Accelerated Modern Human-Induced Species Losses: Entering the Sixth Mass Extinction.

Abstract

The oft-repeated claim that Earth's biota is entering a sixth " mass extinction " depends on clearly demonstrating that current extinction rates are far above the " background " rates prevailing in the five previous mass extinctions. Earlier estimates of extinction rates have been criticized for using assumptions that might overestimate the severity of the extinction crisis. We assess, using extremely conservative assumptions, whether human activities are causing a mass extinction. First, we use a recent estimate of a background rate of 2 mammal extinctions per 10,000 species per 100 years (that is, 2 E/MSY), which is twice as high as widely used previous estimates. We then compare this rate with the current rate of mammal and vertebrate extinctions. The latter is conservatively low because listing a species as extinct requires meeting stringent criteria. Even under our assumptions, which would tend to minimize evidence of an incipient mass extinction, the average rate of vertebrate species loss over the last century is up to 114 times higher than the background rate. Under the 2 E/MSY background rate, the number of species that have gone extinct in the last century would have taken, depending on the vertebrate taxon, between 800 and 10,000 years to disappear. These estimates reveal an exceptionally rapid loss of biodiversity over the last few centuries, indicating that a sixth mass extinction is already under way. Averting a dramatic decay of biodiversity and the subsequent loss of ecosystem services is still possible through intensified conservation efforts, but that window of opportunity is rapidly closing.

Full text

ENVIRONMENTAL SCIENCES
Accelerated modern human–induced species
losses: Entering the sixth mass extinction
Gerardo Ceballos,
1
* Paul R. Ehrlich,
2
Anthony D. Barnosky,
3
Andrés García,
4
Robert M. Pringle,
5
Todd M. Palmer
6
The oft-repeated claim that Earth’s biota is entering a sixth “mass extinction”depends on clearly demonstrating that
current extinction rates are far above the “background”rates prevailing in the five previous mass extinctions. Earlier
estimates of extinction rates have been criticized for using assumptions that might overestimate the severity of the
extinction crisis. We assess, using extremely conservative assumptions, whether human activities are causing a mass
extinction. First, we use a recent estimate of a background rate of 2 mammal extinctions per 10,000 species per
100 years (that is, 2 E/MSY), which is twice as high as widely used previous estimates. We then compare this rate
with the current rate of mammal and vertebrate extinctions. The latter is conservatively low because listing a
species as extinct requires meeting stringent criteria. Even under our assumptions, which would tend to minimize
evidence of an incipient mass extinction, the average rate of vertebrate species loss over the last century is up to
114 times higher than the background rate. Under the 2 E/MSY background rate, the number of species that have
gone extinct in the last century would have taken, depending on the vertebrate taxon, between 800 and 10,000
years to disappear. These estimates reveal an exceptionally rapid loss of biodiversity over the last few centuries,
indicating that a sixth mass extinction is already under way. Averting a dramatic decay of biodiversity and the
subsequent loss of ecosystem services is still possible through intensified conservation efforts, but that window
of opportunity is rapidly closing.
INTRODUCTION
The loss of biodiversity is one of the most critical current environmental
problems, threatening valuable ecosystem services and human well-
being (1–7). A growing body of evidence indicates that current species
extinction rates are higher than the pre-human background rate (8–15),
with hundreds of anthropogenic vertebrate extinctions documented in
prehistoric and historic times (16–23). For example, in the islands of
tropical Oceania, up to 1800 bird species (most described in the last
few decades from subfossil remains) are estimated to have gone extinct
in the ~2000 years since human colonization (24). Written records of
extinctions of large mammals, birds, and reptiles date back to the 1600s
and include species such as the dodo (Raphus cucullatus, extinguished
in the 17th century), Steller’sseacow(Hydrodamalis gigas, extinguished
in the 18th century), and the Rodrigues giant tortoise (Cylindraspis
peltastes, extinguished in the 19th century). More species extinction
records date from the 19th century and include numerous species of
mammals and birds. Records of extinction for reptiles, amphibians,
freshwater fishes, and other organisms have mainly been documented
since the beginning of the 20th century (14,17). Moreover, even in
species that are not currently threatened, the extirpation of popula-
tionsisfrequentandwidespread,with losses that far outstrip species-
level extinctions (18,25). Population-level extinction directly threatens
ecosystem services and is the prelude to species-level extinction (18).
Here,weanalyzethemodernratesofvertebrate species extinction
and compare them with a recently computed background rate for mam-
mals (7). We specifically addressed the following questions: (i) Are
modern rates of mammal and vertebrate extinctions higher than the
highest empirically derived background rates? (ii) How have modern
extinction rates in mammals and vertebrates changed through time?
(iii) How many years would it have taken for species that went extinct
in modern times to have been lost if the background rate had prevailed?
These are important issues because the uncertainties about estimates of
species loss have led skeptics to question the magnitude of anthropo-
genic extinctions (26) and because understanding the magnitude of
the extinction crisis is relevant for conservation, maintenance of eco-
system services, and public policy.
Until recently, most studies of modern extinction rates have been
based on indirect estimates derived, for example, on the rates of de-
forestation and on species-area relationships (11,14). Problems related
to estimating extinction since 1500 AD (that is, modern extinctions)
have been widely discussed, and the literature reflects broad agreement
among environmental scientists that biases lead to underestimating the
number of species that have gone extinct in the past few centuries—
the period during which Homo sapiens truly became a major force on
the biosphere (1–4,6–8,14,15). However, direct evaluation is complicated
by uncertainties in estimating the incidence of extinction in historical
time and by methodological difficulties in comparing contemporary ex-
tinctions with past ones.
Less discussed are assumptions underlying the estimation of
background extinction rates. The lower these estimates, the more dra-
matic current extinction rates will appear by comparison. In nearly all
comparisons of modern versus background extinction rates, the
background rate has been assumed to be somewhere between 0.1 and
1 species extinction per 10,000 species per 100 years (equal to 0.1 to
1 species extinction per million species per year, a widely used metric
known as E/MSY). Those estimates reflect the state of knowledge avail-
able from the fossil record in the 1990s (7,9–13). In a recent analysis,
which charted the stratigraphic ranges of thousands of mammal species,
1
Instituto de Ecología, Universidad Nacional Autónoma de México, México D.F. 04510,
México.
2
Department of Biology, Stanford University, Stanford, CA94304, USA.
3
Department
of Integrative Biology and Museums of Paleontology and Vertebrate Zoology, University of
California, Berkeley, Berkeley, CA 94720–3140, USA.
4
Estación de Biología Chamela, Instituto
de Biología, Universidad Nacional Autónoma de México, Jalisco 48980, México.
5
Department of Ecology and Evolutionary Biology, Princeton University, Princeton, NJ
08544, USA.
6
Department of Biology, University of Florida, Gainesville, FL 32611–8525, USA.
*Corresponding author. E-mail: gceballo@ecologia.unam.mx
2015 © The Authors, some rights reserved;
exclusive licensee American Association for
the Advancement of Science. Distributed
under a Creative Commons Attribution
NonCommercial License 4.0 (CC BY-NC).
10.1126/sciadv.1400253
RESEARCH ARTICLE
Ceballos et al. Sci. Adv. 2015;1:e1400253 19 June 2015 1of5

extinction rates were measured over intervals ranging from single years
to millions of years, and the mean extinction rate and variance were
computed for each span of time (7). In this way, the background extinc-
tion rate estimated for mammals was estimated at 1.8 E/MSY, here
rounded upward conservatively to 2 E/MSY (that is, 2 extinctions per
100 years per 10,000 species). This is double the highest previous rough
estimate.
Those previously estimated background rates were primarily derived
from marine invertebrate fossils, which are likely to have greater species
longevity than vertebrates (10,15). Data deficiencies make it impossible
to conduct empirical analyses (as was done for mammals) for non-
mammal terrestrial vertebrates; therefore, we assume the background
rates of other vertebrates to be similar to those of mammals. This sup-
position leads to a more conservative assessment of differences between
current and past extinction rates for the vertebrates as a whole, com-
pared with using the very low background extinction rate derived from
marine invertebrates.
The analysis we present here avoids using assumptions such as loss
of species predicted from species-area relationships, which can suggest
very high extinction rates, and which have raised the possibility that
scientists are “alarmists”seeking to exaggerate the impact of humans
on the biosphere (26). Here, we ascertain whether even the lowest esti-
mates of the difference between background and contemporary extinc-
tion rates still justify the conclusion that people are precipitating a global
spasm of biodiversity loss.
RESULTS
Modern and background rates of vertebrate extinctions
Modern rates of vertebrate extinction were much higher than a
background extinction rate of 2 E/MSY. Among the vertebrate taxa
evaluated by the International Union of Conservation of Nature
(IUCN), 338 extinctions have been documented since 1500 [“extinct”
(EX), Table 1]. An additional 279 species have become either “extinct in
the wild”(EW) or listed as “possibly extinct”(PE), totaling 617 verte-
brate species summed over the three categories. Most extinctions have
occurred in the last 114 years (that is, since 1900; Table 1). Our esti-
mated “highly conservative”(that is, using data for EX species only)
and “conservative”(that is, by including EX, EW, and PE) modern ex-
tinction rates for vertebrates varied from 8 to 100 times higher than the
background rate (Table 2). This means, for example, that under the 2
E/MSY background rate, 9 vertebrate extinctions would have been
expected since 1900; however, under the conservative rate, 468 more
vertebrates have gone extinct than would have if the background rate
had persisted across all vertebrates under that period. Specifically, these
468 species include 69 mammal species, 80 bird species, 24 reptiles, 146
amphibians, and 158 fish.
Table 1. Numbers of species used in the Table 2 calculations of “highly conservative”and “conservative”modern extinction rates based on
the IUCN Red List (17). For the highly conservative rates, only species verified as “extinct”(EX) were included; for the conservative extinction rates,
species in the categories “extinct in the wild”(EW) and “possibly extinct”(PE) were also included.
Vertebrate taxon
No. of species, IUCN 2014.3
Highly conservative
rates (EX)
Conservative rates
(EX + EW + PE) No. of species
evaluated by IUCN
Since 1500 Since 1900 Since 1500 Since 1900
Vertebrates 338 198 617 477 59% (39,223)
Mammals 77 35 111 69 100% (5,513)
Birds 140 57 163 80 100% (10,425)
Reptiles 21 8 37 24 44% (4,414)
Amphibians 34 32 148 146 88% (6,414)
Fishes 66 66 158 158 38% (12,457)
Table 2. Elevation of “highly conservative”and “conservative”mod-
ern vertebrate extinction rates above background rate of 2 E/MSY (see
table S2 for calculations). For each assessment category, two periods are
shown: extinction rates computed from 1500 to the present, and from
1900 to the present.
Animal group
Elevation of modern rates with
respect to expected rates
Highly conservative Conservative
Since 1500 Since 1900 Since 1500 Since 1900
Vertebrates 8 22 15 53
Mammals 14 28 20 55
Birds 13 24 15 34
Reptiles 5 8 8 24
Amphibians 5 22 22 100
Fishes 5 23 12 56
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Variation in modern extinction rates through time
Modern extinction rates have increased sharply over the past 200 years
(corresponding to the rise of industrial society) and are considerably
higher than background rates (Fig. 1). Rates of modern extinctions vary
among vertebrate groups (Fig. 1). For example, amphibians, comprising
of ~7300 species, show an accelerating rate of extinction: only 34 extinc-
tions have been documented with a high level of certainty since 1500,
yet >100 species have likely disappeared since 1980 (17,23). This may
not only reflect real trends but also a shortage of data for groups for
which most species are not yet evaluated, such as reptiles and fish
(21,22).
Modern extinctions if background rate had prevailed
Our results indicate that modern vertebrate extinctions that occurred
since 1500 and 1900 AD would have taken several millennia to occur
if the background rate had prevailed. The total number of vertebrate
species that went extinct in the last century would have taken about
800 to 10,000 years to disappear under the background rate of 2 E/MSY
(Fig. 2). The particularly high losses in the last several decades accentu-
ate the increasing severity of the modern extinction crisis.
DISCUSSION
Arguably the most serious aspect of the environmental crisis is the loss
of biodiversity—the other living things with which we share Earth. This
affects human well-being by interfering with crucial ecosystem services
such as crop pollination and water purification and by destroying
humanity’s beautiful, fascinating, and culturally important living
companions (4,5,15,27–30).
Our analysis shows that current extinction rates vastly exceed
natural average background rates, even when (i) the background rate is
considered to be double previous estimates and when (ii) data on mod-
ern vertebrate extinctions are treated in the most conservative plausible
way. We emphasize that our calculations very likely underestimate the
severity of the extinction crisis because our aim was to place a realistic
“lower bound”on humanity’s impact on biodiversity. Therefore, al-
though biologists cannot say preciselyhow many species there are, or
exactly how many have gone extinct in any time interval, we can con-
fidently conclude that modern extinction rates are exceptionally high,
that they are increasing, and that they suggest a mass extinction under
way—the sixth of its kind in Earth’s 4.5 billion years of history.
Cumulative extinctions as % of IUCN-evaluated species
1.60
1.40
1.20
1.00
0.80
0.60
0.40
0.20
0
1500-1600 1600-1700 1700-1800 1800-1900 1900-2014
Time interval
Mammals
Birds
Vertebrates
Other vertebrates
Background
A
Cumulative extinctions as % of IUCN-evaluated species
2.50
2.00
1.50
1.00
0.50
0.00
1500-1600 1600-1700 1700-1800 1800-1900 1900-2010
Time interval
Mammals
Vertebrates
Birds
Other vertebrates
Background
B
Fig. 1. Cumulative vertebrate species recorded as extinct or extinct in the wild by the IUCN (2012). Graphs show the percentage of the number of
species evaluated among mammals (5513; 100% of those described), birds (10,425; 100%), reptiles (4414; 44%), amphibians (6414; 88%), fishes (12,457;
38%), and all vertebrates combined (39,223; 59%). Dashed black curve represents the number of extinctions expected under a constant standard
background rate of 2 E/MSY. (A) Highly conservative estimate. (B) Conservative estimate.
Fishes Amphibians Reptiles Birds Mammals Vertebrates
10000
8000
6000
4000
2000
0
Times (years)
Very conservative
Conservative
Fig. 2. Number of years that would have been required for the ob-
served vertebrate species extinctions in the last 114 years to occur un-
der a background rate of 2 E/MSY. Red markers, highly conservative
scenario; blue markers, conservative scenario. Note that for all vertebrates,
the observed extinctions would have taken between 800 to 10,000 years to
disappear, assuming 2 E/MSY. Different classes of vertebrates all show qual-
itatively similar trends.
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Ceballos et al. Sci. Adv. 2015;1:e1400253 19 June 2015 3of5

A final important point is that we focus exclusively on species, ignor-
ing the extirpation of populations—the units relevant to ecological
functioning and the delivery of ecosystem services (4,5,29). Population
extinction cannot be reliably assessed from the fossil record, precluding
any analysis along the lines of that presented here. Also, although it is
clear that there are high rates of population extinction (18), existing data
aremuchlessreliableandfarhardertoobtainthanthoseforspecies,
which will remain true for the foreseeable future. Likewise, we have not
considered animals other than vertebrates because of data deficiencies.
The evidence is incontrovertible that recent extinction rates are un-
precedented in human history and highly unusual in Earth’shistory.
Ouranalysisemphasizesthatourglobal society has started to destroy
species of other organisms at an accelerating rate, initiating a mass ex-
tinction episode unparalleled for 65 million years. If the currently
elevated extinction pace is allowed to continue, humans will soon (in
as little as three human lifetimes) be deprived of many biodiversity
benefits. On human time scales, this loss would be effectively permanent
because in the aftermath of past mass extinctions, the living world took
hundreds of thousands to millions of years to rediversify. Avoiding a
true sixth mass extinction will require rapid, greatly intensified efforts
to conserve already threatened species and to alleviate pressures on their
populations—notably habitat loss, overexploitation for economic gain,
and climate change (31–33). All of these are related to human popula-
tion size and growth, which increases consumption (especially among
the rich), and economic inequity (6). However, the window of oppor-
tunity is rapidly closing.
MATERIALS AND METHODS
To estimate modern extinction rates, we compiled data on the total
number of described species and the number of extinct and possibly
extinct vertebrate species from the 2014 IUCN Red List (17). In the
IUCN’s list, extinct species can be viewed as the minimum number
of actual extinctions during recent human history (that is, since 1500)
because it lists species known to be extinct (EX), extinct in the wild
(EW), and possibly extinct (PE, a subcategory within “critically
endangered”reserved for species thought to be extinct, but not con-
firmed) (17) (table S1). We used the IUCN data to calculate modern
extinction rates in two ways: (i) we estimate a “highly conservative mod-
ern extinction rate”by using the data exclusively on species listed as EX,
and (ii) we calculate a “conservative extinction rate”by including also
both EW and PE species (table S2). Including these latter two categories
recognizes that there is only a slim chance that most of the species in
those categories can reestablish viable populations in their native habi-
tats. In terms of biological impact and the provision of ecosystem
services, we consider EW and PE species to be functionally equivalent
to EX species: even if some individuals still exist, their abundances are
not sufficient to have a substantial influence on ecological function and
processes.
The IUCN’s list is considered the authoritative, albeit likely conserv-
ative, assessment of the conservation status of plant and animal species.
About 1.8 million species have been described since 1758 (when the cur-
rent nomenclature system was developed), of which 1.3 million are
animals (3,17). Of these animal species, about 39,223 (of the currently
counted 66,178) vertebrate species have been formally assessed and re-
ported in the 2014 IUCN Red List (17). In the IUCN sample, mammals,
birds, and amphibians have had between 88 and 100% of their known
species evaluated, whereas only 44% of reptiles and 38% of fish species
have been assessed (Table 1). We focus our comparisons on vertebrates
becausetheyarethegroupforwhichthemostreliabledataexist,both
fossil and modern.
To produce conservative comparisons with modern extinctions, we
assumed a background extinction rate of 2 E/MSY as the highest likely
baseline average background extinction rate (7); that is, we should ex-
pect 2 extinctions per 10,000 vertebrate species per 100 years. That
background extinction rate was empirically determined using the ex-
ceptionally good fossil records of mammals, combining extinction counts
from paleontological databases and published literature on the fossil, sub-
fossil, and historical records (7).Usingtheresultinghighbackgroundex-
tinction rate provides a stringent test for assessing whether current modern
extinction rates indicate that a mass extinction event is under way. Previous
estimates of background extinction rates for other taxa are invariably
lower than the mammal-derived estimate of 2 E/MSY used here.
SUPPLEMENTARY MATERIALS
Supplementary material for this article is available at http://advances.sciencemag.org/cgi/content/
full/1/5/e1400253/DC1
Table S1. Definitions of IUCN categories (17) used to assess modern extinction rates.
Table S2. Estimation of modern extinction rates since 1500 and 1900.
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Acknowledgments: We would like to thank B. Young for helping us with the data on “possibly
extinct species”published by IUCN. J. Soberon, C. Mendenhall, and J. Pacheco gave valuable
suggestions on the manuscript. Funding: This work has been supported by the Programa de
apoyo a proyectos de investigación e innovación tecnológica from UNAM. Competing
interests: The authors declare that they have no competing interests.
Submitted 23 December 2014
Accepted 1 May 2015
Published 19 June 2015
10.1126/sciadv.1400253
Citation: G.Ceballos,P.R.Ehrlich,A.D.Barnosky,A.García,R.M.Pringle,T.M.Palmer,
Accelerated modern human–induced species losses: Entering the sixth mass extinction. Sci.
Adv. 1, e1400253 (2015).
RESEARCH ARTICLE
Ceballos et al. Sci. Adv. 2015;1:e1400253 19 June 2015 5of5