Diversity and composition of herbaceous angiosperms along gradients of elevation and forest-use

17 Pages·2017·7.81 MB·English

RESEARCHARTICLE
Diversity and composition of herbaceous
angiosperms along gradients of elevation and
forest-use intensity
JorgeAntonioGo´mez-D´ıaz1*,ThorstenKro¨mer2,HolgerKreft3,GerhardGerold1,Ce´sar
IsidroCarvajal-Herna´ndez4,FelixHeitkamp1
1 SectionofPhysicalGeography,Georg-August-Universita¨tGo¨ttingen,Go¨ttingen,Germany,2 Centrode
InvestigacionesTropicales,UniversidadVeracruzana,Xalapa,Veracruz,Mexico,3 Departmentof
Biodiversity,Macroecology&Biogeography,Georg-August-Universita¨tGo¨ttingen,Go¨ttingen,Germany,
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4 HerbarioCIB,InstitutodeInvestigacionesBiolo´gicas,UniversidadVeracruzana,Xalapa,Veracruz,Mexico
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Abstract
Terrestrialherbsareimportantelementsoftropicalforests;however,thereisalackof
researchontheirdiversitypatternsandhowtheyrespondtodifferentintensitiesofforest-
OPENACCESS
use.Theaimofthisstudywastoanalyzethediversityofherbaceousangiospermsalong
Citation:Go´mez-D´ıazJA,Kro¨merT,KreftH,Gerold
gradientsofelevation(50mto3500m)andforest-useintensityontheeasternslopesofthe
G,Carvajal-Herna´ndezCI,HeitkampF(2017)
Diversityandcompositionofherbaceous CofredePerote,Veracruz,Mexico.Werecordedtheoccurrenceofallherbaceousangio-
angiospermsalonggradientsofelevationand spermspecieswithin120plotsof20mx20meach.Theplotswerelocatedateightstudy
forest-useintensity.PLoSONE12(8):e0182893.
locationsseparatedby~500minelevationandwithinthreedifferenthabitatsthatdifferin
https://doi.org/10.1371/journal.pone.0182893
forest-useintensity:old-growth,degraded,andsecondaryforest.Weanalyzedspeciesrich-
Editor:RunGuoZang,ChineseAcademyof
nessandfloristiccompositionofherbcommunitiesamongdifferentelevationsandhabitats.
Forestry,CHINA
Ofthe264plantspeciesrecorded,31areendemictoMexico.Bothα-andγ-diversitydisplay
Received:September16,2016
ahump-shapedrelationtoelevationpeakingat2500mand3000m,respectively.Therela-
Accepted:July26,2017 tivecontributionofbetween-habitatβ-diversitytoγ-diversityalsoshowedaunimodalhump
Published:August8,2017 whereaswithin-habitatβ-diversitydeclinedwithelevation.Forest-useintensitydidnotaffect
α-diversity,butβ-diversitywashighbetweenold-growthandsecondaryforests.Overall,γ-
Copyright:©2017Go´mez-D´ıazetal.Thisisan
openaccessarticledistributedunderthetermsof diversitypeakedat2500m(72species),drivenmainlybyhighwithin-andamong-habitatβ-
theCreativeCommonsAttributionLicense,which diversity.Weinferthatthisbeltishighlysensitivetoanthropogenicdisturbanceandforest-
permitsunrestricteduse,distribution,and
useintensification.At3100m,highγ-diversity(50species)wasdrivenbyhighα-andwithin-
reproductioninanymedium,providedtheoriginal
habitatβ-diversity.There,losingaspecificforestareamightbecompensatedifsimilar
authorandsourcearecredited.
assemblagesoccurinnearbyareas.Thehighβ-diversityandendemismsuggestthatmixes
DataAvailabilityStatement:Allrelevantdataare
ofdifferenthabitatsareneededtosustainhighγ-richnessofterrestrialherbsalongthisele-
withinthepaperanditsSupportingInformation
files. vationalgradient.
Funding:Thisworkwassupportedbythe
DeutscheForschungsgemeinschaft(HE6726/4).
Researchermobilitywasgrantedwithintheproject
BIOVERAtoTK(CONACyT)andFH(bytheDAAD
withfundingoftheBundesministeriumfu¨rBildung Introduction
undForschung(BMBF)).JAGDwasfundedbythe
Themajorityofbiomesareundergoingrapidchanges,especiallyinthetropics[1].Conse-
ConsejoNacionaldeCienciayTecnolog´ıa(216230/
311672)andtheDeutshceAkademischer quently,growinghumanpressureonecosystemsposesamarkedthreattoglobalbiodiversity
PLOSONE|https://doi.org/10.1371/journal.pone.0182893 August8,2017 1/17
Herbdiversityalonggradientsofelevationandforest-useintensity
Austauschdienst(91549681).TheresearchofTK [2].Consideringcurrentratesofdeforestationandforestdegradation[3],undisturbedforests
wassupportedbyCONACyT.Thefundershadno willbecomescarceandincreasinglyfragmented[4].Deforestationforagriculture,aswellas
roleinstudydesign,datacollectionandanalysis,
non-sustainableagrarianandforestrypractices,increasesthedemandfornewlandthreaten-
decisiontopublish,orpreparationofthe
ingprimaryforestsandassociatedbiodiversity[5].Forest-useintensityisdefinedasaforest
manuscript.
disturbancederivedfromthehumanactionactingatabroaderlandscapelevel.Theeffectsof
Competinginterests:Theauthorshavedeclared
forestconversiononplantdiversityarewellknown[6];however,thereisalackofknowledge
thatnocompetinginterestsexist.
onhowanthropogenicforest-useintensityaffectsdiversityandcompositionofplantcommu-
nities[7].Forestdegradationmayhavedifferenteffectsonbiodiversity,dependingontheeco-
system,thekindofdegradation(temporalandspatialextent,intensity)andthetaxaofinterest
[6].
Aglobalmeta-analysisoftrendsofforestdegradationfoundanaveragelossof18%ofspe-
ciesrichnessduetoforestuse[8].Accordingtotheanalysis,land-usechangeandtheincrease
ofnon-nativeinvasivespecieshavethehighestnegativeimpactonspeciesrichness[8].How-
ever,somelandscapeshaveexperiencedincreasesinplantspeciesrichnessbecauseinvasions
ofexoticspeciesareexceedingthelossofnativespecies[9].Themagnitudeofanthropogenic
changeandhighdiversityintropicalmountainscallsformorestudiestoidentifythepatterns
ofdiversitychangeduetoforest-useintensityalongelevationalgradients[10].
Littleisknownabouttheinfluenceofforest-useintensityonherbaceousangiosperms
despitetheirimportancefortropicaldiversityandecosystemfunction[11].Thefewstudies
availablehavemixedresultswithforest-useintensityreportedtohavepositive,neutral,orneg-
ativeeffects[12].Moreover,highnumbersofprimaryforestspeciesandendemicspecieshave
beenfoundinnaturallyregenerating[13]andsecondaryforests.Thus,suchhabitatsmight
helptoconserveendemicspecies[14].Forestusemayalsoleadtoanincreaseinspeciesnum-
bersduetoanalterationofthelightregimeandasuppressionofmorecompetitiveherbs[15].
Contrastingfindingsmayreflectdifferentstudyconditions(biome,ecosystem,taxaofinter-
est),differentscales(e.g.landscape,plot)andsamplingtechniquesinvolved[16].Therefore,it
isimportanttocarryoutmoreempiricalresearchtoquantifytheeffectsofforest-useintensity
onherbsusingarobustandreplicatedstudydesignthataccountsforthedifferentcomponents
ofherbdiversity(α,β,andγ).
Despitetheuncertaintiesaboutforest-useintensityeffectsonspeciesrichness,changesin
speciescompositionhavebeenreportedoftenwiththerarestspeciesfoundmainlyinnative
communities[17].Severalstudieshaveshownthatwithincreasingforest-useintensity,local
(α-diversity)andtotal(γ-diversity)speciesrichnessdeclinedlinearly,whereasspeciesturnover
betweenplotsincreased[18].Theforest-useintensityinthemostintensivelyusedplotsledto
sparseherblayerandreducedspeciesrichness[19].
Studiesonlatitudinalandelevationalgradientsshowthateffectsofforest-useintensityon
plantdiversitymaychangedependingontheecosystemorecozone.Ingeneral,α-andγ-diver-
sityofplantsdecreasewithincreasinglatitude,[20,21],andthehighestdiversityofplantsand
variousotherstaxaisusuallyconcentratedintropicallowlandareaswithhighandevenlydis-
tributedrainfall[22,23].Severalstudiesoftropicalelevationalgradientshaveshownmid-ele-
vationspeaksinspeciesdiversityfollowedbyalineardecrease[20]forvariousplantgroups
[24].Mostofthepreviousstudiesonelevationalgradientsofforestherbsfocusedonselected
herbaceousfamilies[25]andwereconductedinnear-naturalecosystems.Giventheongoing
degradationofprimaryforests[6],studiesonelevationalgradientsshouldbeextendedto
includehabitatsthatdifferinforest-useintensityoranthropogenicinfluence.
Thisstudyaimstoassesshowherbaceousangiospermdiversityvariesalongelevationalgra-
dientsinthetropicsandhowthosepatternsareaffectedbyvariationinforestuseintensity.
Wethusfocusedonpatternsofα-,β-,andγ-diversityofherbaceousangiospermsalongcom-
binedgradientsofelevationandforest-useintensity.Thestudywasconductedalongthe
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Herbdiversityalonggradientsofelevationandforest-useintensity
Fig1.MapoftheEasternslopesoftheCofredePeroteinVeracruzstate,Mexico.Blackdotsshowthestudylocations.1=LaMancha,2=
Palmarejo,3=Chavarrillo,4=LosCapulines,5=ElZapotal,6=ElEncinal,7=LosPescados,and8=ElConejo.
https://doi.org/10.1371/journal.pone.0182893.g001
EasternslopesofthevolcanoCofredePeroteincentralVeracruz,Mexico,alonganelevational
gradientfromsealevelupto3500m,whichexhibitsalargerangeofenvironmentalconditions
overashortgeographicdistanceofjustc.80km.Weestablishedplotsateightdifferentloca-
tions(separatedbyc.500minelevation)andwiththreedifferentforest-useintensities(old-
growth,degraded,andsecondaryforest).
Methods
Studyarea
Weestablishedeightsitesalonganelevationalgradientbetween30and3540montheEastern
slopesoftheNationalParkCofredePerote,anextinctvolcanoof4282melevationinthecen-
tralpartofthestateofVeracruz,Mexico(Fig1).Thisregionislocatedatthejunctionofthe
Trans-MexicanvolcanicbeltandtheSierraMadreOriental,amountainousareabetween19˚
25’5.7”and19˚36’54”Nand94˚44’43.5”and97˚09’36.9”W.ThestateofVeracruzcovers
72420km2andhasadiverseangiospermflora(6876species),whichrepresentsabout31%of
theMexicanflora[26].Morethan80%ofVeracruz’primaryvegetationhasbeenconverted
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Herbdiversityalonggradientsofelevationandforest-useintensity
Table1. ListofthestudylocationsandclimaticconditionsalongtheelevationalgradientattheCofredePerote,centralVeracruz,Mexico. Informa-
tionisgivenonelevationalrange,vegetationtypeaccordingtoLeopold[29],meanannualtemperature(MAT),meanannualprecipitation(MAP),daysofrain
(DR),anddaysbelow0˚CaccordingtoNationalMeteorologicalServiceofMexico(datafrom1951–2010)[30].
Location Elevation(m) Vegetationtype MAT(˚C) MAP(mm) DR DB
LaMancha 30–50 Tropicalsemi-humiddeciduousforest 26 1221 81 0
Palmarejo 610–670 Tropicalsemi-humiddeciduousforest 23 938 86 0
Chavarrillo 900–1010 TropicalQuercusforest 21 1552 123 0
LosCapulines 1470–1650 Humidmontaneforest 18 1598 145 0
ElZapotal 2020–2230 Humidmontaneforest 14 3004 199 3
ElEncinal 2470–2600 Pinus-Quercusforest 12 1142 100 12
LosPescados 3070–3160 Pinusforest 10 821 113 14
ElConejo 3480–3540 Abiesforest 8 829 112 16
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andtheremainingpartsarehighlyfragmented[27],thereforeitisrecognisedasapriority
regionforconservationinMexico[28].
Weplacedourstudylocationsatthefollowingelevationsabovesealevel:30–50m,610–670
m,900–1010m,1470–1650m,2020–2230m,2470–2600m,3070–3160mand3480–3540m
(Table1,Fig1).Tosimplify,fromnowonwewillrefertoeverysiteasacategoricalunit(50,
650,1000,1500,2100,2500,3100,3500m).WeusedaGarmin1GPSMAP60Cxdeviceto
recordinformationaboutgeographicalreferenceandelevation.
Datacollection
Thesamplingdesign,aswellasfrequentlyusedtermsareshowninFig2.Fieldworkwascon-
ductedbetweenFebruary2012andJanuary2014.Wesampledthepresence/absenceofterres-
trialherbaceousangiosperms,whichwedefinedasplantswithoutapersistentaboveground
woodystemorplantswithonlyslightlywoodystems,rootedontheforestfloorandofshort
stature(generally<1m);vineswereexcluded[31].Werecordedallspeciesin20m×20m
plots,withoutconsideringseedlings[32].Wechooseaplotsizeof400m2becausefortheher-
baceousflorainhumidtropicalforeststhisareaisregardedtoberepresentative,whilesmall
enoughtominimisewithin-plotvariationofabioticfactors[33,34].Welocatedtheplotsinthe
threedifferenthabitatssubjectedtodifferentdegreesofforest-useintensity;old-growth(OG),
degraded(DE),andsecondaryforest(SE)stands(n=5plotsforeachhabitat).Thesecatego-
riesfollowNewboldetal.[35]andaredefinedinTable2.Eachhabitatwaspresentateachof
theeightlocationsresultinginatotalnumberof120plotsandasampledareaof48000m2.
TheSecretar´ıadeMedioAmbienteyRecursosNaturales(SEMARNATSGPA/DGVS/2405/
14)issuedusaplantcollectionpermit(NOM-059-SEMARNAT-2010),whichcoveredthe
wholestudyareaandthecollectionofprotectedspeciesmentionedintheMexicanlegislation.
Weusedelevation(m),meanannualtemperature(˚C),meanannualprecipitation(mm/a)
andhabitat(afactorwiththreelevelsOG,DEandSE),aswellastheirinteractionasexplana-
toryvariables.Weobtainedmeanannualtemperature(MAT)usingdataloggers(HOBOPRO
v2)foroneyear(January-December2014).Weinstalledatotalof42dataloggers,twoinevery
forest-usehabitatatsixelevations(500m,1000m,1500m,2500m,3000m,and3500m)
alongtheentiregradient.Withintheplots,weplaceddataloggersontreesataheightbetween
twoandthreemeters.Weobtainedmeanannualtemperaturedataforthetwoelevations(50
mand2000m)anddataofthemeanannualprecipitation(MAP)fromeightclimatological
stations(neartothesamplingsites)operatingalongtheelevationalgradientduringtheperiod
1951–2010[30].
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Herbdiversityalonggradientsofelevationandforest-useintensity
Fig2.Schematicrepresentationofthesamplingdesign.Wemeasuredα-diversityinplotsof20mx20m
givenasameanoffiveplots.Fiveplotsrepresentonehabitat.Wedefinedhabitatasahomogenoustypeof
forest-useintensitywithinonelocation.Alocationisrepresentativeofanelevationalbeltandharborsthree
differenthabitats(old-growthOG,degradedDE,andsecondarySE).Wemeasuredtwodifferentβ-diversities
basedonpairsofplots.Within-habitatβ-diversityrepresentsthecompositionalheterogeneityofahabitat.Itis
measuredasthe1-Sørensenindexbasedonmultiplepairwisecomparisonsofthefiveplotswithineach
habitatofaspecificlocation.Between-habitβ-diversityrepresentsthecompositionalheterogeneitybetween
differentforest-useintensity.Measurementissimilartowithin-habitatβ-diversity,butmultiplepairwise
comparisonsbasedontheplotsbetweenhabitatsofaspecificlocation.Wedefinedγ-diversityasthetotal
numberofthelocalspeciespoolacrossall15plotswithinalocation,i.e.threehabitatswithfiveplotseach.
https://doi.org/10.1371/journal.pone.0182893.g002
Speciesidentification
Wecollectedateachlocation,butnotineveryplot,specimensofallspeciesifpossibleinqua-
druplicatesanddepositedattheMexicanherbariaCIIDIR,MEXU,XAL,andXALU.Details
aboutspeciesidentifications,geographicaldistributionandclassificationcanbefoundin
Go´mez-D´ıazetal.[36].Thepresence/absencedataofallthespeciesfoundattheplotscanbe
foundattheSupportingInformation(S1File).
Dataanalyses
Wecalculatedforeachofthe120herbcommunitiesinthedataset,i.e.replicatedplots(5plots
perhabitatx8locations=120),α-diversity,theproportionofendemicsandβ-diversity[37].
Alpha-diversityisthecountofthenumberofspecies(plot-basedspeciesrichness)ineach
standardisedreplicateplot[38].Inordertoevaluatethevalueofendemicspecies,wemeasured
theproportionofendemicspeciesperplot.Weusedthedissimilarity(1-S)variantofthe
Table2. Classificationofhabitatswithdifferentforest-useintensitiesaccordingtothemainphysiognomiccharacteristic,thegapfractioninthe
canopy,dominanceofcanopytrees,thepercentageofshrubs,andthepresenceoflianas[35].
Habitat Characteristic Gaps(%) Forest-useintensity Canopytrees Shrub(%) Lianas
Old-growth Noobviousforest-use,dominanceofmaturetrees <10 Low High <30 No
Degraded Selectivelogging,grazingandunderstoryremoval 11–25 Medium Low 30–50 Low
Secondary Regrownafterclear-cut >25 High verylow >50 High
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Herbdiversityalonggradientsofelevationandforest-useintensity
Sørensenindex[37]asameasureofβ-diversityandwecalculateditas:
b(cid:0) diversity¼1(cid:0) S ð1Þ
whereSistheSørensenindex:
2C
S¼ ð2Þ
AþB
whichisacoefficientofassociation,whereavalueof1showsthatapairofplotsunderconsid-
erationhasexactlythesamespecies.TheSørensenindexcanbeadjustedtomeasurespecies
turnover(effectiveorreal)[39].Theindex1-Sisalsoameasureofβ-diversitybecauseifacoef-
ficientisnearto1,itshowsthattheunitsdonotsharespecies,and,therefore,theyhavehigh
β-diversity[40].Asameasureforlandscape-scaleβ-diversity,wecomparedtheeffectofhabi-
tatsonfloristiccompositionbetweenOGandDE,OGandSEaswellasDEandSEateachsite
[41].Wecalculatedplot-by-plot,i.e.eachplotofhabitatAwascomparedtofiveorfour(inthe
caseofwithinβ-diversity)otherplotsofhabitatB.Additionally,wecalculatedthestandard
errorsfortheβ-diversityestimator,lettingastatisticallyrigorouscontrastoftwoorothersimi-
larityindexvalues.Standarderrorswerecalculatedbythebootstrapprocess,whichneeds
resamplingtheobserveddataforpairsofsamplesandre-computingtheestimatorsNtimes
[41].Weperformedtheseanalysesofβ-diversityinEstimateS9.1.0[42].
Weusedasetofgeneralizedlinearmodels(GLM)andinformatictheoreticapproachbased
onthebias-correctedAkaike’sinformationcriterion(AIC )toexaminetheextenttowhich
c
herbα-diversity,theproportionofendemicsandβ-diversityisrelatedtoelevation,habitat,
MATandMAP.Thesesetsofmodelsaimedtodescribethepatternofdistributionofthe
responsevariables,namelyherbα-diversity,theproportionofendemicsandβ-diversity.We
usedelevation,elevation2,habitat,MAT,MAT2,MAP,MAP2andvarioustwo-wayandthree-
wayinteractionsasexplanatoryvariablesinthesemodels.Weincludedpolynomialtermsof
elevation,MATandMAPinordertodetectpotentialhumpshapesintherelationships
betweenelevationandtheinter-correlatedclimaticvariableswiththeresponsevariables.We
didnotincludethedatabelow500minthecaseofβ-diversityduetothelackofspeciesinsix
plotsandweused“habitattransition”withsixlevels(OGtoOG,OGtoDE,OGtoSE,DEto
DE,DEtoSEandSEtoSE)insteadoftheindependentvariable“habitat”.Weconstructed
thirty-oneplausiblemodelscombiningthesevariablesforthissetofmodels[38].
WecheckeddatafornormalityusingtheShapiro-Wilknormalitytest.Wecheckedthe
homogeneityofvarianceusingtheBartletttest.Noneofthevariablesfollowedanormaldistri-
bution.Therefore,wechoseanerrorstructureforeachvariabledependingonthenatureof
thevariable.Wechoosetheerrorstructureaccordingtothe“descdist”functionoftheRpack-
age“fitdistrplus”version1.0–7.Weusedanegativebinomialerrorstructureformodelsofα-
diversity.Weusedabetaerrorstructureformodelsoftheproportionofendemics.Weuseda
log-normalerrorstructureformodelsofβ-diversity.Weusedmaximumlikelihoodestimation
andAIC valuescomparedtochoosethebestmodelforeachresponsevariableineachsetof
c
models.WeperformedallanalysesinR3.2.1[43].Finally,wecalculatedanR2foreachmodel
[38].
Multiplicativediversitypartitioning. Weusedmultiplicativediversitypartitioning[44]
andfocusedonthreedistinctcomponentsofcommunitydifferentiation(α-diversity),(β-
withinhabitat)andcompositionaldissimilarity(β-betweenhabitats)[45,46].Wepartitioned
totalγ-diversityperlocationintomultiplicativecomponentsrepresentingperplotα-diversity,
withinhabitatsβ-diversityandamonghabitatsβ-diversity.Weusedthefunction“multipart”
oftheRpackage“vegan”topartitiondiversity[45,47].Throughthetext,wewillrefertothe
resultsofthisanalysisasrelative(relativeα-diversity,β-withinhabitat,etc.)
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Herbdiversityalonggradientsofelevationandforest-useintensity
Table3. Summariesofgeneralizedlinearmodels. Thesummarieslinkherbα-diversity,theproportionofendemicsandβ-diversitytoenvironmental
explanatoryvariables,alonganelevationalgradientatcentralVeracruz,Mexico.Wereportedthebestmodels,accordingtothebias-correctedAkaikeinfor-
mationcriterion(AICc).WealsogivethechangeinAICcbetweenthebestmodelandthenextbestandworst.Finally,anR2measuringvariationexplainedby
themodelisgiven.
Response Model AIC ΔAIC (next ΔAIC R2
c c c
best) (worst)
α-diversity Elevation+elevation2+habitat+MAT+MAP2+elevation:MAT+elevation:elevation2 570.96 0.1 1023.3 0.69
+MAP:elevation2
theproportionof Elevation+elevation2+habitat+MAT+MAP2+elevation:MAT+elevation:elevation2 -162.50 1.9 111.7 0.41
endemics +elevation:MAT2+elevation:elevation2:MAT
β-diversity Elevation+elevation2+change+MAT+MAP+elevation:change+elevation:MAT 287.41 1.7 450.6 0.49
+elevation2:change+elevation2:MAT+change:MAT+MAT:MAP+elevation:change:
MAT+elevation2:change:MAT
https://doi.org/10.1371/journal.pone.0182893.t003
Estimationofspeciesdiversity(Hillnumbers). FollowingChaoandJost[48],weuseda
diversityprofileestimatorofqD(Hillnumbers).Thediversityestimatoroforderqineachpro-
filerepresentstheasymptoteintherarefactionandextrapolationcurves[49].Wecalculated
theprofileestimatorwiththefunction“diversity”oftheRpackage“SpadeR”[50].Weconsid-
eredthecasesofqfrom0to3withincrementsof0.25.
Resultsanddiscussion
Alphadiversity
Elevation,elevation2,habitat,MAT,MAP2,interactionsbetweenelevationandelevation2,an
interactionbetweenelevationandMAT,aswellasaninteractionbetweenelevation2and
MATmodeledbesttheα-diversity(Table3).Thismodelexplainedalargeamountofthevari-
anceinspeciesrichness(GLMR2=0.69).Alpha-diversityfollowedahump-shapedpattern,
showingapeakat2500manddeclinestowardstheextremesofthegradientthatdonotchange
dependingonthehabitat(Fig3,Table4).FewerspeciesarefoundathighMATandthiseffect
isgreatestatlowelevationsduetotheinclusionoftheMAT+elevationinteraction.
Hump-shapeddiversitypatternshavebeenreportedfordifferentgroupsofvascularplants
[24],suchaspalms,Acanthaceae,Bromeliaceaeandwoodyplantsalongtropicalmountains
[51–53].Comparedtopreviousfindings,ourresultsshowthepeakinα-diversityshifted
towardshigher,insteadofmid-elevations[54].Oneexplanationforthispatternisthatherbs
areadaptedtocoldclimatesandhadasuccessintemperatezonesduetobeannualandthe
productionofundergroundstructures(e.g.rhizomesandstolons)[55].
LowerelevationsinVeracruzaresubjecttoprolongeddryseasons(Table2),whichmay
limitα-diversity.Withincreasingelevation,precipitationincreases,whiletemperaturesand
potentialevapotranspirationdecrease.Speciesrichnessoffernshasbeenreportedtobeposi-
tivelyrelatedtohumidity[56].Inourstudy,angiospermrichnesspeakedbetween2500mand
3100m,whereprecipitationandthenumberofrainydaysalreadydecrease.However,the
Pinus-Quercusforestsat2500mareoftensubjecttofog,whereasinPinusforests(3100m)
lighttransmissiontotheforestfloorishigh[57],whichlikelyincreasesthegroundcoverof
angiospermsandthusalsotheirdiversity.
Surprisingly,forest-useintensityhadnosignificanteffectonα-diversity(Fig3).Thelackof
adetectablenet-changeinα-diversitymightindicatethatthelevelofforest-useintensityisstill
relativelymoderate;however,otherlifeforms(e.g.trees,epiphytesandferns)mightshowcon-
trastingpatterns.Itisquitewelldocumentedthatforestherbsprofitfrombetterlightcondi-
tionsinDEorSE.Newboldetal.[35],forexample,foundthattherichnessofvascularplant
speciescanincreaseby40%duetotheconversionofold-growthforeststosecondary
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Herbdiversityalonggradientsofelevationandforest-useintensity
Fig3.Alpha-diversityofherbaceousangiospermsalonggradientsofelevationandforest-use
intensityattheCofredePerote,centralVeracruz,Mexico.Wefitthelinesfromanegativegeneralized
linearmodel(GLM),theshadedareamarksconfidenceintervals(CI=1.96timesstandarderror).Difference
tozeroissignificantfortheintercept(xy,OGat50m,p<0.001),butitisnotsignificantfortheeffectofhabitat
(DE:p=0.453,SE:p=0.446).Observedspeciesrichnesson20m×20mplotsalongtheelevational
gradientforOG(green),DE(blue),andSE(red).
https://doi.org/10.1371/journal.pone.0182893.g003
vegetation,butmoreseverehabitatconversion,e.g.fromforesttointensivecropland,
decreasesspeciesrichness.
Proportionofendemicspecies
Thebestmodelfortheproportionofendemicspecieswastheonethatincludedelevation,ele-
vation2,habitat,MAT,MAP2andtheinteractionbetweenelevationandMAT,elevationand
elevation2,elevation2andMATandatripleinteractionwithelevation,elevation2andMAT
(Fig4,Table3).Theproportionofendemicspeciesshowedanon-linearpatternalongtheele-
vationalgradientwiththehighestproportionat500m(Fig4,Table4).Thereisnoeffectof
forest-useintensityontheproportionofendemicspecies,thelackofapatternontheendemic
speciescanbeattributedtotheadaptationoftheendemicherbaceousplant’sspeciesofMexico
toseveralpatternsofdisturbanceortheextinctionofpreviousendemicspecies.Thismodelof
theproportionofendemicspecieshadanR2of0.41.
Betaandgammadiversity
Incontrasttorichness,forest-useintensityhadmarkedeffectsonfloristiccomposition,which
wasmostvisiblewhenlookingathabitattransitions(Table5).Within-habitatβ-diversitywas
generallylower(0.42–0.52)thanbetween-habitatβ-diversity(0.58–0.66).Unsurprisingly,we
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Herbdiversityalonggradientsofelevationandforest-useintensity
Table4. Parameterestimatesfromgeneralizedlinearmodels. Theparameterslinkherbα-diversity,theproportionofendemicsandβ-diversitytoenvi-
ronmentalexplanatoryvariables,alonganelevationalgradientatcentralVeracruz,Mexico.Estimatesareonthestandardizedscale±standarderror.We
markedsignificantestimateswithanasterisk(*<=0.05,**<=0.01and***<0.001).Emptycellsindicatetermsnotincludedinthebestmodelforagiven
responsevariable.
Estimates
Term α-diversity theproportionofendemics β-diversity
Elevation -5.66±0.04*** 7.22±1.25 -2.89±0.38***
Elevation2 7.09±0.28** -5.74±1.72 1.98±0.24***
Habitat.DE 0.01±7.78E-2 0.08±0.02 0.05±3.72E-3
Habitat.SE 16.76±0.85 0.27±0.02 -7.23±0.28*
MAT -1.23±0.02*** -0.84±1.25 -2.47±0.28***
MAP 29.06±6.68
MAP2 -0.04±1.77E-03*** 0.70±0.22***
Elevation:MAT 9.23E-4±2.24E-5** 5.26±3.60 0.26±0.03***
Elevation:Habitat.DE 0.35±0.01
Elevation:Habitat.SE 0.57±0.07
Elevation:elevation2 -7.96E-4±6.49E-5* -0.37±0.06
Elevation2:Habitat.DE -53.4±6.65*
Elevation2:Habitat.SE 5.42E-6±8.04E-7
Elevation2:MAT -0.07±6.49E-3 -8.41±4.13*** 0.03±6.67E-3***
Habitat.DE:MAT -71.2±7.82
Habitat.SE:MAT 28.46±4.17*
MAT:MAP 34.74±1.94***
Elevation:elevation2:MAT 2.10±0.89**
Elevation:Habitat.DE:MAT -0.05±1.94E-3*
Elevation:Habitat.SE:MAT 10.24±2.29*
Elevation2:Habitat.DE:MAT 1.23E-5±1.94E-6
Elevation2:Habitat.SE:MAT -3.70E-3±2.33E-4*
https://doi.org/10.1371/journal.pone.0182893.t004
foundthehighestdissimilarityinthetransitionfromOGtoSE,whereasthemosthomogenous
speciespoolwaswithinOG.Thehighβ-diversitybetweenhabitatsindicatedwiderenviron-
mentaldifferences[58]thantheheterogeneityofplotswithinthesamehabitattype.
Thebestmodelforβ-diversityincludedthemaineffectsofelevation,elevation2,change,
MAT,MAPandinteractionsbetweenelevationandchange,elevationandMAT,elevation2
andchange,elevation2andMAT,changeandMAT,MATandMAP,aswellastripleinterac-
tionsamongelevation,change,MATandelevation2,change,MAT(Table3).Thismodel
explainslittlevariation(R2=0.49).Therewasamarkedeffectofelevationonβ-diversity(Fig
5,Table4).Within-habitatβ-diversityshowedaclearhumped-shapedpatternforOGandSE
withpeaksbetween2500mand3000m.DE,however,hadtheirhighestβ-diversityat650m
withasubsequentdecline.Obviously,DEatlowerelevationsexhibitsadifferentresponseto
environmentalconditionscomparedtoOGandSE.Degradationmayleadtoahigherhetero-
geneityofenvironmentalconditionsand,consequently,offerdiversenichestriggeringcom-
munitydifferentiation[59].Beta-diversitybetween-habitatswasgenerallyhighbutvariedwith
thetypeofhabitattransition.InthetransitionfromOGtoSE,therewasaturnoverofc.50%
ofthespeciesatbothextremesoftheelevationalgradient.Between1500mand2500m,how-
ever,75%ofthespeciesweredifferentwhencomparingOGtoSE.Habitattransitionsrelated
todegradation(OG-DE,DE-SE)showedhighestβ-diversityat650mand2500manddeclined
withincreasingelevation.Endemicspeciescontributetothispatternonlyat650mwherewe
foundtheirpeak(Fig4).Especiallyat3100mand3500m,thechangeinspeciescomposition
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Herbdiversityalonggradientsofelevationandforest-useintensity
Fig4.Theproportionofendemicspeciesofherbaceousangiospermsalonggradientsofelevation
andforest-useintensityattheCofredePerote,centralVeracruz,Mexico.WefitthelinesfromaGLM
withabetaerrorfamily,theshadedareamarksconfidenceintervals(CI=1.96timesstandarderror).
Differencetozeroisnotsignificantfortheintercept(xy,OGat50m,p=0.066)aswellasfortheeffectof
habitat(DE:p=0.771,SE:p=0.226).Observedproportionofendemicspecieson20m×20mplotsalong
theelevationalgradientforOG(green),DE(blue),andSE(red).
https://doi.org/10.1371/journal.pone.0182893.g004
withthetransitionfromOGtoDEwasrelativelylow.Thisindicatesthatpresentenvironmen-
talconditionsfavouraspectrumofadaptedspecies[60],whichthriveregardlessofthehabitat
type.Above3100mtherearefewerspecies,whichareadaptedtoextremeclimateevents,such
asdaysbelow0˚C,lowertemperatureandprecipitation(Table1).
Werevealedtherelativecontributionofrelativeα,relativewithin-habitatβ,andrelative
between-habitatsβ-diversitytoγusingthemultiplicativepartitioningapproach(Fig6).The
contributionofrelativeα-diversitywasonlybetween3and13(Fig6).Diverseforesthabitats
supporthighspeciesdiversityandleadtohighrelativeβ-diversitybetween-habitats(β )
b
Table5. Averageeffectsofthehabitatchange. Meanβ-diversityateveryhabitattransition,lettersin
superscriptdifferencesingroupsafterTukeyposthoctest(HSD=0.138).
Habitattransition β-diversity(1-S)
Old-growthtosecondary 0.66a
Degradedtosecondary 0.61ab
Old-growthtodegraded 0.58ab
Degradedtodegraded 0.52bc
Secondarytosecondary 0.48bc
Old-growthtoold-growth 0.42c
https://doi.org/10.1371/journal.pone.0182893.t005
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