Biological annihilation via the ongoing sixth mass extinction signaled by vertebrate population ...

206 Pages·2017·4.55 MB·English

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Biological annihilation via the ongoing sixth mass P
extinction signaled by vertebrate population
losses and declines
GerardoCeballosa,1,Paul R.Ehrlichb,1,andRodolfoDirzob
aInstitutodeEcología,UniversidadNacionalAutónomadeMéxico,MexicoCity04510,Mexico;andbDepartmentofBiology,StanfordUniversity,Stanford,
CA94305
ContributedbyPaulR.Ehrlich,May23,2017(sentforreviewMarch28,2017;reviewedbyThomasE.LovejoyandPeterH.Raven)
The population extinction pulse we describe here shows, from a especially because many of those species were obscure and had
quantitative viewpoint, that Earth’s sixth mass extinction is more limitedranges,suchastheCatarinapupfish(Megupsilonaporus,
severe than perceived when looking exclusively at species extinc- extinctin2014),atinyfishfromMexico,ortheChristmasIsland
tions.Therefore,humanityneedstoaddressanthropogenicpopula- pipistrelle (Pipistrellus murrayi, extinct in 2009), a bat that van-
tion extirpation and decimation immediately. That conclusion is ishedfromits namesakevolcanic remnant.
basedonanalysesofthenumbersanddegreesofrangecontraction Speciesextinctionsareobviouslyveryimportantinthelongrun,
(indicative of population shrinkage and/or population extinctions becausesuchlossesareirreversibleandmayhaveprofoundeffects
according to the International Union for Conservation of Nature) ranging from the depletion of Earth’s inspirational and esthetic
usingasampleof27,600vertebratespecies,andonamoredetailed resourcestodeteriorationofecosystemfunctionandservices(e.g.,
analysisdocumentingthepopulationextinctionsbetween1900and refs.17–20). The strong focusamong scientistsonspeciesextinc-
2015in177mammalspecies.Wefindthattherateofpopulationloss tions,however,conveysacommonimpressionthatEarth’sbiotais
interrestrialvertebratesisextremelyhigh—evenin“speciesoflow notdramaticallythreatened,orisjustslowlyenteringanepisodeof
concern.”Inoursample,comprisingnearlyhalfofknownvertebrate major biodiversity loss that neednotgenerate deep concern now
species, 32% (8,851/27,600) are decreasing; that is, they have de- (e.g., ref. 21, but see also refs. 9, 11, 22). Thus, there might be
creasedinpopulationsizeandrange.Inthe177mammalsforwhich sufficient time to address the decay of biodiversity later, or to
wehavedetaileddata,allhavelost30%ormoreoftheirgeographic develop technologies for “deextinction”—the possibility of the
rangesandmorethan40%ofthespecieshaveexperiencedsevere latter being an especially dangerous misimpression (see ref. 23).
populationdeclines(>80%rangeshrinkage).Ourdataindicatethat Specifically, this approach has led to the neglect of two critical
beyondglobalspeciesextinctionsEarthisexperiencingahugeepi-
aspectsofthepresentextinctionepisode:(i)thedisappearanceof
sodeofpopulationdeclinesandextirpations,whichwillhavenega-
populations,whichessentiallyalwaysprecedesspeciesextinctions,
tivecascadingconsequencesonecosystemfunctioningandservices
and(ii)therapiddecreaseinnumbersofindividualswithinsome
vitaltosustainingcivilization.Wedescribethisasa“biologicalan-
of the remaining populations. A detailed analysis of the loss of
nihilation” to highlight the current magnitude of Earth’s ongoing
individualsandpopulationsmakestheproblemmuchclearerand
sixthmajorextinctionevent.
moreworrisome,andhighlightsawholesetofparametersthatare
| | | increasingly critical in considering the Anthropocene’s biological
sixthmassextinction populationdeclines populationextinctions
| extinctioncrisis.
conservation ecosystemservice
Significance
Thelossofbiologicaldiversityisoneofthemostseverehuman-
caused global environmental problems. Hundreds of species
Thestrongfocusonspeciesextinctions,acriticalaspectofthe
and myriad populations are being driven to extinction every year
(1–8).Fromtheperspectiveofgeologicaltime,Earth’srichestbiota contemporarypulseofbiologicalextinction,leadstoacommon
ever is already well into a sixth mass extinction episode (9–14). misimpressionthatEarth’sbiotaisnotimmediatelythreatened,
justslowlyenteringanepisodeofmajorbiodiversityloss.This
Mass extinction episodes detected in the fossil record have been
view overlooks the current trends of population declines and Y
measuredintermsofratesofglobalextinctionsofspeciesorhigher G
taxa(e.g.,ref.9).Forexample,conservativelyalmost200speciesof extinctions.Usingasampleof27,600terrestrialvertebratespe- OLO
cies, and a more detailedanalysis of 177mammalspecies, we C
vertebrateshavegoneextinctinthelast100y.Theserepresentthe E
showtheextremelyhighdegreeofpopulationdecayinverte-
loss of about 2 species per year. Few realize, however, that if
subjected to the estimated “background” or “normal” extinction brates, even in common “species of low concern.” Dwindling
population sizes and range shrinkages amount to a massive
rateprevailinginthelast2millionyears,the200vertebratespecies
anthropogenic erosion of biodiversity and of the ecosystem
losses would have taken not a century, but up to 10,000 y to dis-
services essential to civilization. This “biological annihilation”
appear,dependingontheanimalgroupanalyzed(11).Considering
underlinestheseriousnessforhumanityofEarth’songoingsixth
the marine realm, specifically, only 15 animal species have been
massextinctionevent.
recordedasgloballyextinct(15),likelyanunderestimate,giventhe
difficulty of accurately recording marine extinctions. Regarding
Authorcontributions:G.C.,P.R.E.,andR.D.designedresearch;G.C.andP.R.E.performed
global extinction of invertebrates, available information is limited
research;G.C.,P.R.E.,andR.D.contributednewreagents/analytictools;G.C.analyzed
and largely focused on threat level. For example, it is estimated data;andG.C.,P.R.E.,andR.D.wrotethepaper.
that 42% of 3,623 terrestrial invertebrate species, and 25% of Reviewers:T.E.L.,GeorgeMasonUniversity;andP.H.R.,MissouriBotanicalGarden.
1,306speciesofmarineinvertebratesassessedontheInternational
Theauthorsdeclarenoconflictofinterest.
UnionforConservationofNature(IUCN)RedListareclassified
FreelyavailableonlinethroughthePNASopenaccessoption.
asthreatenedwithextinction(16).However,fromtheperspective
1Towhomcorrespondencemaybeaddressed.Email:[email protected]
of a human lifetime it is difficult to appreciate the current mag-
[email protected].
nitude of species extinctions. A rate of two vertebrate species ex-
Thisarticlecontainssupportinginformationonlineatwww.pnas.org/lookup/suppl/doi:10.
tinctions per year does not generate enough public concern, 1073/pnas.1704949114/-/DCSupplemental.
www.pnas.org/cgi/doi/10.1073/pnas.1704949114 PNAS | PublishedonlineJuly10,2017 | E6089–E6096
In the last few decades, habitat loss, overexploitation, invasive species, particularly strong in mammals and birds, which largely
organisms,pollution,toxification,andmorerecentlyclimatedisrup- drivetheoveralllandvertebratepattern(Fig.3,Center).Notably,
tion,aswellastheinteractionsamongthesefactors,haveledtothe some parts of the planet harbor low absolute numbers of verte-
catastrophicdeclinesinboththenumbersandsizesofpopulationsof brate species undergoing decline (Figs. 2 and 3), such as those
both common and rare vertebrate species (24–28). For example, areas of low species richness located in hypercold (northernmost
several species of mammals that were relatively safe one or two locations,particularlyoftheWesternHemisphere)andhyperarid
decades ago are now endangered. In 2016, there were only (Saharan Africa and Central Asia) regions. However, it is in-
7,000 cheetahs in existence (29) and less than 5,000 Borneo and structivetoexaminetheircorrespondingproportionalnumbers,an
Sumatran orangutans (Pongo pygmaeus and P. abelli, respectively) aspectwediscussindetailinanothersectionbelow.
(28).PopulationsofAfricanlion(Pantheraleo)dropped43%since Thenumberofdecreasingspeciesofalllandvertebratesineach
1993 (30), pangolin (Manis spp.) populations have been decimated ofthe10,000-km2quadratsoverEarth’slandsurfacerangesfroma
(31),andpopulationsofgiraffesdroppedfromaround115,000indi- fewtomorethan365(Fig.2).Asexpected,largeconcentrationsof
viduals thought to be conspecific in 1985, to around 97,000 repre- decreasing vertebrate species occur in species-rich areas of moist
sentingwhatisnowrecognizedtobefourspecies(Giraffagiraffa,G. tropical forests adjacent to mountainous regions, such as the
tippelskirchi,G.reticulata,andG.camelopardalis)in2015(32). Andes–Amazonregion,theCongobasin-adjacenteasternAfrican
Animportantantecedenttoourwork(25)usedthenumberof highlands, and the Himalayas–south Asian jungle belt. The dis-
geneticpopulationsperunitareaandthenestimatedpotentialloss tribution of the number of decreasing species considering verte-
on the basis of deforestation estimates and the species–area re- brate classes separately reveals notable differences. First, the
lationship (SAR). Given the recognized limitations of the use of maximum number of decreasing species in a 10,000-km2 quadrat
SARtoestimateextinctions,ourworkprovidesanapproachbased variesfromahighvalueof296decreasingbirdsperquadrat,toa
onreductionofspeciesrangeasaproxyofpopulationextirpation. low maximum of 60 decreasing reptiles in a quadrat. Second,
The most recent Living Planet Index (LPI) has estimated that mammalsandbirdshaverelativelysimilardistributionpatternsof
wildlife abundance on the planet decreased by as much as 58%
between1970and2012(4).ThepresentstudyisdifferentfromLPI
andotherrelatedpublicationsinseveralways,includingthathere
we use all decreasing species of vertebrates according to IUCN,
mappingandcomparingabsoluteandrelativenumbersofspecies,
and focusing on population losses. Previous estimates seem vali-
datedbythedatawepresenthereonthelossoflocalpopulations
andtheseveredecreaseinthepopulationsizeofmanyothers(see
alsorefs.3,4,6–8,26).Hereweexaminethemagnitudeoflossesof
populationsoflandvertebratespeciesonaglobalsystemof10,000-km2
quadrats(Methods).Speciesvaryfromcommontorare,sothat
our analysis, which includes all land vertebrate species (am-
phibians,birds,reptiles,andmammals)deemedas“decreasing”by
IUCN, provides a better estimate of population losses than using
exclusivelyIUCNdataonspeciesatrisk.Obviously,commonspe-
ciesdecreasingarenotordinarilyclassifiedasspeciesatrisk.IUCN
criteria provide quantitative thresholds for population size, trend,
and range size, to determine decreasing species (28, 33). We also
evaluate shrinking ranges and population declines for 177 species
ofmammalsforwhichdataareavailableongeographicrange
shrinkage from ∼1900 to 2015. We specifically focus on local ex-
tinctions by addressing the following questions: (i) What are the
numbersandgeographicdistributionsofdecreasingterrestrialver-
tebratespecies(i.e.,experiencingpopulationlosses)?(ii)Whatare
thevertebrategroupsandgeographicregionsthathavethehighest
numbers and proportions of decreasing species? (iii) What is the
scale of local population declines in mammals—a proxy for other
vertebrates? By addressing these questions, we conclude that an-
thropogenicpopulationextinctionsamounttoamassiveerosionof
the greatest biological diversity in the history of Earth and that
populationlossesanddeclinesareespeciallyimportant,becauseitis
populations of organisms that primarily supply the ecosystem ser-
vicessocriticaltohumanityatlocalandregionallevels.
Results
PatternsofVariationinPopulationLossAmongVertebrates.Consid-
eringalllandvertebrates,ourspatiallyexplicitanalysesindicatea
massive pulse of population losses, with a global epidemic of
speciesdeclines.Thoseanalysessupporttheviewthatthedecayof
vertebrate animal life is widespread geographically, crosses phy-
logeneticlineages,andinvolvesspeciesranginginabundancefrom
commontorare(Figs.1–4).Thelosses,however,arenotuniform: Fig.1. Decreasinglandvertebrates,asexemplifiedwiththesefourspecies,
includetaxawithdifferentconservationstatus(e.g.,lowconcern,critically
some regions exhibit higher concentrations of species with local
endangered), current geographic range (e.g., large, very restricted), and
population extinctions than others, including a strong latitudinal
abundance(e.g.,common,rare).Thedataonconservationstatus,current
signalcorrespondingtoanintertropicalpeak(i.e.,roughlybetween geographicrange,andabundancearefromIUCN(28).Barnswallowimage
the Tropics of Cancer and Capricorn) of number of decreasing courtesyofDanielGarzaGalindo(photographer).
E6090 | www.pnas.org/cgi/doi/10.1073/pnas.1704949114 Ceballosetal.
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Fig.2. GlobaldistributionofterrestrialvertebratespeciesaccordingtoIUCN(28).(Left)Globaldistributionofspeciesrichnessasindicatedbynumberofspecies
ineach10,000-km2quadrat.(Center)Absolutenumberofdecreasingspeciesperquadrat.(Right)Percentageofspeciesthataresufferingpopulationlossesin
relationtototalspeciesrichnessperquadrat.Themapshighlightthatregionsofknownhighspeciesrichnessharborlargeabsolutenumbersofspeciesexpe-
riencinghighlevelsofdeclineandpopulationloss(particularlyevidentintheAmazon,thecentralAfricanregion,andsouth/southeastAsia),whereasthe
proportionofdecreasingspeciesperquadratshowsastronghigh-latitudeandSaharanAfricasignal.Inaddition,thereareseveralcentersofpopulationdeclinein
bothabsoluteandrelativeterms(Borneo,forexample).
decreasingspecies,exceptthatbirdshavemoredecreasingspecies andamphibiansclearlydifferfromeachotherinregionswherede-
inthetemperatezones.Third,mammalsandbirdshavepatternsof creasingspeciesareconcentrated.Forexample,therearemorede-
decreasingspeciesquitedistinctfromthoseofreptilesandamphib- creasing reptiles in the Eurasian and African continents, and more
ians(Figs.2and3),giventhatthelatterarerarerinthenorthernand decreasingamphibiansintheAmericas.
southerntemperateandsubpolarregions(bothareessentiallyabsent There is also great variation in the total population size and
fromtheArcticandaremissingfromtheAntarctic).Fourth,reptiles geographicrangesamongindividualspecies.Althoughthereisno
Ceballosetal. PNAS | PublishedonlineJuly10,2017 | E6091
Fig.3. Latitudinaldistributionofspeciesrichness(Left),decreasingspecies(Center),andthepercentageofspecies(Right)thataresufferingpopulation
lossesinrelationtototalspeciesrichness,ineach10,000-km2quadrat.Patternsofspeciesrichnessinrelationtolatitudearesimilarinallvertebrates,although
therearemorespeciesperquadratinbirdsandmammalsand,asexpected,ascarcityofreptilesandamphibiansathighlatitudes.Thepatternsofnumberof
specieswithdecreasingpopulationsindicatethatregionswithhighspeciesrichnessalsohavehighnumbersofdecreasingspecies,butthepercentageof
decreasing species in relation to species richness shows contrasting patterns between mammals and birds compared with reptiles and amphibians. In
mammalsandbirds,thepercentageofdecreasingspeciesisrelativelysimilarinregionswithlowandhighspeciesrichness.Incontrast,therearepropor-
tionallymoredecreasingspeciesofreptilesandamphibiansinregionswithlowspeciesrichness.
accurateinformationonpopulationsizeformosttaxa,whateveris decreasing populations varies from fewer than 100 individuals in
available indicates that the total population size in species with critically endangered species such as the Hainan black-crested
E6092 | www.pnas.org/cgi/doi/10.1073/pnas.1704949114 Ceballosetal.
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Roughly a third (8,851/27,600) of all land vertebrate species P
examinedareexperiencingdeclinesandlocalpopulationlossesof
a considerable magnitude (Figs. 2–4). Such proportion of de-
creasingspeciesvaries,dependingonthetaxonomicgroup,from
30%ormoreinthecaseofmammals,birds,andreptiles,to15%
inthecaseofamphibians.Furthermore,ofthedecreasingspecies,
many are now considered endangered (Fig. 4). Beyond that,
roughly30%ofalldecreasingspeciesarestillsufficientlycommon
that they are consideredof“low concern” byIUCN,ratherthan
“endangered.”Thatsomanycommonspeciesaredecreasingisa
strong sign of the seriousness of the overall contemporary bi-
ologicalextinctionepisode.
In our 10,000-km2 quadrats, the proportion of decreasing
speciesrangesfromlessthan10%tomorethan50%(Fig.2).The
geographic distributions of absolute (i.e., number) and relative
(i.e., percentage) of decreasing species is contrasting. Whereas
tropical regions have larger numbers of decreasing species, as
expected,giventheirhigherspeciesrichness,theircorresponding
proportionsarerelativelylow.Incontrast,temperateregionstend
Fig.4. ThepercentageofdecreasingspeciesclassifiedbyIUCNas“endangered” tohavesimilarorhigherproportionsofdecreasingspecies,atrend
(including“criticallyendangered,”“endangered,”“vulnerable,”and“near- dramaticallyprominentinthecaseofreptiles.
threatened”)or“lowconcern”(including“lowconcern”and“data-deficient”)
interrestrialvertebrates.Thisfigureemphasizesthatevenspeciesthathavenot Local Population Extinctions in Mammals. Our most detailed data
yetbeenclassifiedasendangered(roughly30%inthecaseofallvertebrates) allow comparison of historic and present geographic range of a
aredeclining.Thissituationisexacerbatedinthecaseofbirds,forwhichclose
sample of 177 mammal species (Figs. 5 and 6). Most of the
to55%ofthedecreasingspeciesarestillclassifiedas“lowconcern.”
177mammalspecieswesampledhavelostmorethan40%oftheir
geographicrangesinhistorictimes,andalmosthalfhavelostmore
gibbon (Nomascus hainanus), to many millions of individuals in than 80% of their ranges in the period ∼1900–2015. At the con-
decreasing common species such as the barn swallow (Hirundo tinental and subcontinental level, some patterns become evident
rustica). Similarly, the smallest ranges (i.e., <1 km2) are seen in (Fig.5).Thepredominantcategoryofrangecontractionis≥80%
speciessuchastheCarrizalseedeater(Amaurospizacarrizalensis) inAfrica(56%ofthesampledmammalspecies),Asia(75%ofthe
from Venezuela and Herrera’s false coral snake (Lampropeltis species),Australia(60%ofthespecies),andEurope(40%ofthe
herrerae) from Mexico,both denizens of tiny islands. The largest species).IntheAmericas,rangecontractionsarelessmarkedbut
ranges are hundreds of thousands of square kilometers, as in stillconsiderable:22%ofthespeciesinNorthAmericaand17%
the bush dog (Speothos venaticus) from South America and the ofthespeciesinSouthAmericahaveexperiencedrangecontrac-
common lizard (Zootoca vivipara) from Eurasia. The sum of tions of at least 80%. Nevertheless, 50% of the species in North
the 10,000-km2 quadrats representing the current ranges of the America and 28% of the species in South America have experi-
encedarangecontractionof41%ormore.
8,851decreasingvertebratespeciesis1,350,876quadrats.Ahighly
The comparison of the 1900–2015 geographic ranges showed
conservative estimate would indicate a similar number of local
that the 177 species of mammals have disappeared from 58,000
populationsfacing extinction.Thisis, ofcourse,a very roughes-
gridcells.Ontheassumptionthatonaverageeachofthe10,000-km2
timate of the total number of populations, as the number of
occupiedquadratsheldasinglepopulationofthespeciesfound
populations of a decreasing species in each quadrat largely de-
within it, this implies that roughly 58,000 populations of the
pends,asidefromsuitablehabitatdistributionwithinthequadrat,
177 mammals we examined have gone extinct. Consider the
on animal body mass and trophicposition (e.g., ref.34).The as-
sumptionofonepopulationper10,000km2mightseemverycon- followingemblematiccases:Thelion(Pantheraleo)washistorically
distributedovermostofAfrica,southernEurope,andtheMiddle
servative, as this area could accommodate many populations of
smallanimals(e.g.,0.1-kgrodents),mostofwhichcouldhavebeen
extirpated. However,10,000 km2maynot besufficient for,orcan GY
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barelyaccommodateaviablepopulationoflargecarnivores(saya OL
330-kg Siberian tiger; ref. 34). Nonetheless, our results provide EC
evidenceoftheextremelylargenumbersofvertebratepopulations
facingextinction,comparedwiththenumberofspecies.
Proportion of Vertebrate Species Decreasing. The proportion of
decreasingvertebratesshowsthatthereareareasacrosstheplanet
with high concentrations of decreasing species in all vertebrates
andregionswithhighproportionsofdecreasingspeciesofapar-
ticular group (Figs. 2, 3, and 5). For example, in mammals, the
highestpercentageofdecreasingspeciesisconcentratedintropical
regions,mostlyintheNeotropicsandSoutheastAsia,whereasin
reptiles,theproportionaldeclineconcentratesalmostexclusivelyin
Madagascar. Decreasing amphibians are prominent in Mexico, Fig.5. Thepercentageofspeciesoflandmammalsfromfivemajorconti-
CentralAmerica,thenorthernAndes,andBrazil’sAtlanticforest nents/subcontinents and the entire globe undergoing different degrees (in
percentage)ofdecline intheperiod∼1900–2015.Consideringthesampled
intheAmericas;WestAfricaandMadagascarinAfrica;andIndia
andSoutheastAsia,includingIndonesiaandPhilippinesinAsia– species globally, 56% of them have lost more than60% of their range, a
pattern that is generally consistent in Africa, Asia, Australia, and Europe,
SoutheastAsia.Finally,decreasingspeciesofbirdsarefoundover whereasinSouthAmericaandNorthAmerica,35–40%ofthespecieshave
largeregionsofallcontinents(Fig.2). experiencedrangecontractionsofonly20%orless.(Seetextfordetails.)
Ceballosetal. PNAS | PublishedonlineJuly10,2017 | E6093
Discussion
Ithasrecentlybeenshown,usingconservativeestimatesofcurrent
and background species extinction rates, that Earth is now in a
period of mass global species extinction for vertebrate animals
(11).But thetrueextent ofthis massextinctionhas been under-
estimated, because of the emphasis on species extinction. This
underestimate largely traces to overlooking the accelerating ex-
tinctionofpopulations.Whereasscientistshaveknownforalong
time that several relatively well-studied species have undergone
majorcontractionoftheirranges,experiencedconsiderablepop-
ulation decreases, and suffered many population extinctions, the
global extent of population shrinkage and extirpation has pre-
viouslynotbeenrecognizedandquantified.
Inaddition,somestudiesdocumentthatinvertebratesandplants
are suffering massive losses of populations and species (35–38).
Hereweextendinvestigationofmassextinctiontoterrestrialver-
tebratepopulationdecreasesandlosses,andgiveestimatesofthe
numberoftheirspecieswithdecreasingpopulations.Theaccuracy
oftheestimatesisstronglydependentonanunknownparameter,
namely, the actual average area occupied by a vertebrate pop-
ulation(e.g.,refs.35,39–41).However,evenifapopulationwould,
on average, occupy an area five times larger than what we have
used here (i.e., 50,000 km2) there would still be hundreds of
thousandsofpopulationsthathavesufferedextinctioninthepast
few centuries. On the other hand, most vertebrates (∼70%) are
small species of mammals, birds, reptiles, and amphibians. If, on
average, they have one population every10 km2 then vertebrates
wouldhavesufferedmorethanabillionpopulationextinctions.
Ourresultsshowthatpopulationextinctioninlandvertebrates
is geographically omnipresent, but with notable prominence in
tropical, species-rich regions. It is interesting, however, that
when population extinctions are evaluated as the percentage of
total species richness, temperate regions, with their typical low
speciesdiversity,showhigherproportions ofpopulation loss.
There are some illustrative qualitative examples of population
decreases and their consequences within terrestrial and marine
Fig.6. Percentageoflocalpopulationextinctionin177speciesofmammals
vertebrates, but ours is an attempt at a quantitative evaluation of
in1°×1°quadrats,asanindicationoftheseverityofthemassextinction
globaltrendsinpopulationextinctions.Recentreviewsindicatethat
crises. The maps were generated by comparing historic and current geo-
graphicranges(49)(SIAppendix,SIMethods).Notethatlargeregionsinall species extinctions, population decreases, and range contraction
continents have lost 50% or more of the populations of the evaluated (implying population extinctions) among terrestrial invertebrates
mammals.Becauseofthesmallsamplesize,biasedtolargemammalspecies, andplantsareassevereasamongvertebrates(e.g.,refs.35–38).For
thisfigurecanonlybeusedtovisualizelikelytrendsinpopulationlosses. example,long-termmonitoringofinsectpopulationsintheUnited
Kingdomshowsthat30–60%ofspeciespertaxonomicorderhave
contracting ranges (36). The situation in plants has been less
East,allthewaytonorthwesternIndia(SIAppendix,Fig.S1).Itis
evaluated; thus it is difficult to compare them with animals, but
nowconfinedtoscatteredpopulationsinsub-SaharanAfricaanda
thereislittlereasontobelievethattheextinctionsituationinplants
remnantpopulationintheGirforestofIndia.Thevastmajorityof
isdramaticallydifferent(37).Furthermore,researchshowsthatthe
lion populations are gone. In its African stronghold, it historically loss of animal populations indirectly leads to changes in plant
occupiedroughlytwothousand10,000-km2cells,andnowitisre- communities(20,37,39),frequentlycausingthereductionoflocal
ducedtosome600cells.Otherspecies,suchasthemountainlion speciesrichnessanddominanceofafewplanttaxathateitherex-
(Pumaconcolor),areknowntobedoingbetter.Themountainlion perience “ecological release” in response to decreasing herbivore
haslostsomeofitslocalpopulationsinNorthAmerica,buthasnot pressures(42,43),and/orexperiencepopulationreductionsdueto
suffered such disastrous losses as its Old World relative, adapting thedeclineofanimalsresponsibleforpollinationordispersal(e.g.,
relativelywelltohuman-dominatedlandscapes,anditisstillfound refs.2−3,20).Thestatusofbiodiversityamongmicroorganismsis
across85%ofitshistoricrange. toopoorlyknowntopermitustomakeanycomparisonandgen-
Clearly,theextinctionofmammalpopulations,althoughvarying eralizations about the current pulse of extinctions, although some
recent research has unraveled feedbacks between local large her-
from species to species, has been a global phenomenon (Fig. 6).
bivore defaunation and mycorrhizal richness (44, 45). Given what
Strikingly, thepredominant color codeinthe mammalian mapis
we know about genetic population differentiation, it is expected
that of 70% or more of population losses, with the exception of
thattherangecontractionsanddeclineswedocumenthereimplya
someareasofSouthAmericaandhighlatitudesofNorthAmerica.
considerable loss of intraspecific genetic diversity (23) but this is,
Particularlyhardhithavebeenthemammalsofsouthandsouth-
clearly,anaspectthatwarrantsfurtherinvestigation.
eastAsia,whereallofthelarge-bodiedspeciesofmammalsana- Insum,bylosingpopulations(andspecies)ofvertebrates,weare
lyzed have lost more than 80% of their geographic ranges. The losing intricate ecological networks involving animals, plants, and
CapeandSahararegionsinAfrica,centralAustralia,theeastern microorganisms(e.g.,refs.2,8,18,45,46).Wearealsolosingpools
UnitedStates,andtheAtlanticforestinSouthAmericahavealso ofgeneticinformationthatmayprovevitaltospecies’evolutionary
sufferedseverelyfrompopulationextinctions. adjustmentandsurvivalinarapidlychangingglobalenvironment.
E6094 | www.pnas.org/cgi/doi/10.1073/pnas.1704949114 Ceballosetal.
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Thissuggeststhat,eveniftherewasnotamplesignthatthecrisis (11, 48). All signs point to ever more powerful assaults on bio- P
extends far beyond that group of animals, today’s planetary diversityin the next two decades,painting adismalpictureof the
defaunation of vertebrates will itself promote cascading cata- futureoflife,includinghumanlife.
strophiceffectsonecosystems,worseningtheannihilationofnature
(2, 3, 46). Thus, while the biosphere is undergoing mass species Methods
extinction(11),itisalsobeingravagedbyamuchmoreseriousand Forfullmethods,pleaseseeSIAppendix.Wedeterminedthenumberofde-
rapidwaveofpopulationdeclinesandextinctions.Incombination, creasingvertebratespeciesusingtheIUCN(28)RedListofThreatenedSpecies.
theseassaultsarecausingavastreductionofthefaunaandfloraof IntheIUCN,speciesareclassifiedasdecreasing,stable,orincreasing(seealso
ourplanet.Theresultingbiologicalannihilationobviouslywillalso ref. 33). Either range contraction (population extinction) or reduction in
have serious ecological, economic, and social consequences (46). numbersinextantpopulationsdetermineswhetheraspeciesisdecreasing.We
Humanitywilleventuallypayaveryhighpriceforthedecimationof usedtheIUCNmapsofterrestrialvertebrates(i.e.,mammals,birds,reptiles,and
theonlyassemblageoflifethatweknowofintheuniverse. amphibians)tocreatetheglobalmapsofnumberofspecies(richness)andof
decreasingspecies,andpercentageofdecreasingspeciesinrelationtototal
Conclusion speciesrichness.Thedistributionofallofthespecieswassuperimposedina
22,000 grid of 10,000-km2 quadrats covering the continentallands. For the
Population extinctions today are orders of magnitude more fre-
grid,aLambertazimuthalequal-areaprojectionwasused(seeref.49forde-
quentthanspeciesextinctions.Populationextinctions,however,are
a prelude to species extinctions, so Earth’s sixth mass extinction tails of the projection methods).Inouranalysesa critical issue is how grid
squaresandpopulationscorrespond.Thisisaverydifficultproblemthatvaries
episodehasproceededfurtherthanmostassume.Themassiveloss
withdefinitionsofspecies.(Inthispaper,westickwiththeclassicbiological
ofpopulationsisalreadydamagingtheservicesecosystemsprovide
definitionofspecies.)Thenumberofpopulationsalsovariesfromspeciesto
to civilization. When considering this frightening assault on the species;forexample,ahighlyphylopatricspecieswouldhavemorepopulations
foundations of human civilization, one must never forget that persquarethanaveryvagilespecies,andspecieswithdifferentmatingsystems
Earth’s capacity to support life, including human life, has been would have different estimates of numbers of Mendelianpopulations, and
shaped by life itself (47). When public mention is made of the thesewouldnotbethesameasestimatesofnumberofdemographicunits
extinction crisis, it usually focuses on a few animal species (hun- (50).Forthepurposesofunderstandingtheannihilation,thesedifferencesare
dredsoutofmillions)knowntohavegoneextinct,andprojecting notcritical.Forexample,ifwehavelost90%ofthelion’sgeographicrange,
many more extinctions in the future. But a glance at our maps whetherthisamountsto10,000demographicunitsor4,000Mendelianpop-
presentsamuchmorerealisticpicture:theysuggestthatasmuchas ulationsistrivialinthepresentcontext.Itwouldbeextremelyusefulifwehad
50% of thenumberof animal individualsthat onceshared Earth muchmoreinformationonpopulationstructureforallvertebrates,butthisisa
major,pendingagenda.
with us are already gone, as are billions of populations. Further-
Thepopulationextinctionanalysiswasconductedon177mammalianspecies
more,ouranalysisisconservative,giventheincreasingtrajectories
occurringonfivecontinents.Specifically,weanalyzed54speciesinAfrica,14in
of the drivers of extinction and their synergistic effects. Future
Asia,57inAustralia,15inEurope,and35inAmerica.Thehistoricaldistribution
losses easily may amount to a further rapid defaunation of the
wasgatheredfromspecializedliterature(seedetailsinref.26)andthecurrent
globe and comparable losses in the diversity of plants (36), in-
distribution from IUCN (28). Historic and current ranges were digitized as
cludingthelocal(andeventuallyglobal)defaunation-drivencoex-
geographicinformationsystempolygonsandelaboratedinArcGis10.1(51).
tinctionofplants(3,20).Thelikelihoodofthisrapiddefaunation Foreachspecies,wecalculatedtheareaofthehistoricalandpresentdistri-
lies in the proximate causes of population extinctions: habitat bution(insquarekilometers)toestimatethepercentageoflostareaandthe
conversion, climate disruption, overexploitation, toxification, spe- percentageofareawherethespeciesareextant.Acaveatoftheseestimates
ciesinvasions,disease,and(potentially)large-scalenuclearwar— regardshowrepresentativethesampleof177speciesis.Werecognizeabiasin
alltiedtooneanotherincomplexpatternsandusuallyreinforcing thatthedataincludealargenumberofmedium-andlarge-sizedspecies,for
eachother’simpacts.Muchlessfrequentlymentionedare,however, whichthebestinformationisavailable.However,giventhatsuchmediumand
theultimatedriversofthoseimmediatecausesofbioticdestruction, largespeciesarethemostseriouslythreatenedbythepredominantproxi-
namely, human overpopulation and continued population matedriversofdefaunation(2,3),thelikelybiasagainstsmall-sizedspe-
growth,andoverconsumption,especiallybytherich.Thesedrivers, ciesshouldnotaffectouroverallinterpretationofresults.
allofwhichtracetothefictionthatperpetualgrowthcanoccurona
ACKNOWLEDGMENTS.WethankJohnHarteforveryhelpfulcommentson
finiteplanet,arethemselvesincreasingrapidly.Thus,weemphasize
themanuscriptandNoéTorres,GiuliaSantulli,andJesúsPachecofortheir
that the sixth mass extinction is already here and the window for
helpwithdataanalyses.TheUniversidadNacionalAutónomadeMéxico
effectiveactionisveryshort,probablytwoorthreedecadesatmost andStanfordUniversitysupportedourwork.
Y
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1 SUPPORTING
 INFORMATION

2

3 The
 real
 sixth
 mass
 extinction:
 Biological
 annihilation
 signaled
 by
 population
 losses

4 and
 declines
 in
 vertebrates

5

6 Gerardo
 Ceballos,1*
 Paul
 R.
 Ehrlich,2*
 Rodolfo
 Dirzo2

7

8

9 I.
 DATA
 ON
 DECLINING
 VERTEBRATE
 SPECIES

10

11 We
 obtained
 the
 list
 of
 vertebrates
 species
 considered
 as
 declining
 from
 the

12 International
 Union
 of
 Conservation
 of
 Nature
 (IUCN).
 We
 accessed
 the
 IUCN
 webpage

13 (www.iucn.org;
 version
 2015.3)
 on
 March
 2016.
 The
 complete
 list
 of
 species
 is
 shown

14 below.

15

16 II.
 POPULATION
 EXTINCTIONS
 IN
 MAMMALS

17 The
 analysis
 of
 population
 extinctions
 was
 done
 in
 177
 species
 of
 mammals
 occurring

18 in
 five
 continents.
 We
 analyzed
 54
 species
 in
 Africa,
 14
 in
 Asia,
 57
 in
 Australia,
 15
 in

19 Europe,
 and
 35
 in
 America.
 The
 historical
 distribution
 was
 gathered
 from
 specialized

20 literature
 (see
 details
 in
 Ceballos
 and
 Ehrlich
 2002);
 the
 current
 distribution
 from
 IUCN

21 (2015).
 See
 the
 historic
 and
 present
 lion
 (Panthera
 leo)
 distribution
 as
 an
 example
 (SI

22 Figure
 1).
 Historic
 and
 current
 ranges
 were
 digitized
 as
 GIS
 polygons
 and
 were

23 elaborated
 in
 ArcGis
 10.1
 (ESRI,
 2011).
 For
 each
 species
 we
 calculated
 the
 area
 of
 the

24 historical
 and
 present
 distribution
 (in
 squared
 kilometers)
 in
 order
 to
 estimate
 the

25 percentage
 of
 loss
 area
 and
 the
 percentage
 of
 area
 where
 the
 species
 are
 extant.
 We

26 estimated
 the
 number
 of
 species
 occurring
 historically
 and
 in
 the
 present
 in
 10376
 cells

27 of
 100
 km2
 on
 the
 five
 continents.
 So
 we
 were
 able
 to
 define
 in
 each
 continent

28 percentage
 of
 cells
 that
 lost
 the
 25%,
 50%,
 75%
 or
 100%
 of
 species
 and
 to
 map
 these

29 percentages
 in
 each
 continent.

30

31

1
32 Figure
 1.
 Historic
 (red)
 and
 present
 (blue)
 lion
 (Panthera
 leo)
 distribution.
 Note
 that

33 there
 is
 a
 single
 population
 left
 in
 Asia.
 Map
 from

34 http://brilliantmaps.com/distribution-­‐of-­‐lions/.

35

36

37

38

39

40

41

2