Invasions but not extinctions change phylogenetic diversity of angiosperm assemblage on

16 Pages·2017·8.5 MB·English

RESEARCHARTICLE
Invasions but not extinctions change
phylogenetic diversity of angiosperm
assemblage on southeastern Pacific Oceanic
islands
Gasto´nO.Carvallo1☯*,SergioA.Castro2,3☯
1 InstitutodeBiolog´ıa,FacultaddeCiencias,PontificiaUniversidadCato´licadeValpara´ıso,Valpara´ıso,
Chile,2 LaboratoriodeEcolog´ıayBiodiversidad,FacultaddeQu´ımicayBiolog´ıa,UniversidaddeSantiago,
Santiago,Chile,3 CentroparaelDesarrollodelaNanocienciayNanotecnolog´ıa(CEDENNA),Santiago,
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Chile
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a1111111111 ☯Theseauthorscontributedequallytothiswork.
a1111111111 *[email protected]
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Abstract
Weassessedchangesinphylogeneticdiversityofangiospermfloraonsixoceanicislands
OPENACCESS
locatedinthesoutheasternPacificOcean,bycomparingflorafromtwoperiods:thepre-
Citation:CarvalloGO,CastroSA(2017)Invasions Europeancolonizationofislandsandcurrenttimes.Wehypothesizethat,inthetime
butnotextinctionschangephylogeneticdiversityof
betweentheseperiods,extinctionoflocalplantspeciesandadditionofexoticplantsmodi-
angiospermassemblageonsoutheasternPacific
Oceanicislands.PLoSONE12(8):e0182105. fiedphylogenetic-α-diversityatdifferentlevels(deeperandterminalphylogeny)and
https://doi.org/10.1371/journal.pone.0182105 increasedphylo-β-diversityamongislands.Basedonfloristicstudies,weassembledaphy-
Editor:UlrichMelcher,OklahomaStateUniversity, logenetictreefromoccurrencedatathatincludes921species,ofwhich165and756were
UNITEDSTATES nativeorexoticinorigin,respectively.Then,westudiedchangeinthephylo-α-diversityand
Received:March3,2017 phylo-β-diversity(1–Phylosor)bycomparingpre-Europeanandcurrenttimes.Despite
extinctionof18nativeangiospermspecies,anincreaseinspeciesrichnessandphylo-α-
Accepted:July12,2017
diversitywasobservedforallislandsstudied,attributedtointroductionofexoticplants
Published:August1,2017
(between6to477speciesperisland).Wedidnotobservesignificantvariationofmeanphy-
Copyright:©2017Carvallo,Castro.Thisisanopen logeneticdistance(MPD),ameasureofthe‘deeper’phylogeneticdiversityofassemblages
accessarticledistributedunderthetermsofthe
(e.g.,orders,families),suggestingthatneitherextinctionsnorintroductionsalteredphyloge-
CreativeCommonsAttributionLicense,which
permitsunrestricteduse,distribution,and neticstructureoftheangiospermsoftheseislands.Inregardtophylo-β-diversity,we
reproductioninanymedium,providedtheoriginal detectedtemporalturnover(variationinphylogeneticcomposition)betweenperiodstoflora
authorandsourcearecredited.
(0.38±0.11).However,whenanalyseswereperformedonlyconsideringnativeplants,we
DataAvailabilityStatement:Theauthorsconfirm didnotobservesignificanttemporalturnoverbetweenperiods(0.07±0.06).Theseresults
thatalldataunderlyingthefindingsarefully
indicatethatintroductionofexoticangiospermshascontributedmorenotablythanextinc-
availablewithoutrestriction.Allrelevantdataare
tionstotheconfigurationofplantassemblagesandphylogeneticdiversityonthestudied
withintheSupportingInformationfiles.
islands.Becausephylogeneticdiversityiscloselyrelatedtofunctionaldiversity(speciestrait
Funding:FONDECYT11150301supportedGOC.
variationsandrolesperformedbyorganisms),ourresultssuggeststhattheintroductionof
CenterfortheDevelopmentofNanoscienceand
NanotechnologyCEDENNAFB0807(Line6)and exoticplantstotheseislandscouldhavedetrimentalimpactsforecosystemfunctionsand
ProyectoBasalUSA1555.48(USACH)supported ecosystemservicesthatislandsprovide(e.g.productivity).
SAC.Wedeclarethatthefundershadnorolein
studydesign,datacollectionandanalysis,decision
topublish,orpreparationofthemanuscript.
PLOSONE|https://doi.org/10.1371/journal.pone.0182105 August1,2017 1/16
Phylo-diversitychangesofflorainPacificislands
Competinginterests:Theauthorshavedeclared Introduction
thatnocompetinginterestsexist.
Human-mediatedglobalchangehasdeeplyimpactedbiodiversitycompositionandecosystems
functioning[1].Highextinctionrates[2,3]andtheintroductionofexoticspecies[4,5]arerec-
ognizedasimportantagentsofbioticchangesbecausethesefactorsmodifythestructuresof
communitiesandecologicalprocesses[2,6].Speciesimportedbyhumanstoareasfarfrom
theirnativegeographicrangeshaveimpactedthetaxonomic[7]andthephylogeneticstructure
ofcommunities[8],thus,exoticspeciesalterdirect(e.g.[9])andindirectinteractionsamong
species(e.g.[10]).Conversely,human-mediatedreductionofthegeographicrangesofspecies
hasresultedinriskofextinction[3],threatenedecosystemfunctioningandultimatelyhas
impactedhumanwellbeing[6].Asaresultoflocalextinctionsandspeciesintroduction,vari-
ouscommunitiesarebecomingsimilarintaxonomiccompositionbothinspaceandtime[11],
aphenomenonknownasbiotichomogenization[12,13].Althoughtheeffectsofbiotichomog-
enizationhavebeenstudiedmainlyinregardtotaxonomiccomposition,othercomponentsof
biodiversitysuchasphylogeneticandfunctionaldiversityarealsoimpactedbythelossofdis-
tinctivenessamongassemblages[8,12].
Thepatternsofevolutionaryrelationshipsamongtaxonomicentitieswithinlocalcommu-
nitiesareusedasproxiestoinferassemblymechanismswhichaccountforspeciescomposition
atdifferentspatiotemporalscales[14].Amongplants,thephylogeneticpropertiesoflocal
assemblagesareakeycomponenttounderstandingecologicalprocessessuchassuccessional
dynamics[15,16],productivity[17],invasionprocesses[18,19],andbioticinteractions[20,21,
22].Becausephylogeneticpropertiesaredeeplyconnectedtoecologicalprocessesandecosys-
temfunctioning[23],wecanassumethatphylogeneticsimilarityamongassemblagestrans-
latesintofunctionalsimilarity.Therefore,animportantissueisdeterminingthecontribution
ofextinctionsandintroductionsasmechanismswhichgeneratephylogeneticsimilarities
amongfloras[8].
Becausebothextinctionsandintroductionsofexoticspeciesarenon-randomlydistributed
withinlocalassemblages[24],theneteffectsoftheseprocessesinphylogeneticstructurefall
alongacontinuum,betweentwoextremes:theycouldfavourphylogeneticclustering(e.g.,the
speciesarefromsomeoverrepresentedclades)orphylogeneticoverdispersion(e.g.,thespecies
tendtobeevenlydistributedinphylogeny)[25].Asextinctionsandinvasionssimultaneously
occurwithinaregion,localassemblagescouldbegintoshowphylogeneticsimilarities.For
example,extinctionscontributetophylogeneticoverdispersionamongcomparableplant
assemblages,becausespecieslossesoccurinphylogeneticallydiversegroups[8].Ontheother
hand,whenassemblagesexperienceintroductionofexoticspeciesfromaparticularwide-
spreadinvasiveclade(e.g.,Asteraceae,Poaceaefamilies),theytendtoshowphylogeneticclus-
teringandahighdegreeofphylogeneticsimilarity[26,27].
Oceanicislandshaveahighdegreeofendemismanduniquenessofflora[28],onaccount
oftheirisolationandhighvulnerabilitytohumanimpacts[29–32].Manyoceanicislandshave
onlybeeninhabitedsincetheEuropeanexpansiontoothercontinents(ca.1500),whichallows
toempiricallyassesstheeffectsofhuman-mediateddisturbanceonbiodiversitycomponents.
Thisisincontrasttoassemblagesofcontinentalflora,wherethesimultaneouscontributionof
differentanthropogenicdriverscouldconfoundtheirrolesonbiodiversitystructure.Some
studieshaveevaluatedtheroleofextinctionsandinvasionsindeterminingthephylogenetic
structureofmainlandregions[8]andoceanicislands(see[33]forananalysisbasedonthe
nativeflora).Inthissense,whenhuman-inducedextinctionshavehappenedintenselyon
islands,significantchangesareobservedinthephylo-diversitywhencomparingpre-European
andcurrenttimecompositions.Ontheotherhand,becauseexoticplantintroductionsexceed
plantextinctions,asresultoftradeanddeliberateintroductions[34],andleadingtotaxonomic
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Phylo-diversitychangesofflorainPacificislands
similarity[29],human-inducedintroductionscouldcontributetoreducingthephylo-β-diver-
sityamongoceanicislandsinspiteofgeographicdistance.Toevaluatethesepredictions,we
conductedastudythatassessedpotentialchangesinphylogeneticdiversityofangiosperm
floraacrosssixislandsfromtheeasternportionofthePacificOcean.Specifically,ourstudy
aimedtoanswerthefollowingquestions:(i)towhatextenthasphylo-α-diversityofangio-
spermislandflorachangedbetweenpre-Europeancolonizationandcurrenttimes?(ii)Isthere
evidenceofadecreaseinthephylo-β-diversityoftheangiospermfloraamongthestudied
islands?
Materialsandmethods
Theislandsandtheirangiospermflora
Weexaminedthefloristiccompositionofangiospermsofsixoceanicislandslocatedinthe
southeasternPacificwheretaxonomichomogenizationhasbeenpreviouslyreported[35,36].
Thestudiedislandsaretheonlylandmasseswithin40millionkm2ofwatermassinthispartof
thePacificOcean[35].TheseemergedfromsubmarinevolcanicplumesduringthePlio-Pleis-
toceneperiod,amountingtoanareaofapproximately350km2[37].Thestudiedislands(Fig
1)includedtheJuanFerna´ndezarchipelago(includingRobinsonCrusoe´,SantaClara,and
AlexanderSelkirkIsland),EasterIsland,andtheDesventuradasarchipelago(includingSan
AmbrosioandSanFe´lixIsland).Amoredetaileddescriptionoftheislandscanbefoundin
[35].
Usingfloristicstudies,weassembledadatabaseoftheangiospermfloraoneachisland(S1
Table).Then,wecheckedthatspeciesinthedatabasewerepresentattheherbariaofthe
MuseoNacionaldeHistoriaNatural(SGO)andUniversidaddeConcepcio´n(CONC).Wedid
notdetectnewrecordsinourdatabaseafterreviewingherbariasheets.Afterflorawerecom-
piledforeachisland,synonymswereremovedandnomenclaturewasstandardizedbyusing
thePlantList(www.theplantlist.org).Basedontheserecompilations,wedividedangiosperm
florasintotwoperiods:(a)pre-Europeanflora,whichincludedthemostlikelycompositionof
nativeangiospermspeciesoneachisland,andincludedextinctspecies,(b)currentflora,
whichincludedactualcompositionofangiospermswithnativeandexoticplants,andexcluded
extincttaxa.Foreachisland,compiledpre-Europeanflorawereexclusivelycomposedofnative
species,includingextinctangiosperms(locallyextinctspecieswithoutherbariarecorded
withinthelast50years).Thecompiledcurrentfloraofeachislandincludedbothnativespecies
(excludingthoseextinct)andexoticangiosperms.Weconsideredexoticspeciesasallnatural-
izedandinvasiveplantsaccordingtocriteriaproposedby[38],basedonindependentrepro-
ductionforatleast10yearswithouthumanintervention[38].Therefore,weconsideredas
exoticangiospermonlythosetaxaabsentinearlyfloristicstudies,andoccurredatleasttwice
inherbariarecordswithaspanof10yearsbetweenspecimenregistries.
Floristicstudiesconsideredtobuildourdatabasedependontheindividualstudyarea.For
theDesventuradasarchipelago(DA),wehaveincludedinformationfromthefirstbotanicalcol-
lectionin1869[39]aswellasthatfromsubsequentexpeditions[40–46]andtaxonomicalstud-
ies[47–49].TheDesventuradasarchipelagohasnopermanenthumanpopulationand,todate,
nospecieshavebeenreportedasextinctonthisarchipelago.ForJuanFerna´ndezarchipelago
(JFA),weusedinformationfromthefirstcollectionthatbeganin1879[50],complemented
withthestudiesofJohow[51]andSkottsberg[52].Althoughhumansdidnotoriginallyinhabit
theislandsoftheJFA,sincetheirdiscoveryin1574,theyhaveheldapermanenthumanpopula-
tionand,presentlyreceivetourists.AmongthePacificislands,thoseoftheJFAhaveoneofthe
mostcomprehensivesetsoffloristicinformationavailable,whichallowsclearidentificationof
exoticandnativeplants,aswellasextincttaxa[48,53–60].RegardingEasterIsland(EI),
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Phylo-diversitychangesofflorainPacificislands
Fig1.Generalaspectsofthestudiedsystem.(a)AmapshowsthegeographicallocationofthesoutheasternPacificislandsincludedinthisstudy(red
circles):EasterIsland(EI),Desventuradasarchipelago(DA)andJuanFerna´ndezarchipelago(JFA).(b)Graphicalmodelsummarizingpotentialeffectsof
plantextinctions(bluebranches)andexoticintroductions(redbranches)onthephylogeneticdiversityofislandflora.(c)AnaerialviewofCumberlandBay
atRobinsonCrusoe´Island,JuanFerna´ndezarchipelago;whitearrowsindicatepresenceofthedominantexotictreesEucalyptusglobulus(Myrtaceae)and
Ailanthusaltissima(Simaroubaceae);photographkindlyprovidedbyG.Rojas.(d)Cirsiumvulgare(Asteraceae)anexoticnaturalizedplantonEaster
Island;photographkindlyprovidedbyG.Rojas.
https://doi.org/10.1371/journal.pone.0182105.g001
inhabitationbyPolynesianpeoplemodifiedflora,causingextinctionofsomeplanttaxa[61].
Botanicalrecordsareavailablesinceitsdiscoveryin1722andsubsequentcolonization[48,62–
66],whichallowsdistinctionofnativeandexoticplants,andidentificationofextinctionsfol-
lowingEuropeancolonization.
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Phylo-diversitychangesofflorainPacificislands
Phylogenetictree
Basedonthechecklistofspeciesrecordedfortheislands,weassembledaphylogenetictree
with921angiospermtaxausingPHYLOMATIC[67](http://www.phylodiversity.net/
phylomatic/accessedJanuary12,2017)usingtreeversionR20120829isbasedontheAPGIII
phylogeneticclassificationofangiosperms[68].Withinfamilies,thephylogeneticrelationships
amonggenerawereresolvedthroughreorderingbyhandtheobtainedtopologybasedonpub-
lishedphylogenies(the“graft”method,[69])usingMesquite2.74(availableatURLwww.
mesquiteproject.org).ThefulllistofconsultedreferencesisprovidedinS2Table.Theresulting
topologywasage-calibratedbasedonthedivergencetimesofangiospermsreportedby[70]
usingtheBLADJalgorithmimplementedinPHYLOCOM[71].Weobtainedatreewith921
tipsand654internalnodes,whichaccountsfor71%oftheinternalnodesresolved(S1Fig).
Complementarily,weassembledatreeexclusivetonativeplants(205taxa)followingthesame
methodology;inthistree,74%oftheinternalnodeswereresolved(S1Fig).Althoughmeasures
ofcommunityphylogeneticdiversityaremoresensitivetolossofresolutionbasallyinthephy-
logeny,andlesssensitivetolossofresolutionterminally[72],ourlevelsofunresolvednodes
wasrelativelylowandshouldnotsignificantlyimpactestimatedindexes.Ontheotherhand,
theuseofPHYLOMATICandthegraftmethodiscontroversial(see[69]forananalyticalcrit-
icismofthismethod).Wechosethistoolbecauseseveralofourspeciesareextinctordonot
havegeneticsequencesavailableinGenBank.
Estimationofphylo-α-diversity
Phylo-α-diversitywasestimatedforeachislandaccordingtopre-Europeanandcurrentflora,
basedonatreebranchlengthindex(Faith’sindex[73])andtwodistance-basedindexes:the
meanphylogeneticdistance(MPD)andthemeannearesttaxondistance(MNTD)[25].Faith’s
indexisthesumofthebranchlengthsconnectingallspeciesinanassemblage[74].TheMPD
isthemeanofallphylogeneticdistancesthatoccurbetweenallspeciespairswithinanassem-
blage[25,75]andisinterpretedasanindicatorofthe‘deeper’phylogeneticdiversityofthe
studiedflora[76,77].TheMNNDisthemeanofthephylogeneticdistancesthateachterminal
nodehaswiththeirclosestrelativeswithinanassemblage[25,75,78].Itisinterpretedasthe
‘terminal’phylogeneticdiversity,whichreflectstheinfluenceofrelatively‘recent’events(e.g.,
localextinctions,migrations)onassemblagestructure[77].Alltheseindexeswereindepen-
dentlyestimatedforflorasofthepre-Europeantime(originalflora,includingextinctspecies)
andcurrentfloras(actualfloracomposition,excludingextinctspeciesandincludingexotic
plants).Inaddition,indexeswereestimatedexclusivelytonativeplantspeciesforeachstudied
period,tocomparethecontributionofextinctionsonphylo-diversity.Indexeswereestimated
basedonacalibratedtree(asachronogram)andthenexpressedinmillionsofyears.Because
allislandassemblagesshoweddifferentlevelsofspeciesrichness(Table1),indexeswerestan-
dardized,whichallowedremovalofbiasesassociatedwithdifferencesinspeciesrichness[74].
Standardizedeffectsize(SES)wasestimatedas(observed–mean )(cid:1)(sd )-1,whereobservedis
null null
thedirectlyestimatedindex,mean isthemeanoftheindexesobtainedafter999randomiza-
null
tionsandsd isthestandarddeviationoftheestimatedindexesafterrandomization.Stan-
null
dardizedMPD(MPD )andMNTD(MNTD )alsoasknownasnetrelatednessindex
SES SES
(NRI)andnearesttaxonindex(NTI),respectively[25,78].Theseindexesareestimatorsof
phylogeneticclustering(NRIorNTI>1)oroverdispersion(NRIorNTI<1)[25,79].We
assessedwhether95%confidenceintervalsofNRIandNTIobtainedfrompooledisland
(N=6islands)weregreaterthan1.96(phylogeneticclustering)orlowerthan-1.96(phyloge-
neticoverdispersion).Forallstandardizations,werandomizedthephylogenytiplabelsacross
alltaxaincludedinthetrees,weusedthisapproximationtomaintainthespatialstructureof
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Phylo-diversitychangesofflorainPacificislands
Table1. AngiospermsrichnessofsixsoutheasternPacificoceanicislandsdifferentiatingpre-Europeanandcurrenttimes.
Pre-European Currenttime
Island Location(lat;long) Complete(allnatives) Complete(nativeplusexoticplants) Nativeplants Exoticplants
SanFe´lix 26˚17’S;80˚05’W 9 15(67%) 9(0%) 6
SanAmbrosio 26˚20’S;79˚53’W 19 25(32%) 19(0%) 6
Easter 27˚06’S;109˚20’W 40 366(815%) 26(-35%) 340
RobinsonCrusoe´ 33˚38’S;78˚50’W 100 575(475%) 98(-2%) 477
SantaClara 33˚42’S;78˚56’W 12 53(342%) 12(0%) 41
AlejandroSelkirk 33˚45’S;80˚47’W 71 217(206%) 69(-3%) 148
Observedrichnesstocurrenttimedifferencednativeandexoticspecies;valuesinparenthesisarepercentageofchangebetweencomparedperiods.We
alsoincludedtheobservedrichnessofexoticangiosperms(onlycurrenttime).
https://doi.org/10.1371/journal.pone.0182105.t001
speciesinthesystem.Otherconstrainednullmodelsthatfocusonrandomizingthecommu-
nitydatamatrix,ratherthanthephylogeny,generatethatanyspatialcontagionordispersal
limitationisnotmaintainedinthenullcommunitydatamatrices[74].Forallourestimations,
weusedthepicantepackage[80]toR3.0(RDevelopmentCoreTeam).
Weperformedtwokindsofanalyseswiththeobtainedindexesaswellasplantrichness.For
thenon-standardizedindexes,weestimatedthepercentofchangeforeachislandbycompar-
ingthepre-Europeanandcurrentfloras;wethenassessedwhetherthesepercentagesdeviated
fromthenullexpectation(μ=0)usingatwo-tailedt-test.Forthestandardizedindex(SES),
weperformedapairedt-testthatcontrastedtheobtainedvaluesbetweenthepre-European
andcurrentfloras.Theseanalyseswereperformedtocomparepre-Europeanandcurrent
timesforcompleteflorasandtoonlynativespecies.
Estimationofphylo-β-diversity
Thephylogenetic-β-diversity(phylo-β-diversity,herein)wasestimatedas1–Phylosor,
wherePhylosorisasimilarityindexthatcomputesthefractionofsharedphylogenetic
branchlengthsbetweentwosamples[81].Thephylo-β-diversityhasvaluesthatrangefrom
0(phylogenetichomogenizationbetweencomparedassemblages)to1(phylogeneticturn-
overbetweencontrastedassemblages).Thephylo-β-diversitywasestimated(i)between
times,bycomparingeachislandbetweenpre-Europeanandcurrenttimes,and(ii)among
islandswithineachstudiedperiod.Phylogeneticdifferencesamongislandswerecorrelated
togeographicaldistanceforeachstudiedperiod,usingaMantel’stest[82].Inthisway,we
aimedtodetecttemporalorspatialphylogeneticturnover.Alltheseanalyseswereper-
formedoncompleteflorasandononlynativespecies.BecausePhylosorisrelatedtothe
speciesrichnessandtheunderlyingtaxonomicbetadiversity[74],theobservedPhylosor
valueswerecomparedtonullvaluesgeneratedbyrandomlyshufflingtaxanamesinthe
phylogeny999times(SES ).Duringeachiteration,thePhylosorwasestimatedfor
Phylosor
eachislandpair,andthesenulldistributionswereusedtocalculatethestandardizedeffect
sizes,wherethemeanofthenulldistributionwassubtractedfromtheobservedmeandis-
similarityandthendividedbythestandarddeviationofthenulldistribution[76].Ran-
domizationproceduremaintainedthecommunitypresence–absencematrix.Because
SES valueisexpressedinunitsofstandarddeviation,valuesbetween-1.96to1.96
Phylosor
indicateno-deviationfromchance[74,83].Toassessthestatisticalsignificanceofthe
changes(eachislandbetweentimesandamongislandswithineachstudiedperiod),we
contrastedtheaverageofestimatedphylo-β-diversitywithanullexpectationofμ=0.
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Phylo-diversitychangesofflorainPacificislands
Results
Overall,weobservedasignificantincreaseof323%±120inangiospermrichness(mean±SE,
N=6islands)whenthecompletepre-Europeanandcurrentfloraswerecompared(Table1)
(resultoft-test:t=2.7,P=0.021),withthegreatestincreaseonEasterIsland(815%)andthe
lowestonSanAmbrosioIsland(32%,Table1).Thisincreasewasduetotheadditionofexotic
angiospermstoislands(Table1).Thenativeflorashowed,onaverage,anon-significant
decreaseinrichnessof7%±6(N=6islands;t=1.7,P=0.853);andthreeislandsdidnot
exhibitchangeinnativeangiospermrichnessbetweenthecomparedperiods:SanFe´lix,San
AmbrosioandSantaClara(Table1).Thisresultquantifiedlocalextinctionsforislands,with
EasterIslandhavingthehighestvalue(Table1).
Amongnativeplantspecies,weobservedthegreateroccurrenceforpre-Europeantimeas
Spergulariaconfertiflora(Caryophyllaceae),whichinhabitedfourislands:AlejandroSelkirk,
RobinsonCrusoe´,SantaClaraandSanFe´lixislands;inthisperiod81%,17%and2%ofthe
205nativeplantsoccurredononlyone,twoandthreeislands,respectively(S1Table).Forcur-
renttimes,Tetragonia tetragonoides(Aizoaceae)showedthegreateroccurrenceforfiveislands:
AlejandroSelkirk,Easter,RobinsonCrusoe´,SanAmbrosioandSantaClaraislands(S1Table);
inthisperiod78%,18%,3%and0.5%ofthe183nativespeciesoccurredononlyone,two,
threeandfourislands,respectively(S1Table).
Thetree-basedphylo-α-diversity(Faith’sindex)showedasignificantincreaseof157%±56
(N=6islands)tocompletefloraofangiosperms(t=2.8,P=0.039;Table2),althoughwedid
notobservestatisticalchangesforthenativeassemblage(-11%±9;t=1.2,P=0.276),inspite
oflocalextinctions.Specifically,thehighestchangesofFaith’sindexwereforEaster,Robinson
Crusoe´,SantaClaraandAlejandroSelkirkislands(>100%change,Table2).Threeislands
(SanAmbrosio,SanFe´lixandSantaClara)didnotvaryinFaith’sindextonativeflora,because
theirtaxonomiccompositiondidnotchangebetweencomparedtimes(Table2).Concerning
tree-basedmeasure,theMPDshowednon-significantdifferencesbetweenthepre-European
andcurrentflorastothecompleteangiospermflora(-2.4%±1.4;t=1.76,P=0.139)aswell
asthenativefloraofangiosperms(-2.6%±2.6;t=0.9,P=0.373).TheMNTDshoweda
Table2. Phylogeneticα-diversity(inmillionsofyears)ofangiospermflorafromsixsoutheasternPacificoceanicislands.
PD MPD MNTD
Islands Period Completeflora Natives Exotics Completeflora Natives Exotics Completeflora Natives Exotics
SanFe´lix(DA) Pre-European 889 227.9 156.7
Current 1,031 709 661 213.5 249.4 199.5 88.1 190.1 80.3
SanAmbrosio(DA) Pre-European 1,472 240.3 94.3
Current 1,607 1,151 1,003 225.5 240.9 210.5 76.8 135.5 108.1
EasterIsland Pre-European 2,849 261.2 111.9
Current 12,760 885 12,580 257.6 216.4 257.0 46.8 67.9 47.9
RobinsonCrusoe´(JFA) Pre-European 4,701 259.4 57.7
Current 18,078 4,247 16,081 260.6 259.5 260.2 41.6 61.0 42.8
SantaClara(JFA) Pre-European 1,083 231.2 132.3
Current 2,802 935 5,432 236.0 231.9 238.3 69.3 131.6 73.6
AlejandroSelkirk(JFA) Pre-European 3,725 265.4 60.6
Current 7,646 3,195 5,977 255.7 267.4 250.3 43.6 71.4 46.7
Phylogeneticdiversityindexesreportedforeachperiod:Faith’sindex(PD),meanphylogeneticdistance(MPD)andmeannearesttaxondistance(MNTD).
Estimatorstocompleteangiospermfloraanddifferentiatingnativeandexoticplants(onlycurrenttime).Abbreviationsafterislandnamesdepictarchipelago
name:JuanFerna´ndezarchipelago(JFA)andDesventuradasarchipelago(DA).
https://doi.org/10.1371/journal.pone.0182105.t002
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Phylo-diversitychangesofflorainPacificislands
significantdecreaseforangiospermflora(-37%±6;t=6.1,P=0.002),althoughthenative
angiospermsdidnotshowdifferencesbetweenthecontrastedperiods(-7%±7;t=1.0,
P=0.359).
Becausephylogeneticdiversityindexesarecorrelatedtospeciesrichness,ouranalyseswere
alsoperformedusingstandardizedeffectsize(SES)indexes(Fig2).Forthestandardized
Faith’sindex,wedidnotobservesignificantdifferencesbetweenthepre-Europeanandcurrent
floras,neitherforthecompleteflora(t=1.9,P=0.110,resultofpairedtest)northenative
flora(t=1.3,P=0.252)(Fig2A).ThestandardizedMPD(netrelatednessindex,NRI)showed
differencesbetweenthecontrastedtimesforthecompleteflora(t=3.9,P=0.011)butnotfor
thenativeflora(t=0.9,P=0.390)(Fig2B).Lastly,thestandardizedMNTD(nearesttaxon
index,NTI)showednon-significantdifferencesbetweenthecontrastedfloras,bothforthe
complete(t=1.53,P=0.187)andnativeflora(t=1.19,P=0.285)(Fig2C),althoughvaluesof
completefloraindicatesphylogeneticoverdispersionforthecurrenttime(Fig2C).
Inregardtophylo-β-diversity,whencompletefloraofangiospermswerecompared
betweenpre-Europeanandcurrenttimesforeachisland,weobservedavalueof0.38±0.11
(meanof1-Phylosor±SE;N=6pairs;resultofcontrastfromnullexpectationμ=0:t =3.3,
1,5
P=0.010).However,thesamecomparisontonativeflorashowedadifferenceof0.07±0.06
(N=6pairs)betweencomparedtimesforeachisland;thisdifferencedidnotdeviatedfrom
nullexpectationμ=0(t =1.3,P=0.127).Theseresultsevidenceanimportantchange
1,5
betweenthestudiedperiods,forcompleteflorabutnotfornativeflora.Inregardtochange
withineachstudiedperiod,completeflorashowedaphylo-β-diversityof0.60±0.04topre-
European(N=15pairs;deviationfromnullexpectationμ=0t =15.0,P<0.001)and
1,14
0.67±0.05tocurrenttime(N=15pairs;t =14.1,P<0.001).Theseresultsevidencespatial
1,14
turnoveramongislands,althoughphylogeneticdiversitywasnotcoupledtogeographicdis-
tance(Fig3A)neithertopre-European(MantelR=0.292;P=0.066)norcurrenttime(Mantel
R=0.165;P=0.073).Tonativeflorawithincurrenttime,phylo-β-diversityshowedavalueof
0.57±0.04(N=15pairs;deviationfromnullexpectationμ=0t =15.5,P<0.001)andthis
1,14
didnotexemplifyarelationshiptogeographicaldistanceamongislands(MantelR=0.196;
P=0.218)(Fig3B).
Discussion
Arecognizedpatterninthefaceoftheeraofglobalchangeisthatspeciesintroductionshave
contributedtoincreasesinthetaxonomicdiversityofvascularplants[84],withthesizeofthe
floraofseveralislandsincreasingbyasmuchas100%[85–87].Thispattern,previously
describedfortaxonomicdiversity[35],isnowalsoobservedforthephylogeneticdiversity,
whichincreasedby157%betweenpre-Europeanandcurrenttimes(Faith’sindex).Because
nativeangiospermsdidnotsignificantlychangebetweenpre-Europeanandcurrenttimes
(Faith’sindex),ourresultssuggestthischangeismainlyattributedtoexoticplants.Increases
inphylo-α-diversitydidnotoccuratalllevels,asweobserveddifferentresultsaccordingtothe
indexused.Theindexrelatedtothe‘deeper’structureofaphylogeny(MPD),whichthus
accountsforthephylogeneticdiversityattheleveloftaxonomicordersorfamilies,didnot
showstatisticallysignificantchangeswhenthenativefloraofpre-Europeanandcurrenttimes
werecompared.Thisresultindicatesthatanyextinctionsthatoccurredontheseislandsduring
thelastca.500yearsdidnotsignificantlyerodephylogeneticdiversity,andthatinvasionshave
contributedtohomogenizationofphylogeneticdiversityofangiospermassemblage.Forexam-
ple,AlejandroSelkirkandRobinsonCrusoe´Islands,whichlost7%and3%oftheirnative
angiospermsbetweenpre-Europeanandcurrenttimes,respectively,didnotshowanychanges
inMPDvalue.Thiscouldbeattributedtoextinctionsthatoccurredwithinoverrepresented
PLOSONE|https://doi.org/10.1371/journal.pone.0182105 August1,2017 8/16
Phylo-diversitychangesofflorainPacificislands
Fig2.Standardizedeffectsize(SES)ofphylo-α-diversityindexesforpre-Europeanandcurrenttime.
(a)Faith’sindex(PD),(b)netrelatednessindex(NRI,aMPD )and(c)nearesttaxonindex(NTI,a
SES
PLOSONE|https://doi.org/10.1371/journal.pone.0182105 August1,2017 9/16
Phylo-diversitychangesofflorainPacificislands
MNTD ).Circlesdepictingmeanofestimators(N=6islands)anddeviationsare±2SEtocompleteflora
SES
(greycircles)andnativeflora(blackcircles).Dashedlinesdepictlimitsofnullexpectation;valuesabove1.96
suggestphylogeneticclustering,andbelow-1.96indicatephylogeneticoverdispersion.
https://doi.org/10.1371/journal.pone.0182105.g002
clades,withphylogeneticallyrelatedplantspeciesremainingontheislands.Inspiteofthe
extinctionsofPodophorusbromoides(Poaceae)andRobinsoniamacrocephala(Asteraceae)on
RobinsonCrusoe´Island,severalnativespeciesofthePoaceaefamilyremain(4species)aswell
asspeciesfromtheRobinsoniagenus(6species).Similarly,onAlejandroSelkirkIsland,effects
oftheextinctionofChenopodiumnesodendrum(Amaranthaceae)orEmpetrumrubrum(Erica-
ceae)couldbemaskedbyotherremainingspeciesofthesamefamiliesorordersontheislands,
suchasSarcocorniafruticosa(Amaranthaceae)orGaultheriaracemulosa(Ericaceae).Onthe
otherhand,exoticspeciesbelongingtocladesalreadypresentdidnotsignificantlycontribute
tochangingthe‘deeper’structureofthephylogeneticdiversityonthestudiedislands.Inlight
ofthesefindings,theneteffectofextinctionsandintroductionsonthedeeperphylogenetic
structurecouldbeconsideredneutral.
Intermsofthe‘terminal’phylogeneticdiversity(MNTD),thediversityreflectingcloserela-
tionshipsamongspecifictaxa(e.g.species),wedidnotobservechangesbetweenthecompared
periodsforthenativeflora(exceptonEasterIsland);however,forthecurrenttimeweob-
servedatendencytophylogeneticoverdispersionofflora.OnEasterIsland,alonghistoryof
Polynesianoccupationhasleftanimpoverishedlandscapeandafloristiccompositionthat
seemtobeveryfarfromtheoriginal[61,88].Thissituationhascausedextinctionsthat
occurredwithincladeswithfewrepresentatives,suchasCaesalpiniaglobulorumandSophora
toromiro,bothfromFabaceaeandexclusiverepresentativesofFabales,aswellextinctionof
Elaeocarpusfloridanus(Elaeocarpaceae,exclusiverepresentativeofOxalidales),Macaranga sp.
(Euphorbiaceae)andXylosma suaveolens(Salicaceae)representativesofMalpighiales.Also,
theextinctionofMetrosideros collina(Myrtaceae,theonlymemberofMyrtales),Paschalococ-
cosdisperta(Arecaceae,theonlyrepresentativeofArecales),Potamogetonsp.(Potamogetona-
ceae,fromAlistamales),Prenmaserratifolia(theonlymemberofLamiaceaeandfromthe
orderLamiales)andSamolusrepens(PrimulaceaetheonlyrepresentativeofEricales).The
extinctionoftheseplantsimportantlycontributedtodecreasesinMPDandMNTDonEaster
Island.However,thedecreaseinMNTDduringcurrenttimesfortheotherislandscouldbe
attributedtotwonon-exclusivepotentialexplanations.First,theislandscouldhavereceived
speciesfromsimilarwidespreadanddiverseclades,suchasPoaceae(84exoticspeciesfrom49
genera),Asteraceae(72speciesfrom57genera),Fabaceae(70speciesfrom40genera),Malva-
ceae(22speciesfrom17genera),Lamiaceae(22speciesfrom13genera),Solanaceae(23spe-
ciesfrom9genera)andRosaceae(20speciesfrom12genera),causingadecreaseinthe
phylogeneticdiversityandcontributingtophylogeneticoverdispersion.Secondly,environ-
mentalconditionsthatoperateasbothabioticandbiotic‘habitatfilters’forexotics,suchascli-
mate,soiltypeorinterspecificinteractions[89],couldcontributetomaintainingphylogenetic
overdispersion.
Inregardtothephylo-β-diversity,weobservedagreaterdifferentiationamongislands
withinperiods,thanbetweenthestudiedperiodsforeachisland.Interestingly,thephylo-β-
diversityofnativespeciesslightlydecreasedfrompre-Europeantocurrenttimes,whichsug-
gestthatdifferencesbetweentimesismainlyduetoarrivalofexoticangiospermswithinrecent
decades.Inaddition,theincreaseofphylo-β-diversityforcompleteflorainthecurrenttime
suggeststhatexoticspeciescontributetothephylogenetichomogenizationoftheseislands.
Wehavedescribedasignificantchangeinthephylogeneticdiversityamongislands
betweentwoperiods–oneassociatedwiththepre-industrialrevolution,andonerelatedto
PLOSONE|https://doi.org/10.1371/journal.pone.0182105 August1,2017 10/16