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Saving a Million Species

EXTINCTION RISK FROM CLIMATE CHANGE

Edited by Lee Hannah

o ISLAND PRESS

Wlr ~lil(IJ1I 1( 11111 11 1 lIlItiml

Chapter 11

Quaternary Extinctions and Their Link

to Climate Change

BARRY W BROOK AND ANTHONY D BARNOSKY

Millennia before the modern biodiversity crisis-a wo rldwide event Iiing driven by the multiple impacts of anthropogenic global 11 lnge-a mass extinction oflarge-bodied fauna occurred After a milshy11111 years ofsevere climatic fluctuations during which the earth w(L(ed lId waned benveen frigid ice ages and warm interglacials with apparshy1ild y few extinctions hundreds of species of mammals flightless l lilds and reptiles suddenly went extinct over the course of the last O()()O years (Barnosky 2009) Due both to our intrinsic fascination i iii huge prehistoric beasts and to the possible insights these wideshyIII hl species losses might lend to the modern extinction problem rill Ill )stery of the megafaunal (large animal) extinctions have led to 1IIlI vil ri1wrizing modeling and digging (for their fossils or environshy111 11111 proxies) over the last 150 years (Martin 2005) The topic ll linllts to invoke strong scientific interest (Koch and Barnosky (l()( Crlyson 2007 Gillespie 2008 Barnosky and Lindsey 2010 ~ J I I I II ~ - lklVO et )1 2010 Price et al 2011)

III Ihis dllptltr we t(gtClI S on recent work that explicitly considers il l I ~ LII ive ruk of larur)1 climate change compared to nonclimate 111 111 1111 cllIscd li1nIIcmiddotnillg processes (stich as habitat loss and huntshy1111 ) ill Iki vill 11ll IIH)llllIll1 11 nrilllliuns Wl hegin with a short I I IV c i I hI )Iuhd pIIIII 1i I)t (~II IIlrl1 1 ry lX Ii n~ 1 iOlls and Sill 1111) 1shy

I I I 111111 1IIII d 11Iit II wllv 111 1 lIlillll1 lt IlIi)hl ill 1 lIli ~ ld lli )

I ~V

IHO EVIDENCE FROM THE PAST

vldn trable to direct human impacts and climate change We then ex IIII IIL how the pattern of megafaunal extinction corresponds to borh I I I chronology ofhuman expansion and climate change and their pro ( Inl impacts Taken together this body of information leads us (0

t t IIld I Id t that climate change alone did not drive the mass extinctioll II 11Il Quaternary megafauna but overlain on direct and indirect htl 111111 IClioIlS it exacerbated overall extinction risk tremendously Thl 11 1l( IIIIIIIC message is that the synergy of fast climate change wilh III I I dirclT human impacts can have particularly fatal consequencl~ ll III III V Iionhuman species-and this is particularly true today wh~1l 111 1111111 ildhl L IlCeS including climate disruption are so dramaticallv II 111 111 111 Ihcy have ever been in the past

I~x t incrion and Vulnerability ofMegafalma

1111 lid () IIIIInLlry (late Pleistocene and Holocene) die-offs COI11

I 1 (1 I ilIi1i ~ 1I11 global mass extinction event which led to the eli III 11 111 11111 II hdt lit 111 mammal species heavier than 44 kilograms (100 I 11111) llleI 1I1 II~T brglt-bodied fauna across most continents (Au I liil I Ii l Norlll alJd South America) and large islands (West I II cI 11 MldI)ISI lr alld Nltw Zealand) between 50000 and 600 yell 1 111 1( 111 (Koch and Barnosky 2006) The losses included large 1111111111 11 (Lmiddotg mammoth genus Mammuthus) reptiles (eg gialll l I lIeI ~ lIdl 1 MCJlatlnia) and huge flightless birds (eg New (1 111111 11111 lIId Ausrralian Genyomis) In Australia around fifty spccic lilt Ilid i1Il rli i noceros-size wombats Short-faced kangaroos and prltd1 I I I I IISI II IlS disappltared (MacPhee 1999) In North America 1111 el lllll Inll was SOI11lt sixty species of large mammals plus the laq(hl l ile1 lIld orroiscs and South America saw the disappearance o( 11 1(11 ~ix l ymiddotsix Iarglt-Jl)lt1111maJ species Eurasia and Mrica were less 1I 1le Ii ii 11 II IVll Ihctss saw major losses in their large-mammal faulI I d 11 lIld 8ltvcmetn specics respectively Region by region these n 1iIt lin ll IVCllrS f()lIowni within a few centuries to a few millenlli 1 IIIi 11 111 di8pLrS 11 or 1-l00YUlsapiens to new lands and wne parricularly W

11 1 ( IV hl lI I hty Were also ltl1twined with changes in rhc ng ioll )I

1II bII lIill1lI~ SYI~llJ l (fig II - I )

SCI IVII W IS Ihl 111 IS IIlCChlIIisll1 hdlind dlls( eX Iilll l inns I 1111 1111111 111 Ill hlll h The drivers 11fIilil (xlililliIIIlS PII lilt l I ~t lll Ill lf i 11 ~ lIq 1Jii llIy din illill I Iill IIVII (Nit Ii llll 1

1--shy

Quaternary Extinctions and Their Link to Climate Change 181

-40kyr~ 135 kyr~ 1gt 4 2 1 1 2 3P 15

~~---i~~~] 17middot 115 115 3 ISO 13f lcyr I~i= 11C~1 Holocene

~lt~rJ3

~Jj~locene I 0i~

-r ~ 6 t

I ~O kyr II 51~O gt16

1 ~7244k -- II 4q 28 I __ yr I

------

Relative size of extinctshyfi nu608 of extinction Correlations in time Numbers indicate how taxon icon corresponds - many genera have robust to relative magnitude of L oJ Humans arriveMoslly Human dating control evidence

Moslly Climale extinction Number of bull Climatic change except as indicated extinct genera is listed

InsuHicient data Provisional evidence on each icon Needs more work

I I Ie 11( JT-I Late Quaternary megafaunal extinctions human hWlting and dishylilol lt ( lange on the continents The dashed box indicates the credible bounds of IIi I IrsI arrival of modern people Homo sapiens sapiens with the best estimate adshyi III In the human figure (the latest estimate for Australia is about 48000 years III Iky r BP]) Substantial climate change events predominantly the last glacial Iii 1 il I IlIlI1 lnd Holocene warming are indicated by gray shading inside boxes III ( Koch and Barnosky 2006

111) ) hut plausibly include (i) being outcompeted by newly evolved II I Illvtsive spccies (ii) failing to adapt to long-term environmental I 101 II l (e g climatic shifts) and (iii) reduction in abundance caused 11 1IIIdpm disturbance events (eg epidemics severe storms) with a IIi wllIlm bilurlt to recover to a viable population (Blois and Hadly ( 1))) C()llJlllOllly cited glt llcralization is that larger-bodied verteshy

1111 (w illl Ihe Lxtrctne rccwr t()rm being the Quaternary megashy11111101 ) 111 111011 eXtillCrio1-prone IhlIl smaller bodied ones (Bodmer I I iI 1))7 McKilIHY II)()) In IlISl hody sizc is inversely cor-

I Ioj Id Willi 11111 i I iI 111 1 h It lit d lIlirnlls rLnd ro hlt kss

111 EVIDENCE FROM THE PAST

11 IIIlld 1I1r and so more intrinsically vulnerable to rapid change and deshyIllographic disruption Indeed when armed with some knowledge of (llIpiridly well established biological scaling rules (allometry Dashy111111 h 1981) such a hypothesis makes a lot ofsense Large-bodied anshyIII 11 Is such as elephants or whales produce only a few precocious offshy11 Iillg but invest substantial resources into their care This life-history IIIIlY kads to the death of juveniles being a major demographic setshyIbull Ide ()II a population-wide basis even an apparently small additional 1-11 0 chronic mortality can result in rapid declines in abundance llld within a few centuries a collapse to extinction (Brook and Johnshy(111 2()()6 Nogues-Bravo et al 2008) The extinction proneness of IIIC bodied animals is further enhanced because of other correlated 11 lil s such as their requirement oflarge foraging area greater food inshy11( high habitat specificity and lower reproductive rates (West and I ~i( WII 2(05)

Why thcn (in evolutionary terms) be big Three reasons are that III~( ~llil11al s arc long-lived (so have multiple attempts at reproducshyIic 11) have relatively better heat regulation and water retention than 111111 lI1inJais cmd have lower predation rates especially when herdshyIII) Their size protects them from all but the biggest predators thcy 11 11It 1 great capacity to ride out hard times by drawing on their fat reshymiddotC middotI Irs rhc) can migrate long distances to find water or forage and t1lC y Lall ()pt not to reproduce in times when environmental condi II IIS IIT unt1vorablc such as during a drought (Brook et al 2007) IIIIIS ill Ihe majority of circumstances being big is good because il

IC I~ IS 1 demog raphic buffer Indeed such ecological specializatioll I 11i Is Ic evolvc repeatedly because in relatively stable environments

~ I 1 1 Illisl species tend to be better than generalists at particular narrow 11middotk Ilmvevtr when an envirorunent is altered abruptly at a rail 11 II lie )lIn11 bKkgrollnd change speciallst species with narrow cco I IIc 11 jllItn nlcs bear the brunt of progressively wlfavorable contli II IS Sll l h as habitat loss degradation and invasive competitors (ll

I II 111 IIIS ( Blllllf(lrd 1996 Harcourt et al 2002) An extremc CVC III III It I~ 1 holide strike ttOI1l space (Haynes 2008) or an inrclligC III 1 l1l w Iclding bipedal ape (Martin 200) tbar also widely allrl 1I IIoI middotIPIS by pracrices such IS burning and farming can be rbc k vcl 11111 IIIIIJillglmiddotS Illl uplill1ality ofrhis r(gu larly evolved srrat(gy ol lI lc I Iy iIImiddot

IIH middotll viIClnllllmiddot1I1l1 (()III~XI lI11II Y P~middotI)tII1( middot 11 1I ~ c) IIdps di (tII l III III 1 11 Ii ) 11 I~ I)IIII I ( Ic dllll1(middot CII IIl) VImiddot 1 IIImiddotCmiddotmiddotmiddotI middot lclI illlmiddotIIIIlI WIIlII

Quaternary Extinctions and Their Link to Climate Change 183

hunted by invading prehistoric people in Pleistocene Australia arboshyreal (tree-dwelling) species occupying closed forests suffered far fewer extinctions than saVaru1a (grassland) species and of the latter group tbose with high per capita population replacement rates (eg grey kangaroos Macropusgiganteus) or the ability to escape to refuges such as burrows (eg wombats Vombatus ursinus) were best able to persist (Johnson 2005)

The Role ofHuman Arrivals

During the last 100000 years modern humans have spread across the world from their center of origin in Africa reaching the Middle East by 90000 years ago Australia by 48000 years ago (based on tlle most s(cure evidence presently known Gillespie et al 2006) Europe by 40000-50000 years ago SoutllAmerica by 14600 years ago NOrtll America by 13000 years ago most of the Pacific Islands by 2000 lears ago and New Zealand by 800 years ago (For dates estimated by radiocarbon dating the radiocarbon age is calibrated to calendar I(ltlrs ) This wave ofhuman dispersal was likely to have been medlated hy climate change a wet penultimate interglacial probably encouraged 111 ( spread of early Homo sapiens out of Africa and in the Northern Ilcmisphere end-Pleistocene immigration into tlle Americas was fashyilirated by glacial ice sequestering water and lowering sea levels which in turn exposed a land bridge between Eurasia and North l1l erica and opened coastal migration routes At the very end of tlle Ikistocene it was global warming that melted ice and opened an iceshyII n CI )rridor through central Canada for a wave of Clovis hlUlters

A striking feature ofthe megafaW1al extinctions is tllat in every mashyl 1 Illstance where adequate data exist the extinction follows the first Illi vd of people on a virgin continent or large island within a few

111111l11(d to a few thousand years (fig 11-1) This point is further unshy1I IK(lred in figure 11-2 which shows the short overlap period for well 1I 1(llllc4aflllnal remains and archeological artifacts in New Zealand r~ I 1111 America and Australia based on the latest dating and sample seshyI Ii III protocols (Gi llespie 2008) (Note the different time scales on 1111 1o middotIN 1 B and ( - rh(se three (vents wcre not synchronous in time) I 111 111 idenemiddot donl is nor sulri(iC1l1 evidence for causation but this con-I 1111 Y11 I hI vny kI ~ 1 1)1( )vil k s sl)( 1I1g LirCIln1Sr111rial support for the

It I 11111 1 1111111111 pn 111 ( VI 1 lit middot middotS ~ IIV plrc l )nd i I ion 1)1 H( I lcrar~middotd

IH4 EVIDENCE FROM THE PAST

A_ ~ Rattus exulans = amp rat-gnawed seeds

-====

Moaeggshell

1shyNew Zealand

~ooo 1500 1000 500 0 -500 -1000 -1500 -2000 -2500

Calendar Age (years caiAOBC)

B ~ Clovis-age ~ Archaeology

i ~

Mammuthus Smilodon fatalis amp Canis dirus

~ -shyNorth America

~

10 15 20 25 30 35 Calendar Age (ka calBP)

c ~ Archaeology - 1middote charcoal

indirect OSL

Extinct megafauna

direct CSUS-ESR amp c gelalin

Australia

(1 30 35 40 45 50 55 60 65 70 75 80 85 90 Calendar Age (ka)

1I11 I I1IU 11 - 2 Dating data on human-megafauna overlap in New Zealand (A) N III I h AnHri ca (B) and Australia (C) The dates are stacked from youngest (tol ) I 1 il-SI (htIITom) for the archeology (dark shading) and oldest (top) to younglt (I lit lIll ) li) Ihe animal remains or proxies (light gray shading) Bars rcprtS11i jdtilll IIIhcrrlillfies SOl1lce Gillespie 2008 (includes detailed legend)

111(1 11 1111)11 lXrin lt tioI1 lspcltiaJly given the evidence that mo~t o( 11 II XI illl l IIX I slirvi vltd through pnvioLls ltqllllly pronounced Cli vi 11 III

11 11111 IlllllIrh II ioll~ bd(lI( humuls uTivnl

fllIlIwi IiiII oj illdincl lvidlIl III1I ~ 1 111)111 l~~rssill-- jOlllllv 1i1( IIIgt1I l i N( ill 1111111111 lhlllldlIh lld 1111 1 11IIIIII IIIil IIII1 T 1

Quaternary Extinctions and Their Link to Climate Change 185

fauna We are a species that broke a fundamental ecological rule large predators and omnivores are typically rare (Tudge 1989) A recent analysis by one ofus (Barnosky 2008) has shown that in achieving ecoshylogical dominance a rising biomass of people ultimately and permashynently displaced tl1e once-ablmdant biomass of megafauna The point well illustrated in figure 11-3 is that when the species richness ofmegashyfauna crashed to todays low levels their equivalent total biomass was replaced by one species (Homo sapiens) Indeed we surpassed the norshymal prehistoric levels ofmegafaunal biomass when tl1e Industrial Revshyolution commenced and now when combined with our livestock vastly outweigh the biomass ofmammal faunas ofthe deep past- an exshyplosion of living tissue supported primarily by the use of fossil energy (which for example makes it possible to produce and distribute inorshyganic fertilizers) The energetic trade-off between a large human bioshymass (lots ofpeople) and a large nonhuman biomass (lots ofother speshycies) demonstrated by tl1is Pleistocene history has a dear conservation implication to avoid losing many more species as the human populashyIion grows in tl1e very near future it will be necessary to formulate polishycies that recognize and guard against an inevitable energetic trade-offat the global scale The pressing need is to consciously channel some meashysure of natural resources toward supporting otl1er species ratl1er than

bull Megafauna Loss vs Global Human Population Growth bull

C) Q)

1 Q) Q

()

III c J III 1ii Ol Q)

2 0 ill

0 E l

400 1 q

350 -

300

250

200

150

100

50

Australia

~I Eurasia Beringia -- Americas-

~I f B ~ t ~ o It) It) ~

14

12

10

80

60

40

20

00

0 X c 0

-sect J Q 0 (L

bull Z

100000 10000 1000

Years before Present

Il t 11 11(1 1 -3 Dcclinc in glohl1111lgaEllma hiodiversity (number of species light 111 ) ll t r rh t il~r g IKi ll - ill rg l l c i ~ 1 cyrle plottld against tbe increase in world i 1111111 i(lll ~i lt (111011-10 l11irllI 1111111 lXlill Iioll evel1t~ by (t)ntincllt arc indishy 11 1 Iy I II k )11) IIIIIW I 1111 101 111111 oi Y IIS hdc Irc pl~lIlI) solrce IIII lI kl OOH

I H(l E V IDE NeE FRO M THE PAS T

~ e lldy toward humans for example in the form of enhanced sustainshyIhk farming practices and stepped-up efforts to protect and expand exshyiSI ing nature reserves Also critical will be developing alternatives toI l ~sil fuels for the energy that currently sustains the global ecosystem ~ IIL c iall y humans so far above its pre-anthropogenic level of megashy1111111 hiomass

Iluman impacts on late Quaternary enviromnents were many and Iried (Barnosky et aI 2004 Lyons et aI 2004a) The role of prehisshyIlli( pcople as hunters of big and small game has been reviewed exshyIlIlsi vdy (Martin 2005 Surovell et al 2005 Grayson 2007) meat IVIS (learly a component of the hunter-gatllerer lifestyle (Bulte et al ()()(l) blll killing may have also occurred for reasons beyond subsisshy

11 111 I (eg hunter prestige) Beyond direct predation however hushy111 ~lT llI ro have stressed megafauna by burning vegetation on a 111 II I ~I Ipl Sllk (and in doing so perhaps radically altering local dishyIII I Milln ct Ji 2005) and by introducing commensal species such pi 01 11) (Iinkl 2005) rats (Duncan et al 2002) and disease (Lyons C II W()Ih) Ovcrkill the hunting of a species at a level sufficient to

It iV( il 11 nl ill( ion with or without an additional pressure from facshyIe 1 H I IS hahirar modification and clin1ate change has been shown 11111 vilhle killing mcchanism for megafawlal species (fig 11-4) if II H 1111111 CIS t1so could LIse other species when they deplete the original 111 )11 specilts Ixlow viable ablmdances (Bodmer et al 1997 Alroy I()O I Bruok and Johnson 2006)

Role ofClimate Change

Nidlc Illodding indicates strong correlation between specific climale VII ilhkmiddots and spccies distributions (Hijmans and Grallam 200() Ne I) IIIS Bravo ct ai 2008) and it now seems clear that climate i ~ I

k(y drlC rtllill ~lIlr ofwhether or not a species can exist in a given 10Clk

1111 lik l hUll1an imp1cts climatic impacts on species are direct and ill tlil ~ I I Direcr impacrs incilide exccedin~ physiologically imposed rnll 11 11111 1lt t llli prnipirarioll limits on a species such as criticalrcmpcl1 1111 ( I I rs II0 Ids li)r J1lllsk oxen o r pikas whieh have limited heal-lo1 Ihilil i(s Il1Ilill ll irnpa(t~ incilidc misrnarch o f lil( histOry SFlll ) ill I I illlill) lr ~( ISllIlS or nlhl1 dim1 ie plrIIIKrCIS (phcllology) 11_1 111111 VlIlll g illg (111111 lIihnnllillll I(Hll ad y ill I Ill ~ plilll IlIl i lll

Quaternary Extinctions and Their Link to Climate Change 187

1000 A

750

500

250

1000

1 c 1000~ 750

ll iii

750 500

c 0

ltU S

500 I 250

C-o n 250

0 0 100 200 300 400 500

Year

FiGURE Ii-4- Overkill by the selective harvest of juveniles (less than 6 years old) of ) simulated population of the extinct giant marsupial Diprotodol~ Ifptatum Solid line is the total regional population (can)i ng capacity = 1000) and the (barely visible toward the bottom ofeach graph) dotted line is the annual number ofjuveshyniles killed by hunting (human population size = 150) (A) Constant hunting offshylake (B) Type II functional response (asslU11cS prey are naivc) (C) Type III funcshyrional response (assumes adaptive prey and higher hunting pressnre) Source

I ~ rook and Johnson 2006

snowmelt has exposed critical food resources (Parmesan 2006 Barshy

11osky 2009) Although numerous examples of climatic change stimulating

Changes in local abundance or geographic range changes exist there are I ~w examples ofclimate change causing worldwide extinction in tlle abshyI IKe of any other biotic stressor Examples such as the golden toad l~li) perigle11es) and harlequin frogs (genus AtelOp~H) may qualify

(1lrl11esan 2006) for recent times and in deeper time the demise of Ilish dllt (Megaloceras) in Ireland and horses (Equus) and short-faced 11 ~ lrs (Arct()du~ ) in Beringia seems artributable mainly to late PleisshyI ilL CIllo climate changes (lhrnosky 1986 Gutllrie 2003 Barnosky et tI 2()04 Koch ~lIld Bamosky 20(6) Although available models fail to Ifqlllld y simllble Il)cg1 tJlIll 11Ixtincrions based on climate change tI 1 Il ( Hre )()k lIld Hllov111111 200middot1 I Y()IlS 11 11 20041) model i ng ltthd

I H(l E V IDE NeE FRO M THE PAS T

~ e lldy toward humans for example in the form of enhanced sustainshyIhk farming practices and stepped-up efforts to protect and expand exshyiSI ing nature reserves Also critical will be developing alternatives toI l ~sil fuels for the energy that currently sustains the global ecosystem ~ IIL c iall y humans so far above its pre-anthropogenic level of megashy1111111 hiomass

Iluman impacts on late Quaternary enviromnents were many and Iried (Barnosky et aI 2004 Lyons et aI 2004a) The role of prehisshyIlli( pcople as hunters of big and small game has been reviewed exshyIlIlsi vdy (Martin 2005 Surovell et al 2005 Grayson 2007) meat IVIS (learly a component of the hunter-gatllerer lifestyle (Bulte et al ()()(l) blll killing may have also occurred for reasons beyond subsisshy

11 111 I (eg hunter prestige) Beyond direct predation however hushy111 ~lT llI ro have stressed megafauna by burning vegetation on a 111 II I ~I Ipl Sllk (and in doing so perhaps radically altering local dishyIII I Milln ct Ji 2005) and by introducing commensal species such pi 01 11) (Iinkl 2005) rats (Duncan et al 2002) and disease (Lyons C II W()Ih) Ovcrkill the hunting of a species at a level sufficient to

It iV( il 11 nl ill( ion with or without an additional pressure from facshyIe 1 H I IS hahirar modification and clin1ate change has been shown 11111 vilhle killing mcchanism for megafawlal species (fig 11-4) if II H 1111111 CIS t1so could LIse other species when they deplete the original 111 )11 specilts Ixlow viable ablmdances (Bodmer et al 1997 Alroy I()O I Bruok and Johnson 2006)

Role ofClimate Change

Nidlc Illodding indicates strong correlation between specific climale VII ilhkmiddots and spccies distributions (Hijmans and Grallam 200() Ne I) IIIS Bravo ct ai 2008) and it now seems clear that climate i ~ I

k(y drlC rtllill ~lIlr ofwhether or not a species can exist in a given 10Clk

1111 lik l hUll1an imp1cts climatic impacts on species are direct and ill tlil ~ I I Direcr impacrs incilide exccedin~ physiologically imposed rnll 11 11111 1lt t llli prnipirarioll limits on a species such as criticalrcmpcl1 1111 ( I I rs II0 Ids li)r J1lllsk oxen o r pikas whieh have limited heal-lo1 Ihilil i(s Il1Ilill ll irnpa(t~ incilidc misrnarch o f lil( histOry SFlll ) ill I I illlill) lr ~( ISllIlS or nlhl1 dim1 ie plrIIIKrCIS (phcllology) 11_1 111111 VlIlll g illg (111111 lIihnnllillll I(Hll ad y ill I Ill ~ plilll IlIl i lll

Quaternary Extinctions and Their Link to Climate Change 187

1000 A

750

500

250

1000

1 c 1000~ 750

ll iii

750 500

c 0

ltU S

500 I 250

C-o n 250

0 0 100 200 300 400 500

Year

FiGURE Ii-4- Overkill by the selective harvest of juveniles (less than 6 years old) of ) simulated population of the extinct giant marsupial Diprotodol~ Ifptatum Solid line is the total regional population (can)i ng capacity = 1000) and the (barely visible toward the bottom ofeach graph) dotted line is the annual number ofjuveshyniles killed by hunting (human population size = 150) (A) Constant hunting offshylake (B) Type II functional response (asslU11cS prey are naivc) (C) Type III funcshyrional response (assumes adaptive prey and higher hunting pressnre) Source

I ~ rook and Johnson 2006

snowmelt has exposed critical food resources (Parmesan 2006 Barshy

11osky 2009) Although numerous examples of climatic change stimulating

Changes in local abundance or geographic range changes exist there are I ~w examples ofclimate change causing worldwide extinction in tlle abshyI IKe of any other biotic stressor Examples such as the golden toad l~li) perigle11es) and harlequin frogs (genus AtelOp~H) may qualify

(1lrl11esan 2006) for recent times and in deeper time the demise of Ilish dllt (Megaloceras) in Ireland and horses (Equus) and short-faced 11 ~ lrs (Arct()du~ ) in Beringia seems artributable mainly to late PleisshyI ilL CIllo climate changes (lhrnosky 1986 Gutllrie 2003 Barnosky et tI 2()04 Koch ~lIld Bamosky 20(6) Although available models fail to Ifqlllld y simllble Il)cg1 tJlIll 11Ixtincrions based on climate change tI 1 Il ( Hre )()k lIld Hllov111111 200middot1 I Y()IlS 11 11 20041) model i ng ltthd

IHH EVIDENCE FROM THE PAST

Il)pirical evidence has shown climate change alone to cause extinctions t(species ranges are restricted by barriers that prevent them from movshyillg to track their needed climate space (Barnosky 19862009 Thomas 1 1 2004) It is precisely this latter situation in which the worlds 111111 (and flora ) today find themselves

Ihe late Quaternary was a period ofmajor natural climate change (Iig Il-5) The most prominent events were the glacial-interglacial cyshylt ks which have repeated thirty-nine times over the last 18 million ymiddotlrs the last nine cycles show about a 100000-year periodicity DurshyiIlg Iltese shifts in climate the globally averaged temperature changed hy 4 6 degrees Celsius-comparable in magnitude to but at a much middot1 IIV~T rate than that predicted for the coming century due to anthroshyII( ) SII ic g-Iobal warming under the fossil fuel-intensive business-asshy11 1111 ~rllwmiddotio (AIFI http wwwipccchIPCC2007)Triggered by ltl1 lgt ill1 Ie )rcing and reinforced by albedo changes (ice-sheet retreat or ) 1 i wilt ) IS well as the feedback of terrestrial and oceanic greenhouse

9 7

11 4 ~ 1i cII MIU)

NIl o l j

Tv Tv TVII TvII T~X - 1

~ ~ ~ 1 I t- - - ~ - - v~ d

- - - shy - 1J 1i ~

~ lt~ ~ 11 middotmiddotmiddot middotu Ii11111

I

lJ 100 200 300 400 500 600 700 000 Age (kyr BP)

ill( i IIltl l II 5 lltarctic icc corc record of polar temperature (top dClitcriulll dil I)

111 ( 1Ih III Ii il xide rOllcclltrlIion (bortoll1 ) for the pas 800000 yea rs I I wi I Ii Id lillnl show m t11l IC1l1pelature and c~rholl dioxid e vllll e~ over diflIllt ilill I 110 Mllinlt isotopc SI I~CS arc in illliltgt 111(1 b ~i III ~lIl lill l t i () Il ~ bylx (c I I) 11 I ll i IIIgtIIltmiddotk lillrs show till lilllillg 1 III IIIIIIIII (middot llilllliIS ill New 11

1 1 NI II ill 1I1lI i 1 11111 IISIIlIi 1 (k i 111 111 ) S 1111 M Idil i~middot1 1111111 1111111 I

d DOH

Quaternary Extinctions and Their Link to Climate Change 189

gas release the longer-term glacial cycles also were punctuated by nushymerous short-lived (and likely regional-scale) abrupt climatic changes such as the Younger Dryas Dansgaard-Oeschger and Heinrich climate events (Overpeck et al 2003) These short-term high-magnitude clishymatic changes probably exacerbated any stresses that the larger-scale glacial-interglacial shifts were placing on species although all of these kinds of cyclical cbanges seem within bounds of what species have evolved to withstand in the absence of impermeable geographic barrishyers (Barnosky 2001 Barnosky et al 2003 Benton 2009)

Mechanistically climate change over the last 100000 years changed vegetation substantially in many parts of the world although rhe naUlre and magnitude of the changes were different in different places (Barnosky et al 2004) In central North America for example rhe end-Pleistocene witnessed a relatively rapid transition of vegetashy1io nal struculre and composition from a heterogeneous mosaic to a 1I10re mnal pattern that was relatively less suitable to large herbivores (Graham and Lundelius 1984 Guthrie 1984) Abrupt events such as he Younger Dryas probably superimposed even more rapid vegetashyI ion shifts (Sulart et al 2004) In Australia the climate became more trid as the depth of an ice age was approached and the surface water Ivailable to large animals would have become scarcer and more patch~ il y distributed (Wroe and Field 2006) Yet most megafauna species IJlpear to have persisted across multiple glacial-interglacial transitions lill y to become extinct within a few thousand years of and in some I~es coincident with the most recent one (fig 11-5 extinctions 1IIIrked with black vertical bars)

I he resilience ofspecies can be inferred from the fossil record and 1111 )kcular markers (Lovejoy and Hannah 2005) In the Northern I k misphere populations shifted ranges southward as the Fennoscanshy1 1 111 u Ki Laurentide ice sheets advanced (or persisted in locally equashyIoli nJugia Hewitt 1999) and then reinvaded northern realms durshy1I1 illterglacials Some species may have also persisted in locally 1IIilrlhle rdllgia that were otherwise isolated within the ntndra and il I I rewn landscapes (Hewitt 1999) In Australia large-bodied i 1111 I1111 Is were able to persist throughout the Quaternary (Prideaux et II I -to()7h) even in remarkably arid landscapes such as the Nullarbor l ldll ( Iridcwx ~t 11 2007 )

1lllIC wltn nun y lilll los durillg IIH h~r 100000 years when the I 11111111 PIIltlIll y ~ 11 iii rrl Ill II II 1iY Ii wrm middotw~r conditions and lid I~ 1) lill (Ii I I (I 1gt 1~ ld 1111 III C( lIllIld ill lorC d l ll) 1 point

i 1)0 EVIDENCE FROM THE PAST

Calcium concentration (ppb)

Range of dated extinctions 0 400 80 120

o Madagascar NZ and Hawaii I

West Indies and Mediterranean I

North America I 20

Eurasia

40

Australia I

80

100

Thousands of years before present

1 11 illIW II Ct G rccnland ice core calcium concentrations (parts per billion) OWl

till IWI 100000 yca rs Low values indicate wet-warm conditions with relativcly d1Ioil1 vL ~l rarivL (ovcr and high values point to a cool-dry climate with spars

11 hd wllarion Also marked are the last glacial maximum YOlmger Dry iI 11I il III lling cvcnt and the Holocene warm period The timing of extincriuw bull II ill1ld ~ 1ld (OlltinUlts is indicated also shown are the earliest and latest cxtilll

II t1I N III Ik rillg ia with Eurasia Source Burney and Flannery 2005

i( illlltgtncd by Ilew stable isotope data from Australia as described ill 111)Ilk 1 1 (2007) )nd summaries presented in recent reviews (lbl III I ~ky l l d 2004 Koch ltlnd Barnosky 2006) Although such challg 1I11111111hrldly ltd to the disappear~l11ce of various species in local 111

1111 1 lrrrn l r1Hir abllllllalHe whcre they rcmained 0 11 the hnd~c1 1l(

II V( Illlv1ns riley persisted regionally or gloh~lI y lJnrii Ihc die-Ilil o I 1IIIIIn middotd ill r1h 11SI liw rens of J)lillllllli l 01 11ll Plcisl()(tnc 1I1d illill 1111 I hllll(IIlmiddot II dilllll( d l1I1( WII 1 dli vlI III Ihost tXlimlillllll 1 1111 111 l1 lllillII11I 1 11111111lt1 rill 111I1I1I 11l1l1ld lllh1I 111111

~

Quaternary Extinctions and Their Link to Climate Change 191 t

ing (in comparison to previous glacial-interglacial transitions) at that time negatively affect such a wide range of species and habitats (Burshyney and Flannery 2005 Johnson 2005) to the extent that onceshyabundant ecologically dominant animals simply disappeared The anshyswer to this question probably lies in threat synergies

Threat Synergies Past and Present

The Pleistocene megafaunaI die-offs provide a salutary lesson about the future of biodiversity under projected global warming scenarios Over most of the last 2 miilion years there was a lack ofwidespread exshytinctions particularly of plants (Willis et ai 2004) despite regular bouts of extreme climatic fluctuations (fig 11-5) So what made the last glacial cycle different We believe it was the synergy ofmutually reshyinforcing events brought by the double blow of anthropogenic threats and natural climate change Together these produced a demographicshyecological pressure of sufficient force and persistence to eliminate a ~izeable proportion of the worlds megafauna species (Barnoslcy et al 2004 Brook 2008 Barnosky 2009 Blois and Hadly 2009)-a group whose evolved life-history strategy left them particularly vulnershyable to chronic mortality stress from a novel predator and modifier of habitats (Brook and Bowman 2005) Without humans on the scene dimate change would not have been enough

A good example of this interaction using a method of coupling hioclimate envelopes and demographic modeling in woolly mammoth Nogues-Bravo et al 2008) shows how the human-climate synergy

pmbably operated in the High Arctic The model indicates that mamshyIlloths survived multiple Pleistocene climatic shifts by condensing II H ir geographic range to suitable climate space during climatically unshy1lvorable times Finally however the new presence of modern hu-11I IIlS during the late-Pleistocene and Holocene at the same time as a liJll1tically triggered retraction of steppe-tundra reduced maximally

Id ll blc habitat by some 90 percent (fig 11-7) resulted in extinction 111lt important message is that mammoth populations resilience was middot1kemd by habitat loss and fragmentation as it may weil have been II I plv iolis inrcrgl1Cia is bur during that last range reduction the 1Il lIl1ll1olhs wen 1111lhk III CIgtPI hlCllISc olrhe addition of predatory 1111 111 (and po~si hl y IIlhl I 11I111~ Il( Illodifications) by human 111111 middot111

11)2 EVIDENCE FROM THE PAST

I11 111111 II 7 (1imlI( lI1velope model of habitat suitability in Eurasia for woolly 111 11111111 Ill (M I11NNUtfJUS primigenius) at five times over the last interglacial-glacialshy1I11 1I I it Lyk (hrk( shading indicates higher suitability Full glacial condishyI ill ll l 111 I I1Jll I 11 21000 years before present (kyr BP) warm conditions (as warm I Wl l lm 111 111 I()day) at 126 and 6 kyr BP The white lines indicate hlcely northshy1111 lin Iii I J1(l)pk Line is dotted where there is uncertainty about the limit 01 111111(111 IHIIHl1lS Source Nogues-Bravo et al 2008

III princip le the same sort of fatal synergy is now attacking many -pllics bu t in a much magnified way Modern climate change is ocshyI IIITiII ~I t a ml1ch faster rate than past events (Barnoslcy et al 2003) II id hCP~111 in ) world that was already relatively hot because warming lIrlnl ill 111 interglacial ratller than in a glacial By 2050 the planet is lI jrlIld ro be hotter than it has been at any time since humans I l l li ved ~lS a species And the backdrop of human pressures on whilth tid r Xl le11l dimate change is taking place is more pronounced thall IWI hdhr in rhe twenty-first century the human enterprise reacil lts illll) -tli W 11le rs or rile planet (Brook et aI 2008) Not only arc oW

111 1gt 111) d1c d iml e irsdfro change (Miller ct aI 2(05) but thanks I() IHII tlllt lll y hi h popul1rioll tknsi ry 1I1d ongoing popu lation g rowlll ( III II ~) lXlv11sivv lppropri lli()11 nrnHIIItI ( lpir11 H1d recl1llolugi ltI IXIIIISil l1 (i ld1 lll (1 tI 2()()7) WI II(l illli li11) m()lL Ih 1I1 LVCI 1)( lllil 1)llIn pl~ il ll1ilil ) iii IrI k 1111 11 111 I1tI lId)IIII IS dimlll IIII 11illl V i ll III 11 II n II II (0 11 111 111 11 f01 III 11 II I I w( 11 V i111iI

Quaternary Extinctions and Their Link to Climate Change 193

ing a similar collision of human impacts and climatic changes that caused so many large animal extinctions toward the end of the Pleisshytocene But today given the greater magnitude ofboth climate change and other human pressures the show promises to be a wide-screen technicolor version of the (by comparison) black-and-white letterbox drama that played out the first time arotmd

Conclusions

The important message from the late Quaternary megafalmal extincshytions is not so much that humans caused extinctions in many (maybe most) places and climate caused them in others Rather the key point is that where direct human impacts and rapid climate change coincide fatalities are higher and faster than where either factor operates alone It is the synergy that presents the biggest problem and that synergy is exactly what we find ourselves in the middle of today Indeed synershygies between seemingly different causal mechanisms seem to characshyterize mass extinctions in general (Barnoslcy et al 2011)

Today that intelligent predatory ape tlle human species is driving a planetwide loss and fragmentation of habitats overexploitation of populations deliberate and accidental introduction ofalien species beshyyond their native ranges release of chemical pollution and tlle global disruption of the climate system Most damaging of all is tlle interacshytions among tllese different threats which mutually reinforce each inshydividual impact Are the modern extinctions resulting from these proshycesses a much magnified version of what already happened once to canse the late Quaternary megafauna extinctions and can this perspecshyImiddotivc illuminate how to chart the future to avoid an even more severe hiotic collapse The emerging consensus quite clearly says yes and Ihat conclusion in turn implies that only a systems-based approach to til reat abatement will be effective in staving off future extinctions

Conversely coming at the problem from trying to figure out what vllIscd Quaternary extinctions the question Was it humans or natushy111 I i111 ate change that t(xever ended the evolutionary journey ofhtmshydrcds of mcgabllnal species is the wrong one to ask That question i1 111 ic ip ~ltcs ) unicaud IllCchlIJisrn which might be appealing on parsishyillOllioliS gT() 1I11d~ hIli 111Iltll hlt ~lIpported by fossil archeological I l i lll ll()l()g i~middot tI l1ltlllltllldill) (vi dclI lmiddot( IllSI ~lS I()r our modern global IlHliv(rs il y Ii i 1111 ililll (1 1 ()VI1IlIJllring) mil) dotl1i shy11 111 III 1111 II( I 1111 I 11 1111111111111 111111 111 1 d- (1 1 1 ~ p(middot i middot

I

1)4 EVIDENCE FROM THE PAST

disappearing off a mountaintop that heats up too much) But at the global scale synergy among the distinct proximate causes adds up to IIlOIC than the sum of each individual cause If one insists on a minishymalistic answer for what caused the late Quaternary extinctions it seems to be this the actions of colonizing and expanding prehistoric hllmans (primarily hunting and habitat modification) seems omnishypnscnt in the past global extinction (Brook et aI 2007 Gillespie

OOH) but in many cases species were left much more vulnerable beshy(lllSC of climate-induced range contractions and changes in habitat (JIllity (Guthrie 2006 Nogues-Bravo et al 2008)

The degree to which climate change was the straw that broke the ~ lInds back probably differed to some extent for each species of exshyr iIllt Quaternary megafauna and will only be really understood after (ktailed study of each extinct species (Koch and Barnosky 2006) But Ille bet that even natural climate change synergistically exacerbated tXtinctions when human pressures first increased is worrisome in the i11( )dcrn context The climate change is now far outside the bounds of whar is normal for ecosystems (Barnosky 2009) and the other kinds ()j 11lIman pressures on species are so much greater than Earth has ever seen In the end it will not only be the extent to which we can minishyIllize each individual cause of extinction-increasing human populashyri( gt11 and attendant resource use habitat fragmentation invasive spcshy(ils and now global warming-but also the degree to which we call Illinimizc the synergy between each separate cause that will determine jllSt how many species we lose

Aclmowledgments

lVt thank Marc Carrasco Kaitlin Maguire Lee Hannal1 and tIV( I

1I1lt) lymolls reviewers for constructive comments BWBs research (Ill (his topic was supported by Australian Research Council grlIli I )IOXX 1764 )lld ADBs by grant DEB-OS43641 from the US Nl i ( III d Slticllcc foundation

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Quaternary Extinctions and Their Link to Climate Change 195

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11111lt II W md ( N Ii l~ 2()()(1 Scicltlivc hUl1tingofjuveniles as a cause i ill iIl1l1(I(( 111 ihl middot I Ikl li i lilt IIISI rlli 1I1 Pkirocc ilc megafauna 1I1 11t 1 ~1111 SI IIIIIII I il) III

1l)6 EVIDENCE FROM THE PAST

llrook B W D M J S Bowman D A Burney T F Flannery M 1( Gagan

R Gillespie C N Johnson et al 2007 Would the Australian megafauna

have become extinct if humans had never colonised the continent QJtatershynary Science Reviews 26 560--64

Ilrook B W N S Sodhi and C J A Bradshaw 2008 Synergies among extincshy

tion drivers under global change Trends in Ecology and Epolution 23 453-60

IllIlte E R D Horan and J F Shogren 2006 Megafauna extinction A paleshy

oeconomic theory of human overkill in the PleistoceneJournal ofEconomic BehaviorampOtganization 59 297-323

lIlimey D A and T F Flannery 2005 Fifty millennia of catastrophic extincshy

tions after human contact Tiends in Ecology amp Evolution 20 395-401

I )lIllllth J 1981 Population density and body size in mammals Nature 290 699-700

I )III1Cal1 R P T M Blackburn and T H Worthy 2002 Prehistoric bird extincshy

tions and human hunting Proceedings ofthe Royal Society ofLomkm B - BiologshyiLfll Sciences 269 517-21

I i( lei S ] 2005 Mans best friend - mammoths wors t enemy A speculative esshy

sayan the role of dogs in Paleo indian colonization and megafaunal extincshytioll WorldArchaeology 37 11-25

( i Ilespie R 2008 Updating Martins global extinction model Ouaternary Scishycnce ReJJiews 27 2522-29

(illcspie R B W Brook and A Baynes 2006 Short overlap of humans and

megafauna in Pleistocene Australia Alcheringa Special Issue 1 163-85

(rl harn R W and E L Lundelius Jr 1984 Coevolutionary disequilibriulll

~nd Pleistocene extinction In Quaternary Extinctions A Prehistoric Revolushyion edited by Paul S Martin and Richard G Klein 223-49 Tucson Univer silY ofArizona Press

t 1 1gt ~ (l1l O 1( 2007 Deciphering North American Pleistocene extinctions

IIIwnal ofAnthropological Research 63 185-213

(lIlhric R D 1984 Alaskan megabucks megabulls and megarams The issul

(I IlcislOccne gigantism Contributions in Qpaternary Vel1ebrate Paleont(It~1Y

I Volmnc in Menwrial to John E Cuilday Carnegie Museum of Natural II i ~

IIHy Spccill Publication 8 482-510

( 111 IlI i I R D 2003 Rapid body size decline in Alaskan Pleistocene horses Iw

Ii gtrc cxrinctioll Nat~tre 426 169-71

(lIilllk R D 2006 New carbon dates link climatic change with hllJ1111l 01 lIi II iOIl llld Pleistocene extinctions Nature 441 207-09

I 11I lIlIrI A 11 - A Copperu and S A Parks 2002 Rarity specil lizlrioll 1111 0 1 illLlion in primates joumal ~fBi(ge(~fTrrtp~y 2lJ 445- 56

111 ) 11( ( V 200X Yollngcr Dryas hhHk IlllI S lnd 1 ilc RIlcholahren ll IlIillil

Ij1 ill Ngtrtil Irncri(l l rotrrtlh(JI III NIIiolllll I ItlOIIY ISitlltl ( l iS I lOS (IS20 2~

I I ( jll l vI II)) 1(gtIIlui rI 11 111111 11111 1111 111 111 lj llI lillIitI 101lIlillII(i l illIIII SO 1 1 111 II I I

Quaternary Extinctions and Their Link to Climate Change 197

Hijmans R ] and C H Graham 2006 The ability ofclimate envelope models

to predict the effect of clinlate change on species distributions Global Change Biology 12 2272-81

IPCC 2007 I ntetgopent1nental Panel on Climate Change Fourth Assessment Report (AR4) Available at http vrwwipccch

Johnson C N 2005 What can the data on late survival ofAustralian megafauna

tell us about the cause of their extinction QtaternalY Science Reviews 24 2167-72

Koch P L and A D Barnosky 2006 Late Quaternary extinctions State of the

debate Annual Review ofEcology Evolution and Systematics 37 215-50

Lovejoy T E and L Hmnah eds 2005 Climate Change and Biodivmity New

Haven Yale University Press Luthi D M Le Flodl B Bereiter T Blunier ]-M Barnola U Siegehnthaler

D Raynaud et al 2008 High-resolution carbon dioxide concentration

record 650000-800000 years before present Natme 453 379-82

Lyons S K F A Smith and] H Brown 2004a Of mice mastodons and men Human-mediated extinctions on four continents Evoltttiorla1Y Ecology Reseanh 6 339-58

Lyons S K F A Smith P J Wagner E P White and] H Brown 2004b Was

a hyperdisease responsible for the late Pleistocene megafaunal extinction

Ecology Letters 7 859-68 MacPhee R D E 1999 Extinctions in Near Time Causes Contexts and Conseshy

quences New York Klllwer AcademicPlemUTI Publishers

Martin P S 2005 Tivilitfht ofthe Mammoths Ice Age Extinctions and the Rell1ilding ofAmerica Berkeley University of California Press

McKinney M L 1997 Extinction vulnerability and selectivity Combining ecoshylogical and paleontological views Annual ReJJiIlV of Ecology and Systematics 28 495-516

1 iller G H M L Fogel ] W Magee M 1( Gagan S J Clarke and B] Johnshyson 2005 Ecosystem coUapse in Pleistocene Australia and a human role in

megafaunal extinction Science 309 287-90

Nogues-Bravo D J Rodigllez J Hortal P Batra and M B Araujo 2008 Clishymate change humans and the extinction of the woolly mammoth PLoS Bishyology 6 685- 92

NOfucs-Bravo D Ohlemuller R Batra P and Araujo M B 2010 Climate predictors oflate Quaternary extinctions Evolution 64 2442-49

( )vl lpck J T C Whitl()ck and B HlU1tley 2003 Terrestrial biosphere dynamshy

its in the climate system Pasr and future In Paleoclimate Global Change and he FutHrc cdited by R S Brldky T F Pedersen 1( D Alverson and K F Iklwnann RI- I () ~ Ikrli ll Springcr-Vcrllg

lIIIlIIsan C 2()()() I () I Ik d II Id (v()llIlionlry rcspollsc to recent climate

IIIIIII r 11111( 1IIigt o(iiloillv oIllioll Ilud SVmiddottImiddotNrttics 37 637- 69

I ( L ( I Wi I 1 1 X 111 A S MIIITY 1 N C()oke S A 11 kllllll 111111 II 101 1111 111111111 1I1i1IIlIlIl rI ~ s l i lhlillll i1I1

1l)6 EVIDENCE FROM THE PAST

llrook B W D M J S Bowman D A Burney T F Flannery M 1( Gagan

R Gillespie C N Johnson et al 2007 Would the Australian megafauna

have become extinct if humans had never colonised the continent QJtatershynary Science Reviews 26 560--64

Ilrook B W N S Sodhi and C J A Bradshaw 2008 Synergies among extincshy

tion drivers under global change Trends in Ecology and Epolution 23 453-60

IllIlte E R D Horan and J F Shogren 2006 Megafauna extinction A paleshy

oeconomic theory of human overkill in the PleistoceneJournal ofEconomic BehaviorampOtganization 59 297-323

lIlimey D A and T F Flannery 2005 Fifty millennia of catastrophic extincshy

tions after human contact Tiends in Ecology amp Evolution 20 395-401

I )lIllllth J 1981 Population density and body size in mammals Nature 290 699-700

I )III1Cal1 R P T M Blackburn and T H Worthy 2002 Prehistoric bird extincshy

tions and human hunting Proceedings ofthe Royal Society ofLomkm B - BiologshyiLfll Sciences 269 517-21

I i( lei S ] 2005 Mans best friend - mammoths wors t enemy A speculative esshy

sayan the role of dogs in Paleo indian colonization and megafaunal extincshytioll WorldArchaeology 37 11-25

( i Ilespie R 2008 Updating Martins global extinction model Ouaternary Scishycnce ReJJiews 27 2522-29

(illcspie R B W Brook and A Baynes 2006 Short overlap of humans and

megafauna in Pleistocene Australia Alcheringa Special Issue 1 163-85

(rl harn R W and E L Lundelius Jr 1984 Coevolutionary disequilibriulll

~nd Pleistocene extinction In Quaternary Extinctions A Prehistoric Revolushyion edited by Paul S Martin and Richard G Klein 223-49 Tucson Univer silY ofArizona Press

t 1 1gt ~ (l1l O 1( 2007 Deciphering North American Pleistocene extinctions

IIIwnal ofAnthropological Research 63 185-213

(lIlhric R D 1984 Alaskan megabucks megabulls and megarams The issul

(I IlcislOccne gigantism Contributions in Qpaternary Vel1ebrate Paleont(It~1Y

I Volmnc in Menwrial to John E Cuilday Carnegie Museum of Natural II i ~

IIHy Spccill Publication 8 482-510

( 111 IlI i I R D 2003 Rapid body size decline in Alaskan Pleistocene horses Iw

Ii gtrc cxrinctioll Nat~tre 426 169-71

(lIilllk R D 2006 New carbon dates link climatic change with hllJ1111l 01 lIi II iOIl llld Pleistocene extinctions Nature 441 207-09

I 11I lIlIrI A 11 - A Copperu and S A Parks 2002 Rarity specil lizlrioll 1111 0 1 illLlion in primates joumal ~fBi(ge(~fTrrtp~y 2lJ 445- 56

111 ) 11( ( V 200X Yollngcr Dryas hhHk IlllI S lnd 1 ilc RIlcholahren ll IlIillil

Ij1 ill Ngtrtil Irncri(l l rotrrtlh(JI III NIIiolllll I ItlOIIY ISitlltl ( l iS I lOS (IS20 2~

I I ( jll l vI II)) 1(gtIIlui rI 11 111111 11111 1111 111 111 lj llI lillIitI 101lIlillII(i l illIIII SO 1 1 111 II I I

Quaternary Extinctions and Their Link to Climate Change 197

Hijmans R ] and C H Graham 2006 The ability ofclimate envelope models

to predict the effect of clinlate change on species distributions Global Change Biology 12 2272-81

IPCC 2007 I ntetgopent1nental Panel on Climate Change Fourth Assessment Report (AR4) Available at http vrwwipccch

Johnson C N 2005 What can the data on late survival ofAustralian megafauna

tell us about the cause of their extinction QtaternalY Science Reviews 24 2167-72

Koch P L and A D Barnosky 2006 Late Quaternary extinctions State of the

debate Annual Review ofEcology Evolution and Systematics 37 215-50

Lovejoy T E and L Hmnah eds 2005 Climate Change and Biodivmity New

Haven Yale University Press Luthi D M Le Flodl B Bereiter T Blunier ]-M Barnola U Siegehnthaler

D Raynaud et al 2008 High-resolution carbon dioxide concentration

record 650000-800000 years before present Natme 453 379-82

Lyons S K F A Smith and] H Brown 2004a Of mice mastodons and men Human-mediated extinctions on four continents Evoltttiorla1Y Ecology Reseanh 6 339-58

Lyons S K F A Smith P J Wagner E P White and] H Brown 2004b Was

a hyperdisease responsible for the late Pleistocene megafaunal extinction

Ecology Letters 7 859-68 MacPhee R D E 1999 Extinctions in Near Time Causes Contexts and Conseshy

quences New York Klllwer AcademicPlemUTI Publishers

Martin P S 2005 Tivilitfht ofthe Mammoths Ice Age Extinctions and the Rell1ilding ofAmerica Berkeley University of California Press

McKinney M L 1997 Extinction vulnerability and selectivity Combining ecoshylogical and paleontological views Annual ReJJiIlV of Ecology and Systematics 28 495-516

1 iller G H M L Fogel ] W Magee M 1( Gagan S J Clarke and B] Johnshyson 2005 Ecosystem coUapse in Pleistocene Australia and a human role in

megafaunal extinction Science 309 287-90

Nogues-Bravo D J Rodigllez J Hortal P Batra and M B Araujo 2008 Clishymate change humans and the extinction of the woolly mammoth PLoS Bishyology 6 685- 92

NOfucs-Bravo D Ohlemuller R Batra P and Araujo M B 2010 Climate predictors oflate Quaternary extinctions Evolution 64 2442-49

( )vl lpck J T C Whitl()ck and B HlU1tley 2003 Terrestrial biosphere dynamshy

its in the climate system Pasr and future In Paleoclimate Global Change and he FutHrc cdited by R S Brldky T F Pedersen 1( D Alverson and K F Iklwnann RI- I () ~ Ikrli ll Springcr-Vcrllg

lIIIlIIsan C 2()()() I () I Ik d II Id (v()llIlionlry rcspollsc to recent climate

IIIIIII r 11111( 1IIigt o(iiloillv oIllioll Ilud SVmiddottImiddotNrttics 37 637- 69

I ( L ( I Wi I 1 1 X 111 A S MIIITY 1 N C()oke S A 11 kllllll 111111 II 101 1111 111111111 1I1i1IIlIlIl rI ~ s l i lhlillll i1I1

IIX EVTDENCE FROM THE PAST

Pleistocene Darling Downs eastern Australia The promise and pitfalls of

dating as a test ofextinction hypotheses Quaternary Science Reviews 30 899shyl) 14

1Jtall x G J J A Long L K Ayliffe J c Hellstrom B Pillans W E Boles

M N Hutchinson et al 2007a An arid-adapted middle Pleistocene veneshyhrate fauna from south-central Australia Nature 445 422-25

I id(IU X G J R G Roberts D Megirian K E Westaway J c Hellstrom and

J I Olley 2007b Mammalian responses to Pleistocene climate change in ~()lItheastern Australia Geology 35 33-36

i llll i lI W P J Crutzen and J R McNeill 2007 The Anthropocene Are hushy

Ian~ now overwhelming the great forces of nature Ambio 36 614-21

0 111111 A J P A Kosintsev T F G Higham and A M Lister 2004 Pleisshylocene to Holocene extinction dynamics in giant deer and woolly mamshyoth Nature 431 684-89

Slirovell T N Waguespack and P J Brantingham 2005 Global archaeological

I vidcnce for proboscidean overkill Proceedings ofthe National Academy ofScishytn ce~ USA 102 6231-36

I middottomas C D A Cameron R E Green M Balltkenes L J BeaLUTIont Y C (ollingham B F N Erasmus et al 2004 Extinction risk from climate change Nature 427 145--48

1lulgc C 1989 The rise and fall of Homo sapiens sapiensraquo Philosophical Transacshyfilms ~fthe Royal Society ofLondonB 325 479-88

WtSl ( bull g and J H Brown 2005 The origin of allometric scaling laws in biolshy

ogy Iiom genomes to ecosystems Towards a quantitative unifYing theory of

hiolvgical structure and organization Journal of Experimental Biology 208 I S7S- 92

Willi ~ K ) K D Bennett and D Wall(er 2004 The evolutionary legacy ofthr

Ir Ages Philosophical Transactions ofthe Royal Society of London B - Biologicfll SIi11ICS ~59 157-58

W 11 S Ind J Field 2006 A review of the evidence for a human role in the ex

I ill t l iOIl of Australian megafauna and an alternative interpretation QuatI lilli Science Reviews 25 2692-703

Chapter 12

Quaternary Tropical Plant Extinction

A Paleoecological Perspective from

the N eotropics

MARK B BUSH AND NICOLE A S MOSBLECH

1

We have found no examples of global plant extinctions from the tropshyics within the Quaternary Examples ofextinctions over longer periods of time are readily documented within the fossil record with the loss ofwhole families evident between Eocene and modern times (Morley 2000 2007) Herein lies a clue to the problem of detecting extinction of tropical plants-the ta(onomic resolution of the fossil record

Most of the paleobotanical records that we have from the tropics are based on fossil pollen plus a few on wood and even less on seeds 1l1d other macrofossils With a few exceptions fossil pollen identiflCashytions are at the genus or family level and so an extinction sufficient to remove an entire genus would be the minimum detectable level of loss Because many tropical genera contain congeners that occupy very diHerent habitats losing all of them requires a huge change in the ecoshysy~tem or a lot of bad luck Over long enough periods of time evolushyI iOIl luck and continental-scale modifications of climate are possishyIlk and extinction does become evident Because of this taxonomic I)i l~ we actually have a clearer vision of extinction that took place beshyI wcn rhe Eoccn( lI1d rhe M ioccilc than we do across the much II Ie )In rill1csc lic e)f 111( (J II lr~TI 111) We can sec at that scale that major i lilll llic ( WillS 1t1d SItld i lin inil il rcd cycles of species loss and IPi i llil)tl II i s 111)1 1I1111I a)lllhk S IIPpCl~~ rhar the spread of fire

II)