Unit III Geo
RESEA RCHARTICL E Climate-Related LocalExtinctions AreAlready Widespread amongPlantandAnimal Species John J.Wiens Department ofEcology andEvolutionary Biology,University ofArizon a,Tucson, Arizona, UnitedStatesof America wiensj@ email.arizo na.edu Abstract Current climatechange maybeamajor threat toglobal biodiversity, butthe extent ofspe- cies loss willdepend onthe details ofhow species respond tochanging climates.Forexam- ple, ifmost species canundergo rapidchange intheir climatic niches,thenextinctions may be limited. Numerous studieshavenowdocumented shiftsinthe geographic rangesofspe- cies thatwere inferred tobe related toclimate change, especially shiftstowards higher mean elevations andlatitudes. Manyofthese studies contain valuable dataonextinctions of local populations thathave notyetbeen thoroughly explored.Specifically, overallrange shifts caninclude rangecontractions atthe ªwarm edgesº ofspecies' ranges(i.e.,lower lati- tudes andelevations), contractions whichoccurthrough localextinctions. Here,dataoncli- mate-related rangeshiftswereusedtotest thefrequency oflocal extinctions relatedto recent climate change. Theresults showthatclimate-related localextinctions havealready occurred inhundreds ofspecies, including 47%ofthe 976 species surveyed. Thisfrequency of local extinctions wasbroadly similaracross climatic zones,clades, andhabitats butwas significantly higherintropical species thanintemperate species(55%versus 39%),inani- mals thaninplants (50%versus 39%),andinfreshwater habitatsrelativetoterrestrial and marine habitats (74%versus 46%versus 51%).Overall, theseresults suggest thatlocal extinctions relatedtoclimate change arealready widespread, eventhough levelsofclimate change sofar are modest relativetothose predicted inthe next 100years. These extinctions will presumably becomemuchmoreprevalent asglobal warming increases furtherby roughly 2-foldto5-fold overthecoming decades.
Author Summary Climate changeisan important threattothe world's plantandanimal species, including species onwhich humans depend.However, predicting howspecies willrespond tofuture climate changeisvery difficult. Inthis study, Ianalyze theextinctions causedbythe cli- mate change thathasalready occurred. Numerous studiesfindthatspecies areshifting their geographic rangesinresponse toclimate change, typically movingtohigher eleva- tions andlatitudes. Thesestudies alsocontain valuable dataonlocal extinctions, asthey document theloss ofpopulations atthe ªwarm edgeºofspecies' ranges(lowerelevations PLOS Biology |DOI:10.137 1/journal.pb io.2001104December 8,2016 1/18 a11111 2 3 ( 1 $ & & ( 6 6 Citation: WiensJJ(2016) Climate-Relate dLocal Extinctions AreAlready Widespread amongPlant and Animal Species. PLoSBiol14(12) :e2001104.
doi:10.137 1/journal.pbi o.2001104 Academic Editor:Anthony Barnosky, University of California-B erkeley,UnitedStatesofAmerica Received: September 14,2016 Accepted: November 3,2016 Published: December8,2016 Copyright: 2016 JohnJ.Wiens. Thisisan open access articledistributed undertheterms ofthe Creative Commons Attribution License,which permits unrestricte duse, distribu tion,and reproduction inany medium, providedtheoriginal author andsource arecredited.
Data Availabilit yStatement: Allrelevant dataare within thepaper anditsSupport ingInformation files.
Funding: Theauthor(s) receivednospecific funding forthis work.
Competing Interests:The authors havedeclared that nocompeting interestsexist.
Abbreviati ons:GLM, general linearmodel; GLMM, general linearmixed model. and latitudes). Here,Iuse these datatoshow thatrecent localextinctions relatedtoclimate change havealready occurred inhundreds ofspecies around theworld. Specifically, among 976 species surveyed, localextinctions occurredin47%. These extinctions arecommon across climatic zones,habitats, andgroups oforganisms butareespecially commonintrop- ical regions (whichcontain mostofEarth's species), inanimals (relative toplants), andin freshwater habitats.Insummary, thisstudy reveals localextinctions inhundreds ofspecies related tothe limited globalwarming thathasalready occurred. Theseextinctions will almost certainly increaseasglobal climate continues towarm inthe coming decades.
Introduction Anthropogenic climatechangemaybeamajor driver ofbiodiversity lossinthe next 100years, but thepossible impactsofclimate changeonspecies survival remainhighlyuncertain [1±3].
Global meanannual temperatures increasedby~0.85ÊC between 1880and2012 andarelikely to rise byan additional 1ÊCto4ÊC by2100 [4].Modeling studieshavepredicted thatvarious levels ofspecies losswillresult fromthisfuture climate change, ranging from0%to>50% of all species currently known[3].This uncertainty hasmany sources (e.g.,different climate models anddifferent hypotheses aboutspecies dispersal). Oneofthe most important sources of uncertainty hingesonthe details ofhow species respond toclimate change. Forexample, if species canevolve rapidly enough inresponse tochanging climate,thenspecies extinctions due toclimate changemightactually belimited [5,6].
Species canpotentially respondtoclimate changeinseveral ways.Themost important case to consider maybethat when thespecies' present-day (realized)climaticnichenolonger occurs withinthespecies' currentgeographic range(because ofthe potential forglobal extinc- tion ofthe species undertheseconditions). Inthis case, thepossible responses ofthe species include thefollowing: (i)undergoing nicheshifts, suchthatthespecies' realized nichechanges to incorporate thesenewclimatic conditions (e.g.,through plasticchanges and/orbyevolu- tionary adaptation tothe modified abioticand/or bioticconditions), (ii)dispersing totrack the original climatic conditions overspace (e.g.,moving tohigher latitudes orelevations), and (iii) going extinct [5±8].While eachofthese responses hasbeen shown insome cases(atleast in local populations), therelative frequency ofeach isstill unclear [7,8].However, changesin species' geographic rangeshavebeen especially welldocumented [9±11].
These dataongeographic rangeshiftscontain important butunderutilized informationon how species respond toclimate change. Rangeshiftsobserved underclimate changetypically involve anoverall shifttowards higherlatitudes andhigher elevations [9±11].Theseshiftscan be composed ofone (orboth) oftwo types ofchanges (Fig1):(i)range expansions atthe cool edge ofthe species range(higher latitudes andelevations) and(ii)range contractions atthe warm edge(lower latitudes andelevations). Thepresence ofwarm-edge contractions iscriti- cally important. Awarm-edge contraction occurswhenpopulations fromoneormore locali- ties atthe lowest latitudes orelevations ofaspecies' regional distribution disappear(i.e.,are inferred tono longer occuratthose localities), leadingtoan overall shiftinthe species range towards higherlatitudes orelevations. Thesecontractions indicatethatspecies arefailing to shift their niches sufficiently totolerate thesenewconditions andthat these populations are instead goingextinct (referred toasªlocal extinctionº hereafter).Thismust betrue regardless of the specific mechanism oflocal extinction (e.g.,elevated deathrates,increased emigration, or declining recruitment). Themany papers thathave assessed rangeshiftsandthat have included surveysofwarm-edge populations cantherefore provideawealth ofdata about Climate Change andExtinction PLOS Biology |DOI:10.137 1/journal.pb io.2001104December 8,2016 2/ 18 which species have(and havenot)undergone localextinctions potentiallyrelatedtoclimate change. Thesedataareparticularly usefulbecause published papersonrange shiftsneednot be strongly biasedtowards documenting warm-edgecontractions, giventhatmany studies that included dataonwarm edgesalsosurveyed thecool edge. Thus, eventhough studiesthat failed tofind anyrange shiftsmight gounpublished (apotential sourceofbias), studies that documented anoverall rangeshiftneed notshow awarm-edge contraction.
Here, Ianalyze theextensive dataonrange shiftstoexamine theprevalence oflocal extinc- tions related tomodern climatechange. Ialso provide asynthesis ofinferred localextinction across habitats, climaticzones,andtaxonomic groups.Isystematically searchedtheliterature for studies thatexamined shiftsinspecies' rangesattheir warm edges, shiftsthatwere consid- ered (inthe original studies) tobe related tocurrent climatechange. Hundreds ofexamples of local extinctions werefound across diverse climatic zones,habitats, andtaxonomic groups.
Not allspecies exhibiting rangeshiftsshowed warm-edge contractions, but~50% ofthe species surveyed hadlocal extinctions inferredtobe related toclimate change. Theseresults suggest that even therelatively smallchanges inclimate thathave already occurred aresufficient to cause widespread localextinctions andthat many species maybeunable respond toclimate change fastenough toavoid extinction asglobal climate warmsevenfurther.
Results The Web ofScience wassearched repeatedly betweenDecember 2014andMarch 2016using keywords relatedtoclimate change, rangeshifts, andlocal extinctions (seeMaterials and Fig 1.Hypothetic alexample illustrating thetwo componen tsof ageogra phicrange shiftassociated withclimate change. Thelarge open circle indicates thespecies' overallgeographic range.Smalldarkbluecircles indicate populationsbefore climate change. Afterclimate change, theoverall geographic rangeisshifted northward (largeopencircle), boththrough therange expansion (newpopulations; smalllightblue circles) addedatthe northern, ªcoldºedgeofthe species rangeandrange contraction (localextinction oforiginal populations;smallredcircles) atthe southern, ªwarmºedge of the species range.Similar patternsoccur forrange shiftsalong anelevation algradient. ModifiedfromCahill etal. [12].
doi:10.1371/jour nal.pbio.2001104.g001 Climate Change andExtinction PLOS Biology |DOI:10.137 1/journal.pb io.2001104December 8,2016 3/ 18 Methods). Allstudies thatmonitored thewarm edgeofatleast onespecies' rangeandthat tied their results toclimate changewithexplicit statistical analyseswereincluded. Importantly, studies candocument overallrangeshiftsbutneed notfind thatthewarm-edge populations that they examined hadlocal extinctions.
A total of27 studies (Table1;[13±39]) metallthe necessary criteriatoaddress potential cli- mate-associated warm-edgerangeshifts(seeMaterials andMethods). Thesampled species were broadly distributed acrossclades(e.g.,animals =716; plants =260) andregions (e.g., Asia =332; Europe =268; Madagascar =30; Oceania =58; North America =233; South Amer- ica =55). Among the976 unique speciessurveyed, 460species hadwarm-edge contractions, and 516didnot (S1Appendix). Therefore,localextinctions relatedtoclimate changeare already verycommon (47.1%ofspecies examined), evengiven therelatively modestrisein global temperatures thathasoccurred sofar (less than 1ÊCincrease inglobal meanannual temperature; [4]).
These 976species spanned manyclades, habitats, andregions (Table1;S1 Appendix).
Comparison betweenthosespecies thatshowed warm-edge contractions andthose thatdid not provides potential insightsintowhich species maybemost sensitive toclimate change, in terms ofthe climatic zonesandhabitats thatthey occur inand theclades thatthey belong to.
Furthermore, thereisno evidence thatthere weremore species withlocal extinctions instudies that ended morerecently, wereoflonger duration, orbegan earlier (based onmidpoints for ranges ofvalues; Table1).Specifically, regressionanalysesofthe proportion ofspecies with local extinctions against(i)the study enddate, (ii)the duration ofthe study, and(iii)thestudy start dateallyielded nonsignificant results(enddate: 2 = 0.001, = 0.8910; duration: 2 = 0.045, = 0.2896; startdate 2 = 0.047, = 0.2788; afterremoving ninestudies withfouror fewer species: enddate: 2 = 0.146, = 0.1181; duration: 2 = 0.132, = 0.1376, butunexpect- edly trending towardsfewerextinctions instudies withlonger durations; startdate 2 = 0.177, = 0.0821, withmore extinctions instudies beginning morerecently, notearlier). Therefore, the frequency oflocal extinctions wasinitially compared acrossspecies indifferent studies, regardless ofdifferences inthe duration, beginning, orend date ofthe study inwhich they were surveyed.
Overall, thefrequency oflocal extinctions wassimilar (closeto50%) across mostclimatic zones, habitats, gradients, andclades. Nevertheless, thereweresome significant differences.
First, localextinctions weresignificantly morecommon inspecies fromtropical andsubtropi- cal regions (combined andreferred toastropical hereafter forbrevity) thaninthose fromtem- perate regions ( <0.0001; Chi-squared test,testing theassumption ofequal frequencies of local extinction amongspecies between regions;subsequent -valuesarealso from Chi- squared tests).Specifically, 54.6%ofthe 504 included tropicalspecieshadlocal extinctions, whereas only39.2% ofthe 472 temperate speciesdid(Fig 2A). Thepattern waseven stronger when onlyconsidering terrestrialspeciesonelevational gradients(54.6%of504 tropical spe- cies versus 28.2%of301 temperate species),whichapplied toall plants andmost animals. In part, thispattern ofmore frequent tropicalextinction arosefromamuch lowerfrequency of extinctions fortemperate plants(59.4% of155 tropical speciesversus8.6%of105 temperate species; < 0.0001). Thevery lowfrequency oftemperate extinctions inplants wasbased ona single studyfromveryhigh latitudes [19].Nevertheless, therewerealsosignificantly more local extinctions intropical animals (52.4%of349 tropical speciesversus38.8%of196 temper- ate species; = 0.0022), ifone compares terrestrial speciesonelevational gradients.This restriction alsomade themmore comparable tothe sampled plants(allfrom terrestrial, eleva- tional gradients) andstillencompassed mostsampled animalspecies (76.1%; 545of716 spe- cies). Across allanimals, thedifference wasnotsignificant ( =0.2309), possibly becauseofthe influence oftemperate marineandfreshwater species(seebelow). Among themost well- Climate Change andExtinction PLOS Biology |DOI:10.137 1/journal.pb io.2001104December 8,2016 4/ 18 Table 1.Summary information onthe 27range-shift studiesusedtodocument localextinction srelated toclimate change. Studiesarelisted alpha- betically byfirst author. Themajor taxonom icgroup surveyed isgiven (Taxon, allgroups areanimals exceptforªPlantº), alongwiththetotal number ofspecies surveyed (TotalSpecies) ,the percenta geofthose species withoneormore localextinctions (%Local Extinction), thegeneral habitattype(Habitat; including terrestrial, freshwater, andmarine) ,the climatic region(tropical-sub tropicalversustemperate ),the geographic regionwherethestudy wasconducted (note that North America hereextends toCentral America) ,the type ofrange shift(latitudinal, elevational),the dates ofthe initial survey andtheresurvey, andthe duration inbetween (forsurveys and/orresurveys spanningmultiple years,themidpoin tof each wasused tocalculate theduration).
Referenc eTaxon Total Species % Local Extinction Habitat Climatic Region Geographi c Region Range Shift Initial Survey Resurvey Date Duration Angelo and Daehler [13] Plant 450Terrestrial Tropical Oceania (Hawaii) Elevation al1966± 1967 2008 41.5 Beever etal.
[14] Mammal 1100Terrestrial Temperate NorthAmerica Elevational1898± 1956 2003±200 677.5 Brusca etal.
[15] Plant 2756Terrestrial TropicalNorthAmerica Elevational1963 2011 48 Chen etal. [16] Insect 20856Terrestrial Tropical AsiaElevational1965 2007 42 Comte and Grenouille t[17] Fish 3174Fresh. Temperate EuropeElevational1980± 1992 2003±200 920 Dieker etal.
[18] Insect 250Terrestrial Temperate EuropeElevational1958± 1986 2008±200 936.5 Felde etal. [19] Plant 1059Terrestrial Temperate EuropeElevational1900 2008 108 Forero-M edina et al. [20] Bird 5529Terrestrial TropicalSouthAmerica Elevational1969 2010 41 Franco etal.
[21] Insect 3100Terrestrial Temperate EuropeLatitudinal 1970± 1999 2004±200 520 Freeman and Freeman [22]Bird 5474Terrestrial TropicalOceania(New Guinea) Elevation al1965 2012 47 Hiddick etal.
[23] Marine invertebrate s 65 55Marine Temperate EuropeLatitudinal 19862000 14 Hitch and Leberg [24] Bird 1100Terrestrial Temperate NorthAmerica Latitudinal 1967± 1971 1998±200 231 Menende z et al. [25] Insect 3954Terrestrial Temperate EuropeElevational1981± 1993 2006±200 724 Moritz etal.
[26] Mammal 2741Terrestrial Temperate NorthAmerica Elevational1914± 1920 2003±200 687.5 Myers etal.
[27] Mammal 812Terrestrial Temperate NorthAmerica Latitudinal 1883± 1980 1981±200 662 Nye etal. [28] Fish 2850Marine Temperate NorthAmerica Latitudinal 19682008 40 Perry etal. [29] Fish 1040Marine Temperate NorthAmerica Latitudinal 19972001 24 Ploquin etal.
[30] Insect 1669Terrestrial Temperate EuropeElevational1988± 1989 2007±200 919.5 Pomara etal.
[31] Squamate 1100Terrestrial Temperate NorthAmerica Elevational1965 2008 43 Raxworthy et al. [32] Amphibian- Squamate 30 37Terrestrial TropicalMadagascarElevation al1993 2003 10 Rowe etal. [33] Mammal 425Terrestrial Temperate NorthAmerica Elevational1927± 1929 2006±200 879 Rubal etal. [34] Mollusca 729Marine Temperate EuropeLatitudinal 1917, 1940 2011 94 Sheldon [35] Insect 10Terrestrial Temperate NorthAmerica Elevational1977± 1978 2006 28.5 Telwala etal.
[36] Plant 12460Terrestrial Tropical AsiaElevational1849± 1850 2007±201 0159 Tingley etal.
[37] Bird 9225Terrestrial Temperate NorthAmerica Elevational1900± 1930 1980±200 678 Warren and Chick [38] Insect 20Terrestrial TropicalNorthAmerica Elevational1973± 1974 2012 38.5 (Continue d) Climate Change andExtinction PLOS Biology |DOI:10.137 1/journal.pb io.2001104December 8,2016 5/ 18 sampled groupsofanimals, tropicalextinction wassignificantly morecommon inbirds (51.4% of109 tropical speciesversus37.1%of124 temperate species; = 0.0284), butnot in insects (localextinctions in55.2% of210 tropical speciesversus59.0%of61 temperate species; = 0.6007). Forother animal groups, thespecies sampled herewere either predominantly tem- perate (mammals, fish,andmarine invertebrates) ortropical (squamate reptilesandamphibi- ans), andsodid not allow forsimilar within-clade comparisons.
Overall, thefrequency ofclimate-related localextinctions (Fig2B)was similar interrestrial (45.6% of835 species) andmarine environments (50.9%of110; = 0.2964). Incontrast, the frequency infreshwater specieswassubstantially higher(74.2% of31; = 0.0053 acrossall three habitats). However, theestimate forfreshwater specieswasbased onasingle studyof European fishes[17].Comparing fishonly (alltemperate) alsosupported asignificantly higher frequency ofextinction infreshwater environments relativetomarine environments ( =0.0240; localextinctions in47.4% of38 marine speciesversus74.2%of31 freshwater spe- cies). Allmarine speciesincluded herewere temperate animals,butthere wasnosignificant difference inextinction frequencies betweenmarineandterrestrial environments whenonly temperate animalswerecompared ( =0.1676; marine: 50.9%of110 species, terrestrial: 42.9% of 226 species). Terrestrial andfreshwater speciesremained significantly differentinthis more restricted comparison ( =0.0011).
The frequency oflocal extinctions (Fig2C)wassomewhat lowerforspecies surveyed along elevational gradientsrelativetothose onlatitudinal gradients(elevational: 45.8%of836 spe- cies; latitudinal: 55.0%of140 species; = 0.0439). Most(78.6%) speciesmeasured alonglatitu- dinal gradients weremarine (andallmarine studiesfocused onlatitudinal gradients), andall were temperate. Again,mostspecies included herewere based onstudies ofelevational gradi- ents interrestrial environments.
Local extinctions werealsobroadly similarinfrequency acrosstaxonomic groups(Fig3).
Nevertheless, localextinctions weresignificantly morecommon ( =0.0018) inanimals (50.1% of716) than plants (38.8% of260). Thisdifference wasreduced whencomparing only animals andplants onterrestrial, elevational gradients(47.3%of556 animal species versus 38.8% of260 plant species; = 0.0236). Amongtheselatter species, theplant±animal difference was nonsignificant fortropical species(andwasactually reversed: localextinctions in52.4% of 349 tropical animalspecies versus59.4%of155 tropical plants; = 0.1500) butwas strong for temperate species(38.6%of207 temperate animalspecies versus8.6%of105 temperate plants; < 0.0001).
The frequencies oflocal extinctions acrossdifferent animalgroups (Fig3)were broadly similar tothe overall valueforanimals (50.1%), butwith higher valuesininsects (56.1% of271 species; basedonsix studies; Table1)and fish(59.4% of69 species; threestudies) relativeto mammals (35.0%of40 species; fourstudies), birds(43.8% of233 species; fivestudies), amphib- ians (36.8% of19 species; onestudy), andsquamate reptiles(lizards andsnakes; 41.7%of12 species; twostudies). Localextinctions werealsobroadly similarinfrequency invarious groups ofmarine invertebrates, includingcrustaceans (46.7%of15; one study), annelids (64.5% of31; one study), andmolluscs (45.4%of22; two studies). Thefrequency inechino- derms waslower (25.0%; onestudy) butwas based onavery small sample size(4species).
Table 1.(Continue d) Referenc eTaxon Total Species % Local Extinction Habitat Climatic Region Geographi c Region Range Shift Initial Survey Resurvey Date Duration Zuckerberg et al. [39] Bird 3171Terrestrial Temperate NorthAmerica Both1980± 1985 2000±200 520 doi:10.137 1/journal.pbi o.2001104.t001 Climate Change andExtinction PLOS Biology |DOI:10.137 1/journal.pb io.2001104December 8,2016 6/ 18 Results weregenerally similarusingbothgeneral linearmodels (GLMs; seebelow) andgen- eral linear mixed models (GLMMs; seenext paragraph). GLMresults aregiven infull inS2 Appendix andaresummarized here.Simultaneously includingall976 species andmost vari- ables (habitat [terrestrial versusfreshwater versusmarine], climaticregions[tropical versus temperate], taxonomicgroup[plants versusanimals], surveytype[latitudinal versuseleva- tional], andstudy dates[start date,enddate, andduration inbetween]) showedthatmost Fig 2.The frequency oflocal extinct ionsrelated toclimate change acrossdifferent climaticregions, habitat s,and gradien ts.(A) Species arecategorize das temperate ortropical (basedonthe location ofthe study), andthepercenta geofspecies withoneormore localextinctions isshown, alongwiththesample sizes of species ineach region. (B)Species arecategorize das terrestrial, freshwater,ormarine, andthefrequenc y of species withlocal extinct ionsisshown (alongwithtotal species perhabitat). (C)Species arecategori zed based onwhether theywere surveyed alongelevational orlatitudinal transects.Vertical linesindicate 95% confidence intervalson the estimated frequencyofspecies withlocal extinctions.
doi:10.13 71/journal.pbi o.2001104.g00 2 Climate Change andExtinction PLOS Biology |DOI:10.137 1/journal.pb io.2001104December 8,2016 7/ 18 variables hadsignificant effectsonthe frequency ofextinction, exceptforthe study dates.
There werestrong effectsofhabitat andclimate ( <0.00001) butweaker effectsoftaxonomic group ( =0.0246). Resultsweresimilar whenexcluding studydatesandtaxonomic group.
Including geographic regionsshowed thatmost regions hadnosignificant effect(except for Madagascar andSouth America). GiventhatMadagascar andSouth America wererepresented by one study each,theseregion effectswerenotconsidered further.Furthermore, theeffects of climatic region,habitat, taxonomic group,andsurvey typeremained significant whengeo- graphic regionswereincluded. Comparing speciesonlyonterrestrial elevational gradients (805 species intotal) further confirmed thesignificant effectsofclimate andtaxonomic group.
Similarly, considering plantsonly(260 species) alsoconfirmed thesignificant effectsofcli- matic region. Considering onlyterrestrial animalsonelevational gradients(545species) showed asignificant effectofclimate ( =0.0023) afterremoving studydates, which hadno significant effect.Considering birdsalone (233species) andincluding climaticregion,survey type, andstudy datesshowed thatclimatic region,surveytype,startdate, andenddate hadsig- nificant effects.Forinsects (271species), whenincluding climaticregion,studydates, andsur- vey type, novariables weresignificant. Forfish (69species), amodel including habitat (freshwater versusmarine), studydates, andsurvey typeshowed thatnovariables weresignifi- cant. However, habitatwassignificant ifother variables wereremoved. Similarly, fortemperate animals (367species), amodel including habitat,surveytype,andstudy datesshowed that only habitat andsurvey typewere significant. Comparison ofplants andanimals onterrestrial elevational gradients(including studydates) showed thatextinction issignificantly different between temperate plantsandanimals (morecommon inanimals), butnot between tropical ones. Across animals, theeffects oftaxonomic groupwerelimited anddepended onthe other variables included. Ifonly taxonomic groupsandstudy dateswereincluded, thenannelids, fish, andinsects showed significantly moreextinction ( =0.03±0.05). Includinghabitatand survey type(and removing studydates) showed stronger effectsinfish and annelids (aswell as in crustaceans andmolluscs), butnot ininsects.
Fig 3.The frequency oflocal extinct ionsrelated toclimate change acrossdifferent taxonomicgroups. Thepercentage ofspecies with one ormore localextinctions ineach taxonom icgroup isshown, alongwiththetotal sample sizeofspecies surveyed inthat group. Forease of presenta tion,fourdifferent groupsofmarine inverteb rates(annelids, crustaceans,molluscs ,and echinoderm s)are shown together. Frequenc ies for these fourgroups wereaverage dto obtain asingle value, andsample sizesofspecies acrossgroups weresumme d.Squamat ereptiles include lizardsandsnakes. Verticallines indicate 95%confidence intervalsonthe estimated frequency ofspecies withlocal extinctions.
doi:10.137 1/journal.pbi o.2001104.g003 Climate Change andExtinction PLOS Biology |DOI:10.137 1/journal.pb io.2001104December 8,2016 8/ 18 Results werealsobroadly similarusingGLMMs, withstudy identity included asarandom effect. Results aresummarized belowandgiven infull inS3 Appendix. Theimpacts ofstudy dates weresomewhat counterintuitive (andrarely significant), andanalyses including them sometimes failed.When mostvariables wereincluded (habitat,climaticregion,taxonomic group [plantversus animal], surveytype,andstudy dates), allvariables weresignificant except for study datesandtaxonomic group,withstrong effectsofhabitat, climatic region,andsurvey type. When studydateswereremoved, onlyhabitat andsurvey typewere significant. When geographic regionswereincluded (andstudy datesexcluded), onlySouth America hadasig- nificant effect,andhabitat, taxonomic group,andclimatic regionweresignificant ormargin- ally significant. Comparing tropicalandtemperate speciesonterrestrial, elevational gradients showed significant effectsofclimatic region( =0.0017) andtaxonomic group( =0.0119), but not ofstudy dates. When studydateswereremoved, novariables weresignificant. Plants alone showed asignificant effectofclimatic region( <0.0001), butanalyses failedifstudy dates wereincluded. Animalsonterrestrial, elevational gradientsshowednosignificant effect of climatic region(again, studydateshadtobe excluded). Considering birdsalone showed no significant effectofclimate butasignificant effectofsurvey type(excluding studydates).
Insects showed nosignificant effectsofclimate orsurvey type,regardless ofwhether study dates wereincluded. Analysesoffish failed unless studydatesandsurvey typewere excluded, but habitat alone(marine versusfreshwater) hadasignificant effect( =0.0265). Analyses of temperate animals(367species) including habitat,surveytype,andstudy datesshowed only habitat typeassignificant ( =0.0307), butexcluding studydatesshowed significant effectsof habitat andsurvey type.Comparing onlytemperate plantsandanimals showedasignificant effect oftaxonomic group,whenstudydateswereincluded ( =0.0116) orexcluded ( =0.0005; studydateshadnosignificant effect).Incontrast, therewasnosignificant effectof taxonomic groupwhencomparing tropicalplantsandanimals (504species total;excluding study dates). Analyses ofanimals aloneshowed nosignificant effectoftaxonomic group.
In summary, severalpatterns emerged assignificant acrossall(or most) analyses. First, there weresignificant effectsofclimatic regionoverall, withextinction morecommon intropi- cal regions. Thiswaspresent inplants across allanalyses andgenerally presentinanimals. Ani- mals showed significantly moreextinction thanplants overall andwhen comparing temperate, but not tropical, species.Thereweresignificant effectsofhabitat onanimals overall(higher extinction infreshwater), evenwhen considering fishalone. Finally, GLManalyses showed some effects oftaxonomic groupsacrossanimals (withhigher extinction infish and annelids) and possibly ininsects, molluscs, andcrustaceans. TheGLMM analyses didnot show these group effects, possibly becausemanyanimal groupsareincluded basedonasingle study.
Discussion The results ofthis study showthatlocal extinctions (inferredtobe related toclimate change) are already widespread andhave occurred inhundreds ofspecies. Roughly halfofthe 976 species that were surveyed forrange shiftsshowed evidence oflocal extinctions (47%).Thisproportion was surprisingly similaracrossdiverse climatic regions,habitats, andtaxonomic groups.The results heresuggest thateven themodest changes inclimate thathave occurred sofar are enough to drive localpopulations inmany species toextinction. Theresults herealsosuggest thatlocal populations inmany species cannotshifttheir climatic nichesrapidly enough toprevent extinc- tion. Thispattern ofwidespread localextinction seemslikelytobecome evenmore prevalent as the global climate warmsfurther (byroughly 2to 5-fold [4])inthe next several decades.
The results hereshowed generally similarpatterns oflocal extinction acrossclimatic zones, habitats, andclades. Nevertheless, mostanalyses showedthatlocal extinctions were Climate Change andExtinction PLOS Biology |DOI:10.137 1/journal.pb io.2001104December 8,2016 9/ 18 significantly morecommon intropical species(Fig2A), infreshwater species(Fig2B), andin animals. Agreater impactofclimate changeontropical specieshasbeen predicted byseveral authors (e.g.,[40±42]). Thisprediction isrelated tothe narrower climaticnichewidths for temperature-related variablesintropical speciesthatareassociated withreduced temperature seasonality inthe tropics (e.g.,[43,44]) andlower ratesoftemperature-related climaticniche change intropical species(e.g.,[42]). Theresults hereprovide support forthis prediction based ondocumented localextinctions thathave already occurred: speciesintropical regions had local extinctions morefrequently thanthose intemperate regions(54.6%versus39.2%), especially whenspecies werecompared onterrestrial, elevational gradients(54.6%versus 28.2%). Thispattern wasstrongest inplants andwhen animals werecompared onterrestrial elevational gradients.Overall,theseresults further support theidea thatthenegative impacts of climate changeonbiodiversity aremore frequent (perspecies) intropical regions[40±42], where biodiversity ishighest.
Climate-related localextinctions werealsosimilar infrequency inmarine andterrestrial spe- cies (Fig 2B)butwere more common infreshwater species(although freshwater habitatswere represented byasingle study). Freshwater speciesmaybeespecially susceptible tochanges in precipitation patterns(e.g.,drought), whichcansubstantially alteroreliminate theirhabitats (e.g., [45]), quickly resulting inlocal extinction. Incontrast, marinespeciesmayexperience less impact fromchanges inprecipitation. Furthermore, theymay bebuffered fromtemperature changes becausetheycanpotentially adjustthetemperatures thatthey experience bymovement within thewater column (moresothan ispossible formost freshwater species;[46,47]).
The frequency oflocal extinctions wasalso broadly similaracrossdiverse taxonomic groups (~35%±60%; Fig3),including plants,insects, fish,amphibians, squamatereptiles,endothermic vertebrates (birdsandmammals), andmany marine invertebrates (annelids,crustaceans, and molluscs). However,localextinctions weresignificantly morecommon inanimals thanplants (and animals arefarmore species-rich thanplants). Theywerealsorelatively common in insects (themost species-rich groupofanimals) andfish(the most species-rich groupofverte- brates). Localextinctions werenotparticularly commoninamphibians (36.7%)orsquamate reptiles (41.7%), although bothgroups wereincluded herebased primarily onone study [32].
Nevertheless, bothgroups appeartohave been strongly impacted byclimate changeoverall.
For example, manyamphibian specieshaveundergone sharpdeclines andglobal extinctions, many ofwhich arethought tobe caused byan interaction betweenclimatechangeandan infectious disease(chytrid fungus;[48]).However, thesechytrid studieswerenotincluded here because theywere notfocused onsurveying warm-edge populations overtime. Similarly, local extinctions relatedtoclimate changehavebeen documented inmany lizardspecies [49].
Again, thesewerenotincluded herebecause theywere notbased onasystematic surveyof warm-edge populations. Nevertheless, ifthe species studied bySinervo etal. [49] were included here,thefrequency oflocal extinctions insquamates wouldgofrom 41.7% (of12spe- cies) to77.4% (of124 species), butwith thecaveat thattheir study focused ondocumenting local extinctions andsomight overestimate thisfrequency. Itshould alsobenoted thatthe well-publicized declinesinamphibian populations globallyarenot necessarily inconsistent with thefrequency oflocal extinction observedhere.Forexample, aglobal assessment of amphibian populations [50]noted declines in43% ofamphibian species(compare tothe 47% of all species herewith local extinctions andthe37% foramphibians), butthese declines also included thoseunrelated toclimate change(e.g.,habitat destruction andoverexploitation).
Thus, thefrequency ofclimate-related declineshereisnot necessarily anunderestimation rela- tive tothe declines documented bythe global amphibian assessment [50].
A major conclusion ofthis study isthat populations ofmany species arealready unableto undergo nicheshiftsthatarefast enough toprevent localextinction fromclimate change. The Climate Change andExtinction PLOS Biology |DOI:10.137 1/journal.pb io.2001104December 8,2016 10/ 18 rate isemphasized herebecause evenifthe absolute amountofniche change needed toavoid extinction mightbeattainable, itmight require moretimetoachieve thanisallowed bythe rapid paceofanthropogenic climatechange. Giventhisresult, andthat climate ispredicted to change evenfurther inthe near future, thepersistence ofmany species mightdepend largely on their ability tosuccessfully shifttheir geographic rangestohigher latitudes orelevations and remain withintheiroriginal climatic niche.Indeed, thesummary hereshows numerous instances ofcool-edge expansions (in367 of904 species, withcooledges thatwere stable in 371 others andcontracted in166 others).
Unfortunately, thesemovements maybeimpeded formany species byone ormore factors.
First, human impacts mayprevent speciesfromsuccessfully dispersing(including agriculture, roads, andurbanization), orthese human impacts maysimply leavethem nohabitat todis- perse to(e.g., [51,52]). Second,manyspecies arealready confined toislands, peninsulas, and mountaintops, wheredispersal tohigher latitudes orelevations maynotbepossible (e.g.,[53]).
Third, evenifdispersal isunimpeded byhuman ornatural barriers, itmay simply occurtoo slowly toallow species toremain withintheirclimatic niche(e.g.,[54,55]).
The combination ofthese potential limitstodispersal andthewidespread localextinctions documented hereistroubling. However,theresults heredonot rule outthepossibility that rapid niche shiftswilloccur insome populations ofmany species inthe future, preventing global extinctions. Indeed,roughly halfofthe species surveyed showednolocal extinctions, and most species hadsome populations thatpersisted locally(butagain, thisisunder thelim- ited climate changethathasalready occurred). Thefuture persistence ofspecies willdepend on many factors [6,8],including ratesandpatterns ofclimate changeateach location, dis- persal, nicheshifts, localclimatic microrefugia [56],andthecontribution ofpopulation-level niche width tospecies-level nichewidth (e.g.,whether speciesarebroadly tolerant orlocally specialized todifferent climaticconditions acrosstheirranges [44]).Mostimportantly, Isug- gest that thepatterns ofpresent-day localextinctions obtainedfromrange-shift studiesshould be part ofthe evidence usedtopredict speciespersistence inthe future.
There areseveral potential sourcesofbias thatmay have influenced someaspects ofthese results butshould notoverturn themajor conclusions. First,ªlocal extinctionº meansthat individuals ofagiven species areentirely absentfromalocation thatthey previously occupied.
However, itcan bedifficult todistinguish betweenextinction andasubstantial declinein abundance thatcauses thespecies togo undetected atagiven location (e.g.,[57]), andstudies did not necessarily providestatistical evidenceforthe absence ofaspecies atasite. Here, the estimates ofprevious researchers wereused, anditwas assumed thatthey adequately docu- mented localabsences (otherwise, theirestimates ofrange shiftswould alsobeerroneous).
Furthermore, strongdeclines thatmake aspecies undetectable atagiven sitemight soonlead to local extinction. Second,theremaybeabias interms ofunpublished results.Specifically, some researchers whomonitored thewarm edgeofapopulation butfailed tofind anychanges associated withclimate changemaynothave published theirnegative results.Suchareporting bias would leadtooverestimating theproportion ofspecies experiencing localextinction in this study. Nevertheless, localextinctions werestilldocumented inhundreds ofspecies across regions andclades, evenifthere arehundreds ofadditional speciesinwhich theselocalextinc- tions didnot occur. Additionally, numerousspecies( =171) showed evidence ofacool-edge expansion withoutacorresponding contractioninthe warm edge.Thus, aspecies canundergo a range shiftbutwithout localextinction, whichshould limitthissource ofpublication bias.
Third, itwas assumed thatprevious researchers correctlyassociated thepatterns thatthey observed withclimate change. Intheory, otherfactors suchasoverharvesting orhabitat destruction mayhave contributed tothe observed localextinctions insome cases(e.g.,[21]).
Climate Change andExtinction PLOS Biology |DOI:10.137 1/journal.pb io.2001104December 8,2016 11/ 18 Again, theanalyses hereprimarily assumethatthemain conclusions ofthese previous studies were noterroneous.
Finally, despitethewidespread patternofwarm-edge contractions andlocal extinctions, 521 species showed nolocal extinctions atthe warm edge,indicating thatthey have success- fully persisted inthe face ofthe climate changethathasoccurred sofar. However, eventhese species mightstillgoglobally extinctwhenglobal climate changes further.Additionally, con- trary tothe overall trend,54species weredocumented hereashaving expansions atboth their warm edgeandtheir cooledge (6.0% of904 species withdataonboth coolandwarm edges).
One scenario bywhich thismay occur isifcool-edge limitsaresetbycolder temperatures (allowing expansion asglobal climate warms) andwarm-edge limitsaresetbylow precipita- tion (allowing warm-edge expansion), giventhatprecipitation mayincrease insome areas because ofclimate change[4].Indeed, somestudies havefound evidence forwarm-edge expansions throughthismechanism [58].Itisalso important tonote thatlocal extinctions related toclimate changeneednotbeconfined tothe warm edgeofthe species rangeandso might actually beunderestimated here.Forexample, therecould beclimate-related local extinctions farfrom thewarm edgethatareassociated withcertain microclimates (e.g.,equato- rially facing slopesatthe cool edge ofaspecies range;[59]).
In summary, theresults hereshow thatwidespread localextinctions (seeminglyrelatedto climate change) havealready occurred inhundreds ofspecies, withbroadly similarpatterns of extinction acrossdiverse clades,habitats, andclimatic regions.Importantly, levelsofclimate change sofar are limited relative tothose generally predicted forthe next 100years [4].The results here suggest thatmany species areunable toshift their niches rapidly enough toprevent local extinction. Thisinference ofclimate changeoutpacing nichechange supports predictions from other sources, including transplant experiments inplants [60],phylogenetic analysesofrates of niche change inplants andanimals [42,61,62], andprojections basedonselection, heritability, and temperature tolerancesinlizards [49].Local extinctions fromclimate changemightalso impact speciesthatmany human populations dependonfor food, suchasgrasses (e.g.,wheat, rice, andcorn [62]). More generally, thisstudy demonstrates thatanalyses ofrange shiftscanpro- vide extensive dataonlocal extinctions relatedtoclimate changethathave already occurred.
These localextinctions offerapotentially importantbutunderutilized sourceofinformation for the challenging taskofpredicting patternsofspecies survival andextinction inthe future.
Materials andMethods Selection ofStudies Web ofScience searches wereinitially conducted fromDecember 2014toApril 2015using the Boolean searchtermsTopic =(global warming ORclimate change) ANDTopic =(local extinction ORrange contraction ORrange shift). Asecond WebofScience searchwascon- ducted between April2015andMay 2015 toidentify additional studiespotentially missedby the first setofkeywords, usingthesearch termsTS=(global warm OR climate change) AND TS =(extinction OR contraction OR range shift ), excluding resultsfromTS=(global warming ORclimate change) ANDTS=(local extinction ORrange contraction ORrange shift). EachsetofWeb ofScience resultswassorted byrelevance andthen binned intosubsets of 50. Searching wasceased whenlessthan 1in 50 studies persubset wasrelevant (seebelow for criteria). Finally,athird WebofScience searchwasperformed on1March 2016tofind more recently published studies.Thisthird search usedthekeywords TS=(global warm OR climate change) ANDTS=(extinction OR contraction OR range shift ). A total of1,530 results werefound inthis third search. Results weresorted byrelevance, andthefirst 300 (~20%) wereexamined. Thelast40ofthese 300included norelevant studies.
Climate Change andExtinction PLOS Biology |DOI:10.137 1/journal.pb io.2001104December 8,2016 12/ 18 Some additional studieswerealsofound thatwere listed asreferences inthe papers identi- fied bythese initial WebofScience searches. Thereference listwas also checked againsta recent review study[11],which alsoconducted thoroughsearchesofthe literature onclimate- related rangeshifts. Three studies wereadded fromthatsurvey whichwerenotinitially included here.Finally, severalrelevant studieswerealsofound inthe survey ofGibson-Rene- mer etal. [63], which hadsimilar rulesforinclusion ofstudies. Although thoseauthors didnot conduct asystematic searchofthe literature (asdone here), theynevertheless includedfive studies notfound inthe searches described above.Thesewerealsoadded here.
In theory, thefact that ªextinctionº andªcontractionº wereincluded askeywords might have biased theresults toinclude morepapers documenting localextinctions andrange con- tractions thanwould beobtained fromasearch ofrange-shift studiesthatexcluded theseaskey- words (possibly leadingtooverestimation ofthe frequency oflocal extinctions). However,this seems unlikely inpractice. First,thesewereincluded asªorº keywords, alongwithªrange shifts.º Examining thekeywords andtitles ofthe 27selected papersshowed thatmost werefocused on overall rangeshifts, withnomention oflocal extinction (extinction orextirpation aremen- tioned inthe titles ofonly 4of 27 studies andaskeywords inonly 4of the 21studies withkey- words; ªcontractionº ismentioned inonly 1).Furthermore, thefact that thesurvey resultshere were checked againstanother recentreview onrange shifts[11],andthat three missing studies were added, alsomakes thispotential biasseem unlikely. Inother words, ifmany range-shift studies weremissed because ofthis bias, theyshould havebeen added atthat point.
Overall, thesesearches wereextensive butmay notbetruly exhaustive. Regardless, many studies werefound thatdocumented localextinctions, andfinding morestudies thatdidso would notoverturn thismain conclusion.
Studies wereincluded thatmonitored oneormore populations atthe warm edgeofaspe- cies' range (theedge thatislower inelevation orcloser tothe equator) overarelatively long time span. Studies wereonlyincluded thatspanned aninterval ofatleast 10years. Themean study duration was~50 years (range =14 to159; Table 1).Studies wereincluded thatrelated their findings onrange shiftstoclimate changethrough anexplicit statistical analysis(butnot- ing that these inferences couldstillbeincorrect, forexample, ifother factors instead ofclimate change causedlocalextinctions ofaparticular species).Theincluded studiesalldocumented populations alongelevational orlatitudinal transectsattwo ormore discrete timepoints.
Some recent studies haveinferred climate-related rangeshiftsbased onoverall trendsinlat- itudinal andelevational distributions acrossalarge number oflocalities overtime, rather than systematically resurveyingspecificlocalities atdifferent timepoints (e.g.,[64]). These studies are valuable fordocumenting rangeshiftsingeneral butwere excluded here,since theydonot unambiguously representlocalextinctions (becausetheoverall patterns described mightbe driven solelybyrange expansions instead).
Categorizing Species Studies thatdocumented warm-edgerangecontractions (andthatwere linked toclimate change bythe authors ofthe original studies)wereconsidered evidenceofclimate-associated local extinction, regardlessofchanges atthe cool edge. Studies differed inwhether they reported changesatthe population level(e.g., [28,37]) orspecies level(e.g., [33]). Theanalysis here wasconducted atthe species level.Therefore, ifpopulations ofthe same species differed in the pattern oftheir range shifts, thespecies wascategorized asshowing evidence oflocal extinction ifat least onepopulation didso.
Most species wereincluded inonly onestudy. However, theplant species wasincluded byboth Angelo andDaehler [13](inHawaii) andFelde etal. [19] (in Climate Change andExtinction PLOS Biology |DOI:10.137 1/journal.pb io.2001104December 8,2016 13/ 18 Europe). However, sincethisspecies isnot native toHawaii, itwas excluded fromthedataset of Angelo andDaehler [13],along withallother nonnative speciesinthat study.
For each study, itwas noted whether therange shiftswereelevational orlatitudinal, aswell as the general habitatofthe organisms (i.e.,terrestrial, freshwater, ormarine), thehigher taxa to which theybelonged, thespecific geographic locationofthe study, andwhether thespecies occurred inatropical orsubtropical region(arbitrarily definedaswithin 35Êofthe equator) or in atemperate region(>35Ê). Specieswereassigned tothese climatic regionsbasedsolelyon the location wheretheywere surveyed, ratherthanontheir overall geographic range.Species were alsoassigned totaxonomic categories,includingplants,insects, fish,amphibians, birds, mammals, andsquamate reptiles(i.e.,lizards andsnakes), aswell asmarine annelids, crusta- ceans, echinoderms, andmolluscs. Thebeginning andenddates ofthe study werealsonoted (e.g., thedate ofthe initial survey andthesubsequent resurvey)andwere usedtoestimate the duration ofthe study. Somestudies provided arange ofdates forthe start and/or enddate. In these cases, themidpoint ofeach range ofdates wasused toestimate thestart, end,anddura- tion (Table 1).Data forallspecies areprovided inS1 Appendix.
The studies included (Table1)spanned manygeographic regions(e.g.,North America, South America, Europe,Asia,andOceania). Manystudies wereconducted inNorth America ( =13; here extending toCentral America) andEurope ( =8), but theactual number ofspe- cies sampled wasmore broadly distributed amongregions (e.g.,Asia=332; Europe =268; Madagascar =30; Oceania =58; North America =233; andSouth America =55). Africa and Australia werenotrepresented, althoughnearbyMadagascar andNew Guinea were.Thenum- bers oftemperate andtropical speciesincluded werenearly equal.Further, therewasnoclear hypothesis forwhy particular continents aloneshould bean important factorinfluencing the frequency oflocal extinctions (e.g.,separate fromtemperate versustropical effects).
Statistical Analyses Chi-squared analyseswereinitially usedtocompare theproportion ofclimate-associated local extinctions acrosssomecategories (i.e.,tropical versustemperate; freshwaterversusmarine versus terrestrial; andlatitudinal versuselevational gradients),testingthenull hypothesis that frequencies oflocal extinction wereequal between thesecategories. Aseries ofanalyses were conducted toassess whether frequencies oflocal extinction werehigher intropical regionsrel- ative totemperate regions,afteraccounting forthe potential influence ofdifferent habitats, gradients, andclades (seeResults). Similaranalyses wereconducted toassess theimpacts of different habitatsandclades (i.e.,plants versus animals). However, potentialanalyseswere restricted bythe available data.Forexample, itwas notpossible tocompare theeffect oftropi- cal versus temperate climatesonmarine orfreshwater organisms, sinceonlytemperate marine and freshwater specieswereincluded here.Forthis reason, different setsofanalyses werecon- ducted foreach question.
These analyses werethenrepeated usingGLMs andGLMMs, bothinR. These analyses were implemented treatingthepresence ofwarm-edge localextinction inaspecies asthe bino- mial, dependent variable.GLMManalyses wereconducted usingtheRpackage [65].
GLMM analyses treatedthestudy (from which thespecies datawere obtained) asthe random variable andtheother variables asthe fixed variables. GLMandGLMM analyses initially included allspecies andallormost variables andwere thenrestricted tosmaller setsofspecies (and variables) totest additional hypotheses andreduce potentially confounding effects(asin the Chi-squared analyses).
Phylogenetic informationwasnotincorporated here,since phylogenies andcomparable branch lengths spanning allthe included specieswerenotavailable (especially species-level Climate Change andExtinction PLOS Biology |DOI:10.137 1/journal.pb io.2001104December 8,2016 14/ 18 phylogenies forfish, insects, plants,andmarine invertebrates). Nevertheless,someanalyses were conducted toassess patterns withinandbetween clades(seeResults).
Supporting Information S1 Appendix. Dataforthe 976 species usedinthis study.
(XLSX) S2 Appendix. ResultsofGLM analyses, showingvariablecoefficients.
(DOC) S3 Appendix. ResultsofGLMM analyses, showingvariablecoefficients.
(DOC) Acknowledgmen ts I am very grateful toD. Davison forher extensive workonthe initial literature searchesfor this study. Ithank E.Beever, J.Lenoir, andA.Phillimore formany helpful comments that greatly improved themanuscript.
Author Contributions Conceptualization: JohnJ.Wiens.
Investigation: JohnJ.Wiens.
Writing ±original draft:JohnJ.Wiens.
Writing ±review &editing: JohnJ.Wiens.
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