hippidion and L. cf. L. owenii po-
end-Pleistocene climate change requires observing a discordance tentially corresponds with increasing forest cover and fire frequency,
between the timing of defaunation and climate change proxies with these changes also could be explained entirely by contemporane-
respect to the hypothesized biotic responses, and/or by observing ous climate changes in the region. The extinction of Mylodon does
biotic indicators (for example, of vegetation change or fire fre- not correlate with any major vegetation or fire changes and comes
quency) that make more sense as the result of a defaunation only after Nothofagus forest is well established. Dung samples of
rather than from a climatic trigger. The relative contribution of Mylodon confirm that it primarily grazed in open landscapes (40)
human activity and climate change in causing the late-Quater- (e.g., specializing on grasses), suggesting its loss would have little

ECOLOGY
nary defaunation events is still debated (19). However, our goal impact on woody vegetation (23).
here is simply to understand whether or not the chronology of
megafauna extinction, changes in vegetation and fire records, and South AmericaPampas. The Pampas region (here considered
changes in mammal species diversity support or reject the expec- bounded by 40 S, 60 W; 35 S, 65 W; 25 S, 55 W; 28 S, 45 W;
tations of ecological changes triggered by megafauna extinction, following ref. 41) (Fig. S5) is located between tropical Brazil and
regardless of the ultimate cause of defaunation. We emphasize the cold dry Southern Cone. The region contains ecotones that

AND PLANETARY SCIENCES


that, given the limitations of the fossil record, only the coarsest shifted as late-Quaternary climate changed (42) such that the

EARTH, ATMOSPHERIC,
effects of defaunationsuch as vegetation and diversity changes timing of the Pleistocene-to-Holocene vegetation transitions varied
we examine herecan be recognized by our approach. across the study area over 2,000 y, beginning about 12,000 y ago
(Fig. 2) (4345). Although different parts of the region featured
Vegetational Changes locally distinctive vegetation regimes (see Supporting Information
South AmericaSouthwestern Patagonia. Recent work in the l- for more detail), in general, the end-Pleistocene Pampas was a
tima Esperanza region in Chile has produced a detailed chro- C3-dominated grassland steppe. In the Holocene, C4 vegetation in-
nology of colonization of the region by humans and megafauna, creased, as did seasonal variation in proportions of C3 versus C4
megafauna extinction, and vegetation, fire, and climatic changes grasses (4345). Overall, the increase in C4 grasses (46) and other
for the period 19,000 y ago to 5,000 y ago (23) (Figs. S1S4). vegetational changes (Supporting Information) are consistent with
There, Lama gracilis and Vicugna vicugna [these two taxa may be late-Quaternary climatic warming driving a transition to warmer,
synonymous (38)] became locally extinct about 15,000 y ago. more humid conditions, as also indicated by sedimentology (47),
Humans arrived in the area by 13,750 y ago. The extinction of malacological remains (48), and paleobotanical data (4345, 49).
megacarnivores (Smilodon and Panthera), 1,100 and 1,700 y Most likely well after the vegetation changed (Fig. 2), pro-
boscideans (Notiomastodon), horses (Equus and Hippidion), a llama
(Palaeolama), and meridiungulates (Toxodon and Macrauchenia)
40W
disappear from the record. Xenarthrans (ground sloths and glyp-
160W 140W 120W 100W 80W 60W
todonts) go extinct even later (Fig. 2). Based on morphological
80N analyses and isotopic data from the Pampas region, Notiomastodon
Alaska/Yukon Greenl
n and and Macrauchenia were mixed feeders that consumed both C3
shrubs and C4 grasses; Equus and Toxodon were grazers, and
60N
Hippidion consumed primarily C3 vegetation (50). Generally,
mammalian herbivores prefer C3 grasses when they are available
40N
Norrth (46), and in Uruguay today, grazing promotes the dominance of
Americ
r a C4 grasses where both C3 and C4 grasses are present, although the
Northwestern Northeastern
USA USA effect is variable; C3 and C4 grasses both are heavily used but in
20N different seasons (51). These considerationsin addition to the
fact that the grazers and the xenarthrans likely became extinct only
0 well after the vegetation transition began (Fig. 2)suggest that
Sou
o th
climate change, not defaunation, was the primary cause of the C3
Ame
m rica to C4 transition.
20S There is no evidence that loss of Notiomastodon significantly
impacted the amount of shrubby vegetation in the dry southern
Pampas pampas (Fig. S5), which actually retracted in range across the
40S
Southern PleistoceneHolocene transition (43, 48). However, many un-
Patagonia dated Notiomastodon specimens (52) come from northern Uru-
guay and southern Brazil (Fig. S5), where locally gallery forests
Fig. 1. Areas examined for impacts of late-Quaternary defaunation. along rivers and tropical woodlands expanded somewhat at the

Barnosky et al. PNAS | January 26, 2016 | vol. 113 | no. 4 | 857
Fig. 2. Chronology of megafaunal loss, vegetation, and climate change in the Pampas. The diagram shows robust calibrated radiocarbon dates on bone
collagen or tooth enamel (the error bars span the 2- probability distribution and, for many dates, are too small to appear on the chart). A transition (darker
green shading) from an ecosystem dominated by C3 (Pooid) grasses to C4 (Panicoid) grasses begins 12,000 y ago and is asynchronous across the Pampas (see
Supporting Information for details). The red and blue shading on the left illustrates cool (blue) and warm (red) times. ACR, Antarctic Cold Reversal, which
overlaps the northern hemispheres Younger Dryas to some extent but is somewhat earlier. Gray distributions indicating the probability of timing of ex-
tinction for megafauna were calculated using the GRIWM best-estimate method (59); also see ref. 68. for R-code. GRIWMs best estimate of the extinction
time and its 95% confidence band are younger than 5,000 y ago for glyptodonts (estimated probable timing of extinction: 1,903 calibrated years BP; range:
4,126 to 256 calibrated years BP; the negative number indicates the probability extends into the future) and Notiomastodon (estimated probable time of
extinction: 2,415 calibrated years BP; range: 3,0011,838 calibrated years BP). Clearly, these anomalously young extinction estimates come from a paucity of
radiocarbon dates, with those few available being widely spaced in time. Such results do not provide evidence for persistence of megafauna well into the
Holocene; rather, they emphasize that more radiocarbon dates are needed. Dietary preferences of extinct megafauna are indicated by G (grazer), B
(browser), M (mixed feeder), and U (unknown) (50, 69).

end of the Pleistocene (44, 45). More Notiomastodon dates from suggest significant decline in their abundance by 12,600 y ago,
these areas are needed to assess whether a defaunation signal with last records by 11,700 y ago. Confidence intervals calculated
would emerge. Available data are insufficient to evaluate fire by the Gaussian-resampled, inverse-weighted McInerny et al.
history in this region. (GRIWM) method (59) from the data in ref. 58. indicate high
probability of extinction by 11,000 y ago. Thus, if the Sporormiella
North AmericaNortheastern United States. Previous work links decline does indicate significant decrease in megafauna abundance,
megafaunal population crashes with vegetation response and this decline also indicates that noticeable impacts of defaunation
increased fire at Appleman Lake, IN (17, 29); Silver Lake, OH can occur from reducing animal densities even in the absence of
(25); and in southeastern New York (Otisville, Binnewater Pond, final extinction. Also near 11 ka, Quercus pollen (oak) and charcoal
Pawelski Farm) (36), using percentage decline of the dung-spore abundance increase dramatically, an expected consequence of both
fungus Sporormiella (17, 25, 29, 53, 54) in palynological records megafaunal extinction and warming climate.
as a proxy for local decline of megafauna, with recognition that
the taphonomy of Sporormiella is not yet fully understood (24, North AmericaNorthwestern United States. We used composite
53, 55). Vegetation and fire response is consistent with climate data for the biogeographic region covering northern California into
change interacting with defaunation (17, 29), but less so with the Pacific Northwest. We correlated palynological and charcoal
climate change on its own (17, 25, 29). Of interest is the increase records from Twin Lake (34) in Californias Klamath Mountains
in taxa such as Fraxinus nigra (ash), Ostrya/Carpinus (hornbeam/ and Mumbo Lake in the Trinity Mountains (35) with mammal data
ironwood), and Quercus (oak) in the Indiana and Ohio sites, and from nearby Potter Creek (60) and Samwell Caves (32, 61), within
Alnus (alder), Betula (birch), and Quercus in the New York sites 100 km to the southeast. Regional timing of extinction is con-
during the Younger Dryas, a temporary return to cool conditions strained by megafauna dates from Oregons Willamette Valley
that presumably would not have favored their expansion. At the (62) plus the Manis Mastodon (63), all within 800 km north
same time, charcoal frequencies rose. Increasing percentages of of the California cave sites, and Sporormiella declines docu-
ash, hornbeam/ironwood, oak, alder, and birch and a concomi- mented from lake sediments in Californias central Sierra Nevada,
tant increase in fire fits the model of defaunation well, because about 800 km to the south of the caves (53, 54). Corresponding
contemporary ecosystems exhibit such increases in woody un- pollen profiles from the Sporormiella sites have not been pub-
derstory and tree-forming plants when megafauna, especially ele- lished. For proxies of regional vegetation and sea surface tem-
phants, are removed (3, 11, 56, 57), and the increase in combustible perature, we used information from Ocean Drilling Program
woody fuel promotes fires (1517, 36). The proboscideans Mammut (ODP) site 1019 (64).
americanum (mastodons) and Mammuthus (mammoths) occupied These data document that by 14,000 y ago, megafauna near
the region, as did Cervalces (stag-moose), Megalonyx (ground sloth), Twin Lake and Mumbo Lake included Mammuthus (mammoth)
Ovibos moschatus (shrub ox), Castoroides ohioensis (giant beaver), and Mammut (mastodon), Bison (bison), Platygonus (peccary),
Platygonus compressus (peccary), and Bison priscus (bison) (58). Equus (horse), and the sloths Megalonyx, Paramylodon, and
These megafauna remained on the landscape for >2,000 y after the Nothrotheriops (32, 60, 61). The youngest radiocarbon dates and
Sporormiella decline, which occurred by 13.7 ka at Appleman Lake, associated confidence intervals indicate that these taxa were
13.9 ka at Silver Lake, and between 1314 ka at the New York likely extinct by 12,400 y ago (Fig. 3). Unlike the northeastern
sites. Summed probability distributions of radiocarbon dates United States, where Sporormiella declines long before final ex-
from extinct megafauna in the northeast compiled by ref. 58. tinction of megafauna, in the northwestern United States, the

858 | www.pnas.org/cgi/doi/10.1073/pnas.1505295112 Barnosky et al.


SPECIAL FEATURE
E
C
D
A B

Fig. 3. Chronology of vegetation change in northern California compared with sea surface temperature (SST) and regional extinction of megafauna. (Left)

ECOLOGY
SST and pollen-percentage curves are from ODP site 1019 (64). (Center) Twin Lake pollen diagram reproduced with permission from ref. 34. TCT, un-
differentiated pollen from Taxodiaceae, Cupressaceae, and Taxaceae. Blue shading indicates Younger Dryas (YD). Megafauna dates are from ref. 62, except
for the oldest proboscidean date from ref. 63. (Right) Proboscideans (Mammuthus and Mammut) (A), Bison (B); Equus (C), Paramylodon (D), and Sporormiella
(E) from Mono Lake on the left and Exchequer Meadow on the right (53, 54). Probability distributions for extinction timing at right estimated using GRIWM
method (59); see Fig. 2 for explanation. The dating of the Sporormiella decline is not amenable to estimating extinction timing with the GRIWM method
because of the nature of the data, so here we simply report the 95% uncertainty in the dates used to constrain the ages of the youngest occurrences at each
of two separate lake localities.

AND PLANETARY SCIENCES


EARTH, ATMOSPHERIC,
youngest radiocarbon dates on bones and the Sporormiella de- Supporting Information). The ecological transformation from
cline appear generally coeval (Fig. 3). productive forests and grasslands to tundra has been interpreted
The Twin Lake record documents that Alnus (alder), a tree- (26, 27) to result from the loss of mammoths plus human-caused
forming shrub that spreads rapidly in the absence of browsing reduction in the densities of megafaunal species that survived. With
and trampling by ungulates (57), arrived in the region about fewer megafauna on the landscape and proboscideans absent, the
14,000 y ago, as the climate became favorable for its growth and reduction of trampling, browsing, and grazing pressure by big an-
when megafauna were still present. Alnus abundance declines imals is postulated to have stimulated an increase in woody and
slightly at the beginning of the Younger Dryas (12,900 y ago), leafy plants, which set off an ecological cascade by promoting
consistent with the expected response to cooler conditions, but accumulation of surface leaf litter that insulated soil, reduced
then begins to increase in the midst of the Younger Dryas summer soil temperatures, caused formation of permafrost,
cooling (12,000 y ago), at odds with expectations of an exclu- and favored growth of mosses and shrubs at the expense of
sively climate-driven change but consistent with predicted re- grasses and other nutritious fodder for herbivores. Experi-
sponse to defaunation (Fig. 3). This is in marked contrast to the mental studies support this idea (26, 27, 65).
persistence of other plant taxa that reflect cool conditions all of the
way to the end of the Younger Dryas: Abies (fir), Picea (spruce), Mammal Communities
and Tsuga heterophylla (western hemlock); these disappear at Of regions discussed in this paper, only northern California has
11,600 y ago. At the same time (from about 12.611.8 ka), char- an adequate published record, from Samwell Cave (32), to test
coal abundances indicate that fire frequency increased (34), con- for local impacts of defaunation on mammalian community
sistent with expectations of decreased large-herbivore populations. structure. Samwell Cave is near the two pollen sites discussed in
At Mumbo Lake, both Alnus and Quercus (oaks) were present North AmericaNorthwestern United States. There, coeval with
by 13,500 y ago. Beginning 12,000 y ago, an increase in ever- the regional signal for megafaunal extinction, a lasting decline in
green and deciduous oaks and in Alnus, and an inferred transition both richness and evenness (a metric describing to what degree
to a more closed, diverse forest with more burnable biomass, fits abundances of individuals in different taxa are equal) in the small
expectations of megafaunal loss, although previously those changes
have been attributed entirely to climatic drivers (35).
Climate proxy and vegetation data from ODP site 1019 sug-
gest that regionally vegetation changed in the mid-Younger
Dryas in ways that are inconsistent with expectations from cli-
mate change alone (64). Especially suggestive of defaunation is
the dramatic rise in Alnus pollen, which precedes, by about 600 y,
the warming of local sea surface temperatures (Fig. 3).

North AmericaAlaska and the Yukon (Beringia). Past work has Fig. 4. Amboseli National Park, Kenya. Typical vegetation is shown where
pointed out that end-Pleistocene vegetation changes in Beringia elephants roam freely (A) compared with a nearby area where elephants are
are consistent with defaunation (26, 27, 33) (summarized in excluded (B).

Barnosky et al. PNAS | January 26, 2016 | vol. 113 | no. 4 | 859
mammal community has been well documented (32). At the con- Conclusions
tinental scale and within biogeographic provinces, most mammalian Our data provide a test of whether many different kinds of
communities in the lower 48 United States also became less megafaunasuch as proboscideans, giant ground sloths, glypto-
species-rich during the time when megafauna extinction was ac- donts, toxodonts, equids, and llamascause similar, lasting eco-
celerating (30, 31) (also see Supporting Information). Such di- logical changes when they go extinct. We find that the clear and
versity losses at the local to continental scales are consistent with lasting defaunation effects are variable, depending on the mega-
megafaunal extinction triggering adjustments of small-mammal fauna species and the particular ecosystem from which it was de-
density and distribution. leted. In general, it seems extinction of megafauna will likely trigger
permanent ecological state shifts that manifest as substantially
Discussion modified vegetation and mammalian community structure if (i) the
Pinpointing a particular taxons extinction precisely is not pos- lost megafauna are significant ecosystem engineers; and (ii) the
sible given vagaries of the fossil record; therefore, we have ecosystem contains plant species susceptible to ecological release
expressed extinction timing in terms of confidence bands (Figs. with declining herbivore pressure. The North American systems
2 and 3 and Fig. S4; also see ref. 23). Wide bands result from a we studied, which contained proboscideans, showed particularly
paucity of dates, a limiting factor in our approach. Also, the strong response to defaunation. The two South American areas we
fossil record is likely to preserve only the most dramatic, obvious studied did not exhibit as strong a defaunation signal, either be-
signs of defaunation. This is both a strength and a weakness of cause megafauna that acted as major forest-ecosystem engineers
our study. The strength is that if the fossil record does reveal were absent (southwestern Patagonia, which lacked proboscideans)
effects of losing megafauna, those effects are severe and the or because soil and climatic limitations prevented the plant taxa
implication that they have for ongoing defaunation are robust. capable of forming dense forest to flourish, or the requisite plants
The weakness is that subtler but perhaps equally important ef- never dispersed there (the Pampas).
fects of defaunation, such as changes in nutrient cycling or in As has been previously recognized (17, 25, 29), the ecosystems
environmental heterogeneity, may not be revealed by our that are most prone to shift into new regimes are those that are
methods. With those caveats, the data available warrant some simultaneously impacted by both climate change, which sets the
tentative conclusions. stage for previously minor components of vegetation to flourish,
In all regions examined, end-Pleistocene climate change clearly and defaunation, which further promotes major vegetational
played a role in reshaping ecosystems, as is widely recognized (17 transformations. Both conditions are present in contemporary
19, 21, 23, 2527, 2935). However, in all three North American ecosystems with megafauna, as they were during the Pleistocene
regions, a common aftermath of losing herbivore megafauna was Holocene transition.
an apparent increase in plants that form understory and deciduous Our study also provides insights about which modern-day eco-
forest; this was not observed for either of the South American systems are most in danger of disappearing as a result of con-
regions. These differences may illustrate an important point temporary defaunation. Risks of irreversible change may be highest
about potential effects of megafauna lossthe extent of ecolog- in mixed mosaics of grassland and forest that still contain the
ical change depends on: (i) the ecological roles of the deleted largest megafauna, which tend to be ecosystem engineers. For
megafauna; and (ii) the chance abiotic constraintsincluding example, large swaths of savannah in East and South Africa, where
climate and historical contingencythat provide opportunities elephants are in danger of extinction within the next two decades
for marked transformation of vegetation. In the North American from intense poaching, would be likely to transform radically (Fig.
sites, a critical ecosystem engineer seems to have been pro- 4). However, because our study demonstrates that not all mega-
boscideans; only after mammoths and/or mastodons disappeared faunal species play equal roles in maintaining ecosystem structure
or declined substantially did denser understory and deciduous and function, it highlights the necessity to thoroughly understand
forests began to flourish, much as is evident in African savannah- the ecological role of each species before making predictions about
grasslands today (Fig. 4). how its removal will or will not cascade through an ecosystem to
In southern Patagonia, forest-forming vegetationNothofagus trigger irreversible changes.
was there, but proboscideans were not. This finding may ex-
plain why, in this study area, the signal for defaunation is at Methods
best equivocal for extinction of an equid and a llama and absent for Following refs. 21 and 66, we assume that the actual extinction of a given
deletion of the mylodont sloth. The lost taxa were not ecosystem species was more recent than its youngest dated specimens, so we calculated
engineers in the sense of knocking over trees, tearing off their estimates of the temporal intervals over which taxa became regionally ex-
branches, and trampling and eating new shoots. Instead, the lost tinct using the GRIWM method (59) (Figs. 2 and 3). GRIWM provides an es-
taxa inhabited open grasslands almost exclusively; only when the timate of the true time of extinction by extending the observed stratigraphic
grasslands disappeared, as a result of climatic changes that allowed range by the average gap size (but up-weighting younger gaps to accom-
Nothofagus forest to become widespread, did those megafauna modate nonrandom preservation and recovery of fossils) within the known
disappear from the region. stratigraphic range. GRIWM accommodates the uncertainties in the radio-
metric dates by providing a 95% confidence band around the estimated
In the Pampas a forest-ecosystem engineer, Notiomastodon,
extinction time. All dates mentioned in the text were vetted from published
was present (and lost), but in most of the region that contains literature and are expressed in calendar years before present calibrated
dated Notiomastodon fossils, either the soil and climatic regimes using Calib version 7.0.2 (67). For South American megafauna dates, only
remained unsuitable for the establishment of forests, or tree radiocarbon dates considered robust (with a score of 11, following ref. 21)
species capable of thriving in that environment never dispersed were used.
there, so even after Notiomastodon disappeared, major restruc-
turing of the vegetational component of the ecosystem did not ACKNOWLEDGMENTS. We thank Y. Mahli and C. Doughty for inviting us to
result. Further work is needed to see whether loss of Notio- present this work. F. Martn and L. Borrero helped in assembling data from
southern Patagonia. J. L. Prado provided a preprint of ref. 22. We appreciate
mastodon might help explain local early-Holocene expansion of discussions with R. Byrne, G. Politis, J. L. Prado, L. Avilla, and D. Moth. This work
forests in the northern, more tropical pampas (northernmost was funded by National Science Foundation Earth Sciences Grant 1148181. This
Uruguay and southeastern Brazil). is University of California Museum of Paleontology Contribution 2072.

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Barnosky et al. PNAS | January 26, 2016 | vol. 113 | no. 4 | 861
Supporting Information
Barnosky et al. 10.1073/pnas.1505295112
ltima Esperanza Site, Southwestern Patagonia C3-to-C4 grasslands, regionally across the Pampas distinctive pat-
Details of the ltima Esperanza analysis have been published terns of change are apparent (Fig. S5): (i) grassland to Amaranthus
elsewhere (23). Here, we provide summary figures and information steppe and expansion of subtropical forest in the north-central
most pertinent for interpreting the impacts of defaunation. pampas between 12,00011,500 y ago (45); (ii) C3 to C4-domi-
Fig. S1 shows the location of the megafaunal and pollen sites in nated grasslands and widespread development of wetland and
the study area, which is in southern Chile near the eastern flank of floodplain vegetation in the easternmost regions between 12,000
the Andes Mountains, within a climatic regime that today supports 10,600 y ago (43, 44); and (iii) replacement of shrub steppe and
a mixed Nothofagus forest. Note that the megafauna sites and the xerophytic woodland with humid grassland in the southernmost
lakes that provide paleoenvironmental information (vegetation, Pampas between 11,00010,000 y ago (43).
climate, and fire histories) are all found within about 30 km of each
other, most within 10 km, making this a highly resolved record of North AmericaBeringia (Alaska and the Yukon)
events in a small geographic region. Refs. 26, 27, and 33 present detailed information to track the
Figs. S2 and S3 show relevant data on which the interpretation changing abundance and extinction of megafauna with respect to
of the transition to Nothofagus forest from the preexisting cool vegetation changes. The basic chronology of relevance to assessing
grasslands is based, and charcoal records from which fire history vegetational impacts of megafaunal loss is that Equus drops out of
is inferred. the record first, by 12,300 y ago, coincident with arrival of humans
Fig. S4 summarizes the available radiocarbon dates for all and with increasing numbers of Cervus elaphus (wapiti) (26, 27, 33).
megafauna found from the sites shown in Fig. S1, compared with a Contemporaneous vegetation changesincrease in Salix (willow),
summary of climate change, fire frequency, and human arrival. As Gramineae (grasses), Cyperaceae (sedges), Artemisia (sagebrush),
explained in ref. 23, the GRIWM best-estimates of the time of and Betula (dwarf birch)are more parsimoniously explained by
extinction (or arrival in the case of the humans) is indicated by the climate change to warmer, moister conditions than by replacing
colored normal distributions, which represent the 95% confidence horses with wapiti. Mammoths remained until 11,200 y ago; with
intervals (black line in Fig. S4, most probable time of extinction). their decrease (27), Betula increased rapidly, leveling off at peak
Warming and cooling events are inferred from the Epica Dome abundance coincident with the youngest radiocarbon dates on
C Antarctic ice core (70) and are consistent with the pollen mammoth bones. The pattern of increasing birch forests with
chronologies; red and blue bands at left in Fig. S4 summarize cli-
loss of mammoths is consistent with removing proboscideans
mate data as warm versus cooling events, respectively. Note that
from the ecosystem (26, 27, 33). Coeval with last records of
the ACR is a temporary return to cold conditions, which occurred
mammoths were apparently decreasing abundances of wapiti
after end-Pleistocene warming had commenced and had caused
glaciers to retreat from their maximum extent. The ACR occurs and bison, along with an increase in human population densi-
slightly earlier than, but overlaps, the Younger Dryas in North ties, further climatic warming, and conversion of vast tracts of
America. Major vegetation changes (yellow, light green, and dark formerly productive forests and grasslands to tundra.
green bands at right in Fig. S4) and fire frequency information Mammal Communities
(black dashed rectangle in Fig. S4) are extracted from ref. 39; see
also Figs. S2 and S3. The richness decline of mammal communities at the continental
scale had two components, actual extinction of megafauna, and
Pampas Region individualistic range adjustments of the small-bodied mammal
Fig. S5 shows boundaries of the Pampas as considered in this species. The small-bodied species did not suffer much extinction,
study, the location of paleoenvironmental proxy sites, and the with only 6 species known to die out, in contrast to at least 60 large-
location of specimens of Notiomastodon, both dated and undated. bodied ones. The biogeographic adjustments of small mammals,
The data presented in Fig. 2 of the main text were compiled from however, apparently contributed considerably to depressing richness:
recent literature, as cited in the main text. Radiocarbon dates for causing small mammal diversity to decline by 1651% (depending
megafauna were taken primarily from refs. 21 and 22 and vetted so on the biogeographic province), effectively doubling the regional
that only dates with rank 11 or above (as explained in ref. 21) were diversity loss attributable to megafaunal extinction alone (30).
used. The paleovegetation and paleoclimatic proxies as interpreted Detailed diversity studies are not available for the South
by the studies cited in Fig. S5 were used to compile the vegetation- American regions addressed in this paper, but low richness and
change and climatic histories of the region. Although the general evenness has been noted in early-Holocene rodent communities
vegetation change across the entire study area involved a shift from in the Pampas (71).

Barnosky et al. www.pnas.org/cgi/content/short/1505295112 1 of 5


ltima Esperanza Ice Lobe
LGM position
B N
Palaentological and/or
Archaeological site 5133S

Lake and/or bog core site

ltima Esperanza
Sound
5140S

ltima Puerto
A
Esperanza Natales

Pantano
Dumestre 5146S
4 km

A 7235W 7224W

Cerr
o Se N
ore
t
Lago
Sofa
CLS1
CLS4
AQ
5132S
Cer Vega Bentez
ro B
A3-DH ent
ez
CM
CdM
Lago
CCh
Eberhard
4 km

B 7239W 7233W

Fig. S1. (A) General view of the ltima Esperanza area. The location of the bog and lake records that provide vegetation change and fire history are shown by
the blue rectangles. The megafaunal sites are shown by orange dots. The thick gray line shows the approximate maximum late glacial extent of the ltima
Esperanza Ice Lobe. Until about 18,000 y ago, a proglacial lake submerged the study area; thus, in this region, it is possible to obtain information about both
the earliest records of occupation by megafauna and humans and extinction of the megafauna. (B) Closer view of the Cerro Bentez, Cerro Seoret, and Lago
Sofa areas. This is the region that supplies the data discussed in the text and summarized in Fig. S4, which allows building the detailed chronology of human
occupation, vegetation change, fire history, and megafaunal extinction that is used to interpret effects of defaunation. A3-DH, Alero 3 Dos Herraduras; AQ,
Alero Quemado; CCh, Cueva Chica; CDM, Cueva del Medio; CLS1, Cueva Lago Sofa 1; CLS4, Cueva Lago Sofa 4; CM, Cueva del Milodn. Reproduced with
permission from ref. 23.

Barnosky et al. www.pnas.org/cgi/content/short/1505295112 2 of 5


Lago Eberhard
Depth
10.4 510
520

Acaena
10.6

Poaceae
10.8 530
540
11.0

Asteraceae subfam. Asteroidea


550

Nothofagus dombeyi type


11.2
560

Cal ka BP
11.4 570

Misodendron
11.6 580
11.8 590
12.0 600
610
12.2 620
630
12.4
640
650
12.6 660 20 40 60 80 5 20 40 60 80 10 10
% pollen
Pantano Dumestre
Depth
9.0 200

Asteraceae subfam. Asteroidea


9.5 210
10.0
10.5 220
230
11.0 240

Acaena
250
Nothofagus dombeyi type

11.5 260
Cal ka BP

12.0 270
280
12.5
290
13.0 300
Misodendron

Galium type
310
13.5 320
330
14.0 340
350
360
20 40 60 2 20 40 60 80 20 40 60 10
% pollen

Fig. S2. Percentage diagram of pollen from Lago Eberhard (Top) and Pantano Dumestre (Bottom). Pollen percentages are shown as the proportion of ter-
restrial pollen total sum. Only taxa most informative for inferring vegetation changes relevant to megafauna extinction are shown. For a complete pre-
sentation and analysis of these records, see refs. 23 and 39. Reproduced with permission from ref. 23.

Lago Eberhard Pantano Dumestre


A 3 B 2
% Organic

% Organic

2
matter

matter

1
1
0 0

-1 -1
100 60
C 80
D
charcoal
% Grass
charcoal
% Grass

60 40
40
20
20
0 0
4 2.5
frequency
frequency

E 3 F 2
Fire
Fire

2 1.5
1
1 0.5
0 0
160 160
G H
(particles*cm

(particles*cm

120 120
CHAR

CHAR
*year )

*year )

80 80
40 40
0 0
2 3
(Standarized)
(Standarized)

I J 2
1
ROC
ROC

1
0
0
-1 1
10.5 11 11.5 12 12.5 13 9.0 10 11 12 13 14 15
Cal ka BP Cal ka BP

Fig. S3. Comparison of Lago Eberhard (Left) and Pantano Dumestre (Right) charcoal and vegetation-change records. Traces A and B indicate percentage of
organic matter through time; traces C and D indicate percentage of grass charcoal; traces E and F indicate fire frequency, measured as fire events/500 y; traces G
and H indicate Charcoal Accumulation Rates analyses (CHAR); traces I and J indicate rates of change analyses (ROC) in the pollen records. Information is
extracted and modified from refs. 23 and 39. Black triangles show the timing of the onset in the increase of Nothofagus for each site. Reproduced with
permission from ref. 23.

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Climate Vegetation
5
6
7 Nothofagus
forest
8 established
9
10
Fire frequency 11
increase Increase in
12 Nothofagus
Warming Cal ka BP Cold grassland
13
ACR 14 Reclus volcanic eruption

15

Warming 16
17
Onset of ice free conditions
LGM 18
Felidae Equidae Camelidae Pilosa Evidence of
humans
Rank
Smilodon Lama cf. Lama 11
Hippidion owenii gracilis Mylodontidae
Rank
Panthera saldiasi Vicugna Lama 12
Mylodon Rank
Mylodon darwini
vicugna guanicoe
13

Fig. S4. Chronology of megafaunal extinctions plotted against climate change as indicated by oxygen isotope and pollen data (left colored bands, where blue
is cool and red is warm); vegetation change [right colored bands, with yellow equating to cold grassland dominance, yellowish green representing mixed
grasslands and Nothofagus forest, and olive green (younger than 11,000 ka) indicating predominance of Nothofagus forest]; and timing of increase in fire
frequency (dotted-line box). See Figs. S2 and S3 for more details on vegetation change and fire frequency indicators. The megafaunal extinction chronology
and the chronology of human arrival is based on dates listed in ref. 21; all dates were vetted for robustness, with only those of rank 11 (as explained in ref. 21)
or higher used. The timing of local ice-free conditions is taken from ref. 72 (light blue rectangle). Also shown is the timing of the Recls Volcano eruption (red
line), which although it distributed considerable ash in the region, had no apparent effect on the timing of the faunal or vegetation changes (23). The time axis
is in calibrated years before present. For the radiocarbon dates on megafauna and human occupation, the dots (or triangles for humans) show the median and
the whiskers show the 2- probability. Distributions indicating the probability of timing of extinction for megafauna and first arrival for humans were cal-
culated using the GRIWM best-estimate method; see ref. 68 for explanation and R-code. Dietary preferences are indicated in brackets by C (carnivore), M
(mixed feeder herbivore), G (grazer), and U (unknown) (40, 7375). Reproduced with permission from ref. 23.

Barnosky et al. www.pnas.org/cgi/content/short/1505295112 4 of 5


Fig. S5. Red lines delineate the area of the Pampas considered in this paper, which is the area of southeastern South America that comprised a grassland-
steppe ecosystem during the Last Glacial Maximum (41). Green dots show the provenance of paleoclimate proxy data that indicate a shift in vegetation and
climate in various regions, which took place at somewhat different times over 2,000 y beginning 12,000 y ago, as explained in the Pampas Region section.
Details of the environmental interpretation at each site are given in the following references: ref. 45 (site 1, Pay Paso); ref. 44 (site 2, Los Ajos); ref. 49 (site 3,
Arroyo Sauce Chico; site 4, Empalme Querandies; site 5, Cerro La China); and ref. 43 (site 6, Sauce Grand; site 7, La Horqueta II; site 8, Napost Grande). Black
dots show sites that have yielded Notiomastodon (52), although very few of these specimens have been radiocarbon-dated. Abbreviations for environmental
conditions in the late Pleistocene are as follows: HP, Humid Pampas; IP, Inland Pampas; SP, Southern Pampas; XW, xerophytic woodland.

Barnosky et al. www.pnas.org/cgi/content/short/1505295112 5 of 5