Elevation Regimes Modulated the Responses of Canopy Structure of Coastal Mangrove Forests by Puerto Rico Sea Grant

remote sensing

Article

ElevationRegimesModulatedtheResponsesofCanopy StructureofCoastalMangroveForeststoHurricaneDamage

QiongGaoandMeiYu*

Citation: Gao,Q.;Yu,M.Elevation RegimesModulatedtheResponsesof CanopyStructureofCoastal MangroveForeststoHurricane Damage. RemoteSens. 2022, 14,1497. https://doi.org/10.3390/rs14061497

AcademicEditor:ChandraGiri

Received:9February2022

Accepted:18March2022

Published:20March2022

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Copyright: ©2022bytheauthors. LicenseeMDPI,Basel,Switzerland. Thisarticleisanopenaccessarticle distributedunderthetermsand conditionsoftheCreativeCommons Attribution(CCBY)license(https:// creativecommons.org/licenses/by/ 4.0/).

DepartmentofEnvironmentalSciences,UniversityofPuertoRico,RioPiedras,SanJuan,PR00926,USA; q.gao@ites.upr.edu

* Correspondence:meiyu@ites.upr.edu

Abstract: Mangroveforestshaveuniqueecosystemfunctionsandservices,yetthecoastalmangroves intropicsareoftendisturbedbytropicalcyclones.HurricaneMariasweptPuertoRicoandnearby CaribbeanislandsinSeptember2017andcausedtremendousdamagetothecoastalmangrove systems.Understandingthevulnerabilityandresistanceofmangroveforeststodisturbancesis pivotalforfuturerestorationandconservation.Inthisstudy,weusedLiDARpointcloudstoderive thecanopyheightofﬁvemajormangroveforests,includingtruemangrovesandmangroveassociates, alongthecoastofPuertoRicobeforeandafterthehurricanes,whichallowedustodetectthe spatialvariationsofcanopyheightreduction.Wethenspatiallyregressedthepre-hurricanecanopy heightandthecanopyheightreductiononbiophysicalfactorssuchastheelevation,thedistance torivers/canalswithinandnearby,thedistancetocoast,treedensity,andcanopyunevenness. Theanalysesresultedinthefollowingﬁndings.Thepre-hurricanecanopyheightincreasedwith elevationwhenelevationwaslowandmoderatebutdecreasedwithelevationwhenelevationwas high.Thecanopyheightreductionincreasedquadraticallywiththepre-hurricanecanopyheight,but decreasedwithelevationforthefoursitesdominatedbytruemangroves.ThesiteofPalmadelMar dominatedby Pterocarpus,amangroveassociate,experiencedthestrongestwind,andthecanopy heightreductionincreasedwithelevation.Thecanopyheightreductiondecreasedwiththedistance torivers/canalsonlyforsiteswithlowtomoderatemeanelevationof0.36–0.39m.Inadditiontothe hurricanewinds,therainfallduringhurricanesisanimportantfactorcausingcanopydamageby inundatingtheaerialroots.Insummary,thepre-hurricanecanopystructures,physicalenvironment, andexternalforcesbroughtbyhurricanesinterplayedtoaffectthevulnerabilityofcoastalmangroves tomajorhurricanes.

Keywords: urbanmangroves;LiDAR;canopystructure;hurricanedamage;Caribbean

1.Introduction

Growingundermultiplephysiologicalstresses,coastalmangrovespossessunique ecosystemfunctionstomaintainhighcarbonsequestration[1,2],topurifycoastalwater, tohostanumberofvertebrateandinvertebratespecies[3],tooffsetthesealevelrisevia verticalaccretion[4,5],andtoprotectsocietalpropertiesofcoastalcommunitiesduring tropicalstorms[6].However,thecanopiesofcoastalmangrovesarelikelytobeseverely damagedbytropicalstorms,thusgreatlyreducingthefunctionsofmangroveforests[7–9]. Understandingthevulnerabilityandresistanceofmangrovesunderstormdisturbanceis vitaltorestoreandtoconservecoastalwetlands.

Inadditiontothegreatwindspeedofstorms,severalbiophysicalfeaturesmay elucidatethevulnerabilityoftropicalforeststodisturbance;emergenttreesorhigher canopy,smallertreediameter,lowertreedensity,andlowersoil-rootanchoragemayincur morecanopydamage[10,11].Mangroveswithhighercanopytendtointerceptmorewind force,treeswithsmallerdimeterhaveasmallshearmodulus,alowertreedensitymakes thewindeasiertotraversethecanopy,andalowersoil-rootanchoragemakesthecoastal

foresteasiertofallorslantunderstormwind[11].Inaddition,stormsoftenbringagreat amountofrainfallandseawatersurge[12],whichmayﬂoodcoastalmangrovesand immersetheiraerialroots,andtheprolongedimmersionmayleadtodelayeddeathof mangrovetrees[13].

Canopyheight,stemdensity,andtreediameterarelikelytobeshapedbythephysical environment,aswellastropicalstorms[14].Formangrovesinthetropics,salinityisa majorlimitingfactorinmostcircumstances[15–17].Althoughmangroverootscanexclude andleavescanexcretevariableamountsofsalts,thecanopyheightwasfoundtodecrease withsoilsalinity,whichisaresultofinterplaybetweensaltbroughtbytheseatidesor groundwaterandthehydrologicalprocesses[18,19].Amplerainfall,overlandﬂow,and riverdischargemaycarrysaltawayordilutethesaltconcentrationinsoil,whereastides bringthesalttomangroveforest,andevapotranspirationremovesmostlypurewaterand letssaltaccumulatewithinthesoil.Hence,thesoilsalinitydependsonboththeclimate regionandthefrequencyoftides[20].Inadditiontosalinity,mangrovegrowthmayalso bethreatenedbydeﬁciencyofnutrients,whichdependsnotonlyontheparentmaterials andmineralization,butalsoonexternalsourcessuchasurbanprocesses.

Theimpactofhumanactivitiesmayalsoaffectthemangrovegrowthandthevulnerabilityduringtropicalstorms.Mostoftheworldpopulationlivesnearcoastsand oftencompeteforhabitatwithmangroves.Mangroveforestsandneighborhoodurban areasmaybeconnectedviaaerodynamicsandhydrology,andtheconnectionsviasewage canals/pipesprovidefreshwaterandnutrientstomangroveforests,thusaffectingtheir growth[21].Thisisespeciallyimportantforcoastalmangroveforestsinheavilypopulated islands,wheremangrovesareinclosedistancetourbancommunitiesandwerehistorically drainedforagricultureandurbandevelopment[22].

Theeffectsofsalinityandnutrientsonmangrovegrowthdependonthespeciessalt toleranceandnutrientbudget[15,23].Threemajorspeciesoftruemangroves[24]are foundonCaribbeanislands:redmangrove(Rhizophoramangle)withstiltrootsgrowing inthecoastalwater,blackmangrove(Avicenniagerminans)oftenfoundinshallowwater ormuddysoilwithpneumatophoresgrowingfromhorizontalcableroots,andwhite mangrove(Lagunculariaracemosa)growinginslightlydrierconditionsthanblackmangrove. Redandblackmangroveshaveahightolerancetosalt,whereaswhitemangroveshave moderatetolerance[15].Inadditiontotheabovetruemangrovespecies,therearemangrove associateswhichwereonceclassiﬁedasmangrovesinhistory[25].Buttonwoodmangrove (Conocarpuserectus)isoccasionallyfoundinrelativelydryspots,and Pterocarpusofﬁcinalis as ahardwoodisalsofoundinbrackishwater.Thesespecieshaverelativelylowertolerance tosalinityandoftengrowtogetherwithtruemangroves.Therefore,whenwemention mangroveforests,weimplybothtruemangrovesandmangroveassociates.

Theimpactoftropicalstormsoncoastalmangrovescanbeassessedbygroundinventory,aswellasremotesensing[26,27].Groundinventoryisoftenlimitedbyscales[28]. Remotesensing,usingaerialphotosandsatellite-basedmultispectralimagesas2Dtools, isoftenlimitedtotheassessmentofgreennessandfallsshortintheassessmentofthe verticaldimension[7,29–31].AirborneLiDAR(lightdetectionandranging)providesan idealtooltomeasurethe3Dchangesinthemangrovecanopyatlandscapescales.A LiDARinstrumentonboardanaircraftemitsnear-infraredlaserbeamswhichhittheleaves, branches,trunks,andground,resultinginmultiplereturnsofthelaserbeams[32].The heightofthereturnsisrecordedbytheLiDARinstrumentsasameasurementofthetop andinternalcanopystructure.

TwomajorhurricanesinSeptember2017impactedtheCaribbeanregion,especially theislandofPuertoRico[7,33].HurricaneIrmapassedbyon6SeptemberasaCategory5, whileHurricaneMariatraversedPuertoRicoon20Septemberasahigh-endCategory4, whichresultedintremendousdamagetothecoastalmangroveecosystems.Treeswere defoliatedandstemswererupturedorslanted(photosinAppendix A),thuslargely reducingthecanopyheight.LiDAR-basedassessmentofthehurricanesdamageoncoastal mangrovesisvitaltounderstandtheirvulnerabilityatlandscapescales.Theapplication

ofLiDARdatatothelargestbasinmangrovesinPuertoRicoshowedthatelevation,tree density,anddistancetofreshwaterorsewagecanalsareimportanttoexplainthespatial variationsofthepre-hurricanecanopyheight,aswellasthecanopyheightreductionby thehurricanes[34].However,itisunknownwhethertheseﬁndingscanbegeneralizedto themangrovesofvarioustypeswithdiverseenvironmentalsettings.

Theobjectiveofthisstudywastoexplorethespatialvariationofthepre-hurricane canopystructureofmultiplemangroveforestsalongthePuertoRicocoast,aswellasthe damagetothecanopyduetothemajorhurricanesin2017.Wehypothesizedthatthe pre-hurricanecanopyheightofcoastalmangroveforestsisafunctionofthetopography, thedistancetotherivers/canalswithinandnearby,andthedistancetothecoast,asthese variablesmaymodifythehydrology,salinity,andnutrientsupply.Wealsohypothesized thatthecanopyheightreductionbyhurricanesisalsoafunctionoftheabovefactors,but moreimportantlydeterminedbythepre-hurricanecanopystructure.

2.MaterialsandMethods

2.1.SiteDescription

PuertoRicoliestotheeastendoftheGreatAntillesislands(Figure 1,upperpanel) withacentrallatitudeof18.22◦N.RainfallinPuertoRicovariesgreatlyfrom~1000mmin thesouthwestto~4000mmintheeastmountainpeak,whichshieldstherainfallbrought bytheeasterlytradewinds.Ingeneral,thenorthernandeasterncoastsreceivemore rainfallthanthesouthernandwesterncoasts.Amplerainfallonthenorthcoasttends toproducemorestreamdischargeandoverlandﬂowthanthesouthcoast,whichdilute thesalinity.Thedifferencebetweenthenorthernandsoutherncoastsalsoarisesfrom bathymetry.ThenortherncoastisboundedbytheAtlanticOceanwiththedeepesttrench, whereasthesoutherncoastfacesthemuchshallowerCaribbeanSea.Thus,thetidalenergy onthenortherncoastishigherthanthatonthesoutherncoast.Theconsequenceisthatthe northerncoasthasdevelopedmoreandlargeﬂuvialplainsandsandybeachesthanthe southerncoast.Basinandriverinemangroveforestsaremostlyfoundonthenortherncoast, whereasfringeandover-washedmangroveforestsareusuallyfoundonthesoutherncoast. Historically,PuertoRicooncehadabout11,000haofmangrovesin1800s,whichdeclined toabout6000hain1960sduetotheexpansionofagricultureandurbandevelopment[22]. Theconservationofwetlandsguidedbyinternationalandnationallawsledtotherecovery toabout8000hainlarge,aggregatedpatches[5,22,35,36].PuertoRicohasallthreetrue mangrovespecies,aswellasthemangroveassociates,foundintheCaribbean.

Thisstudyanalyzedﬁvemangroveforests,includingtruemangrovesandmangrove associates,alongthePuertoRicocoast,fourofwhichwereintheeastandnortheast,along withonesiteinthesouthwest(Figure 1,thelowerpanel).Thesesiteswereselectedmostly onthebasisofdataavailability.Thefoursitesintheeastandnortheast(PalmadelMar, Fajardo,CañoMartínPeña,andToaBaja)werealsoclosertothepathofHurricaneMaria thanLaParguerainthesouthwest.TheforestinPalmadelMarisdominatedby Pterocarpus ofﬁcinalis,amangroveassociate,whereastheotherfouraredominatedbytruemangroves.

2.2.DataSource

Toinvestigatethespatialpatternsofthemangrovecanopyandtoassessthehurricanes damage,weusedairborneLiDARdataprovidedbytwocampaignsbeforeandafterthe hurricanes.InMarch2017,thecampaignofGoddard’sLiDAR,Hyperspectral,andThermal Imager(G-LiHT)[37]bytheNationalAeronauticsandSpaceAdministration(NASA) coveredanumberoftransectstripsinPuertoRico.AfterthehurricanesinSeptember 2017,USGSLiDARcampaignsin2018(https://nationalmap.gov/3DEP/,accessedon 15March2022)coveredmostoftheisland.Bothcampaignsprovideddataintheform ofpointclouds.Hence,theboundariesoftheﬁvesiteswerederivedonthebasisofthe intersectionsofcoverageofG-LiHTandUSGSLiDARandtheforestedwetlanddelineated bytheNOAA2010C-CAP(CoastalChangeAnalysisProgram)land-covermap,andthen wereshrunkforsimplicity[38].TheLiDARdataoftheG-LiHTtransects(Table 1)were

usedtoderivethecanopyheightbeforethehurricanes,whichwehereafterrefertoas the‘pre-hurricanecanopyheight’,whiletheUSGSdatawereusedtoderivethecanopy heightafterthehurricanes(Table 1),whichwehereafterrefertoasthe‘post-hurricane canopyheight’.ForG-LiHTdata,thenormalpointspacingofthepointcloudis0.24m withhorizontalandverticalaccuraciesof1m(https://glihtdata.gsfc.nasa.gov/,accessed on15March2022),whereasthenormalpointspacing,verticalaccuracy,andhorizontal accuracyofUSGSLiDARpointcloudare0.34,0.1,and1m,respectively.

Figure1. PuertoRicogeographicallocation(up)andlocationofﬁvesitesalongitscoast(low).Red andbluelinesdepictthepathsofHurricaneMariaandHurricaneIrma,respectively.

Table1. Pre-andpost-hurricaneLiDARpoint-cloudimagesprovidedbytheNASAG-LiHTandthe USGS3DElevationProgram.

SitePre-HurricaneGLiHTTransectsPost-HurricaneUSGSTiles

CañoMartínPeñaPR_10March2017_118

E_2018_19QHA37506600, E_2018_19QHA39006600 FajardoPR_15March2017_75

PalmadelMar

PR_12March2017_58a, PR_12March2017_58b

H_2018_20QKF81005700, H_2018_20QKF81005850

H_2018_20QKF66002850, H_2018_20QKF67502700, H_2018_20QKF67502850

LaPargueraPR_8March2017_114A_2018_19QFV28001200

ToaBaja

PR_10March2017_117, PR_17March2017_199

G_2018_19QGA22506750, G_2018_19QGA22506900, G_2018_19QGA24006900, G_2018_19QGA25506900

EachG-LiHTtransectconsistsofafewtiles,andeachtileisapproximately80mby 500m;onlythosetileswithinthesiteswereanalyzed.TheUSGSLiDARtilesforthe post-hurricaneanalysesarealsolistedinTable 1.InadditiontotheLiDARpointclouds, weusedthedigitalelevationmodel(DEM)of1mresolutionprovidedbytheUSGS3D

ElevationProgram(https://www.usgs.gov/3d-elevation-program,accessedon15March 2022),whichhasaverticalaccuracyof10cm(RMSEz,RootMeanSquareErrorinz).

2.3.AnalysisofPre-HurricaneCanopyHeightandCanopyHeightReductionbytheHurricanes Mangroveforestcanopieswerederivedasfollows:WeﬁrstclippedtheLiDARtiles accordingtotheboundaryofeachsite.Thecanopyheightbeforeandafterthehurricanes werederivedat1mresolutionfromtheG-LiHTandUSGSpointclouds,respectively,using thegrid_canopy()andnormalize_height()functionsprovidedbythe‘lidR’packageversion 3.1.3[39].Tohelpexplainthecanopyheightreduction,wealsotriedtodetecttreesand treeheightsusingtheﬁnd_trees()functionusinglocalmaximumalgorithm.Thisalgorithm maynotbeabletoidentifysmalltreeswithcrownsoverlappingwiththeadjacenttrees. However,theparameterssetinapreviousstudyallowedustoverifythedensityderived againstagroundsurveyfortreeswithstemdiametergreaterthan10cm[34].Wenamedthe treedensityderivedusingthismethodas‘algorithm-derivedtreedensity’.Thereduction incanopyheightbyhurricaneswasfurthercomputedasthepre-hurricanecanopyheight minusthepost-hurricanecanopyheight.

Consideringthesalinityandnutrientavailabilitywhichareaffectedbytherivers,the freshwaterorsewagecanalswithinornearby,aswellasthecoastalwater,wecalculated thedistancetotherivers/canalsandthedistancetothecoastat1mresolution.Average gustwindspeedandhurricanerainfallforeachsitewereestimatedonthebasisofground measurementsandkriginginterpolations[31,40].

Totestourhypothesesandtoexplainthespatialvariationinpre-hurricanecanopy height,aswellasthecanopyheightreductionbythehurricanes,weappliedspatialregressiontomodeltheresponseofpre-hurricanecanopyheightandcanopyheightreduction totheabovementionedcovariatesforeachsite.Thespatialerrormodeltookthefollowingform:

y = xβ + u, u = λWu + ,(1) where y isthedependentvariablerepresentedasan n × 1matrix(n,numberofrecords inthedataset), x isoneormultiple(m)independentvariables(covariates)representedby an n × (m +1)matrix, β isan(m +1) × 1coefﬁcientmatrixtobeestimated,and u isan n × 1 spatialerrormatrix. W isan n × n weightmatrixdeterminedbytheneighborhood structure, λ isthespatialautocorrelationcoefﬁcient,and ε isthenormali.i.d.(independent andidenticallydistributed)residual.

Toapplythespatialerrormodel,allthespatialvariableswereaggregatedinto20m gridstoobtainthemeanquantities.Inaddition,wecomputedthestandarddeviationofthe pre-hurricanecanopyheightforthe20mgridtoreﬂecttheunevennessofthepre-hurricane canopyheight.Thevariablesat20mresolutionwerenormalizedintherangeof0to1,so thatwecouldcomparethecoefﬁcientsestimatedbytheregressions.

Toexplorethespatialresponsesofthemangrovesacrosssites,wealsopooledthedata ofallsitesforthesamesetofspatialregression.Thiswasdonebysampling150gridcells of20m × 20mfromeachsiteinthreestratadeﬁnedas0–33,33–67,and67–100percentiles ofthepre-hurricanecanopyheight.Thespatialregressionswerethenconductedforthe pooleddatasets.

Thecovariatesincludedintheregressionofthepre-hurricanecanopyheightwerethe elevation,thedistancetowithinornearbyrivers/canals,thedistancetocoastalsaltwater, andthealgorithm-derivedtreedensity.Theadditionalcovariatesfortheregressionofthe canopyheightreductionbythehurricaneswerethepre-hurricanecanopyheightandthe canopyroughness.Thepooledregressionalsoincorporatedthemeangustwindspeed andtotalrainfallduringthehurricanetoexplainthedifferenceacrosssites.Allthedata analysesandmappingweredonewithR[41]andArcGISPro(ESRI,Redlands,CA,USA).

3.Results

3.1.SpatialVariationandSummaryStatisticsoftheCanopyHeightsbeforeandafter theHurricanes

Elevationwasfoundtobethemostimportantenvironmentalvariableexplainingthe pre-hurricanecanopyheight,aswellasthecanopyheightreductionbythehurricanes[34]. Theelevationproﬁlesoftheﬁveforests(Figure 2,Table 2)showedgreatvariationsacross thesites.TheFajardositehadthehighestelevationwithamean ± SDof1.61 ± 1.07m, followedbyPalmaDelMarwith1.03 ± 0.38m.LaParguera(fringemangroves)inthe southwesthadthelowestelevationwithamean ± SDof0.16 ± 0.07m.CañoMartínPeña andToaBajahadmoderateelevationswithmeans ± SDof0.36 ± 0.32and0.39 ± 0.31m, respectively.

Figure2. DEMoftheﬁvemangroveforests.Blueandlight-greenlinesdepictriversandcanalsof freshwater/sewage,respectively.

Table2. Summaryofthecanopyheightsbefore(CHM_2017)andafterthehurricanes(CHM_2018), canopyheightreduction,algorithm-derivedtreedensity,andthecovariatesofDEM,distanceto rivers/canalsandtocoast,andhurricanerainfallandgustwindbasedonthe20mgridmaps.

Thepre-hurricanecanopyheight(CHM_2017,Figure 3)showsthattherewerewide variationsinmangrovecanopyheightwithinandbetweensites(Table 2).Themeancanopy heightofCañoMartínPeña,PalmadelMar,andToaBajawereintherangeof9.3–11.7m, higherthanthatinFajardoandLaParguera(6.7and6.2m,respectively).Comparedto thepre-hurricanecanopyheight,themeanpost-hurricanecanopyheight(CHM_2018)was moreevenbothwithinandacrossthesites(Figures 3 and 4).Themeanheightvariedfrom 4.2minPalmadelMarto6.1minCañoMartínPeña.Wefoundapatternthatahigher pre-hurricanecanopyledtoagreaterreductionbythehurricanes(Figure 5).ToaBajawith thehighestmeanpre-hurricanecanopyshowedthegreatestreductionof6.1m,whereasLa Parguerawiththelowestpre-hurricanecanopyexperiencedthesmallestreductionof0.5m (Table 2).Themeanalgorithm-derivedpre-hurricanetreedensityreachedthegreatestlevel inCañoMartínPeñaandToaBaja(2135ha 1 and2132ha 1,respectively),butwaslower inLaPargueraandPalmadelMar(1674ha 1 and1682ha 1,respectively).

Figure3. Thepre-hurricanecanopyheight,derivedfromtheG-LiHTpoint-clouddata.

TheforestsinPalmadelMarandFajardoaretheclosesttorivers/canalswithmean distanceof57.8 ± 55.3and83.8 ± 60.8m(Table 2),respectively,whereastheforestin LaPargueradoesnothaveanyriversorcanalsnearbyandthenearestrivers/canalsare 948.1 ± 157.9m away.TheforestnearCañoMartínPeñahastheclosestmeandistanceto coastalwater(101.2m)becausewetreatedthewaterintheChannelofMartínPeñaassalty. The Pterocarpus forestinPalmadelMargrowsinwardtothelandandisconnectedtothe coastbychannelsandariver,suchthattheforesthasthefarthestmeandistancetothe coast(710.3m).Thegreatmeandistanceof516.9mtothecoastandthemediumdistance of341.5mtotheriver/canalsoftheToaBajaForestarelargelybecauseofitslargeareaof 71.1ha.

Windspeedandrainfallinterpolatedfromthegroundobservationsduringthehurricane[31,40]showedthatthemeangustwindspeedwasthehighestatPalmadelMar (49.5m s 1,Table 2),thesiteclosesttothelandfallofHurricaneMaria,whereasLaParguera inthesouthwestfarthestfromthehurricanepathhadthelowestmeangustwindspeed (34.1m s 1).Theotherthreesitesinbetweenalsohadgustspeedsofmorethan44m s 1 . Thehurricane-broughtrainfallshowedmorevariationacrosssitesthangustwindspeed.

ToaBajaandCañoMartínPeñaexperiencedthehighestrainfallof497.2and427.8mm, respectively,whereastheforestatLaParguerareceivedonly91.1mm.PalmadelMar,even closertothelandfallofMaria,onlyreceived286.5mmrainfall.

Figure4. Thepost-hurricanecanopyheight,derivedfromtheUSGSLiDARpointclouds.

Figure5. Canopyheightreductioncalculatedasthepre-hurricanecanopyheightminustheposthurricanecanopyheight.

3.2.SpatialRegressionModelsofthePre-HurricaneCanopyHeightandtheCanopyHeight ReductionbytheHurricanes

Thespatialregressionofthepre-hurricanecanopyheightyieldedequationswith signiﬁcantcoefﬁcientslistedinTable 3.Forexample,theequationforPalmadelMarwas

,(2)

where h isthenormalizedpre-hurricanecanopyheight, z isthenormalizedelevation, and d isthenormalizedalgorithm-derivedtreedensity.ForsymbolsinTable 3, sc isthe normalizeddistancetocoast,and λ isthespatialautocorrelationcoefficient.Thespatial errormodelforPalmadelMarhada λ of0.90and r2 of0.68.Exceptfortheforestin Fajardo,thepre-hurricanecanopyheightdependedsignificantlyontheelevation,butthis dependencedifferedacrosssites(Table 3).ForLaParguera,thepre-hurricanecanopy heightincreasedlinearlywithelevation.Similarly,thepre-hurricanecanopyheightofthe forestsinCañoMartínPeñaandToaBajaincreasedwithelevationwhenelevationwaslow, butthendecreasedwithelevationwhenelevationwashigherastheabsolutevalueofthe z2 coefficientwasgreaterthanthatof z.Thepre-hurricanecanopyheightofthesethree sitesalsosignificantlydecreasedwiththedistancetothecoast.Thepre-hurricanecanopy heightinPalmadelMardecreasedquadraticallywithelevation.

Table3. Spatialregressionofnormalizedpre-hurricanecanopyheight(h)onnormalizedcovariates. z,theelevation; d,thenormalizedalgorithm-derivedtreedensity; sc, thedistancetothecoast; λ,the spatialautocorrelationcoefficient; r2,thecoefficientofdetermination.Allcoefficientsweresignificant at α =0.05.

Thedependenceofthepre-hurricanecanopyheightonthealgorithm-derivedtree densitydifferedacrosssites;threesites(LaParguera,PalmadelMar,andFajardo)had pre-hurricanecanopyheightdecreaseswithdensity,whereasthepre-hurricanecanopy heightincreasedwithdensityinToaBaja.Thedensitywasnotasigniﬁcantexplanatorof thepre-hurricanecanopyheightinCañoMartínPeña.

TheequationsofthespatialerrormodelforthecanopyheightreductionwithsigniﬁcantcoefﬁcientsareshowninTable 4 andcouldbeexpressedasfollowsfortheToa Bajasite:

where ∆h isthenormalizedcanopyheightreduction, sh isthenormalizedstandarddeviationofpre-hurricanecanopyheightwithinthe20mgrid,and s isthedistanceto rivers/canals.

Thecanopyheightreductionofallsitesincreasedlinearlyorquadraticallywiththe pre-hurricanecanopyheight(Table 4).ThereductionatallsitesexceptPalmadelMar decreasedquadraticallywiththeelevation.ForPalmadelMar,thecanopyheightreduction increasedwithelevationwherethe Pterocarpus forestoccupiedahigherelevationcompared toothersites.ThecanopyheightreductioninPalmadelMarandFajardowassigniﬁcantly cutbackbythehightreedensity,whilethatinToaBajawassigniﬁcantlypromotedbythe unevennessofthepre-hurricanecanopyheight(sh).ThecanopyheightreductionatToa BajaandCañoMartínPeñawasloweredbythedistancetotherivers/canalssuchthata fartherdistancefromrivers/canalsledtolesscanopyheightreduction.Thecanopyheight reductionatCañoMartínPeñawasalsocutbackbythedistancetothecoastwater.

Table4. Spatialregressionofnormalizedcanopyheightreduction(∆h)onnormalizedcovariates: h,pre-hurricanecanopyheight; z,elevation; d,algorithm-derivedtreedensity; sh,standarddeviationofpre-hurricanecanopyheight; s,distancetorivers/canals; sc,distancetocoast; λ,spatial autocorrelationcoefficient; r2,coefficientofdetermination.Allcoefficientsweresignificantat α =0.05.

Poolingthedataofallsites,wefoundthatthepooledpre-hurricanecanopyheight hadthefollowingequation:

Hence,thepooledcanopyheightdecreasedquadraticallywiththeelevationand linearlywiththealgorithm-derivedtreedensityandthedistancetorivers/canals.The regressionhada λ of0.48and r2 of0.54.ThemodelﬁttothedataisshowninFigure 6a.

Figure6. (a)Model-predictedversusLiDAR-derivedpre-hurricanecanopyheight,and(b)modelpredictedversusLiDAR-derivedcanopyheightreduction.Codesfortheﬁvesites:CM—CañoMartín Peña,FJ—Fajardo,PG—LaParguera,PM—PalmadelMar,TB—ToaBaja.

Theregressionofthepooledcanopyheightreductionresultedin

where p isthenormalizedrainfall,and w isthenormalizedgustwindspeed.Theregression hada λ as0.51and r2 as0.85.Hence,theprevailingpatternacrosstheﬁvesitesisthatthe canopyheightreductionincreasedwiththepre-hurricanecanopyheightbutdecreased withelevation.Largerainfallandgustspeedincurredmorecanopyheightreduction; however,theimpactofthewindspeedwasgreaterthanthatofrainfallasindicatedbythe biggercoefﬁcientbeforewindspeed.ThemodelpredictionversusLiDAR-derivedcanopy heightreductionisdepictedinFigure 6b.

4.Discussion

4.1.CanopyHeightbeforeHurricanes

Ouranalysessupportedourhypothesisthatthecanopyheightreductionsigniﬁcantly dependsonthepre-hurricanecanopyheight,asahighercanopybeforehurricanesmeans moreinterceptionofthewindforcetodamagethecanopy[42,43].Theeffectofprehurricanecanopyheighthasbeenidentiﬁedastheprimaryparameterinseveralmodels thatsimulatetheriskofwinddamagetoforeststands.

Thedependenceofthecanopyheightreductiononthepre-hurricanecanopyheight wasquadratic,ratherthanlinear,whichimpliesthattheslopedecreasedastheprehurricanecanopyheightincreased.Moreover,thepre-hurricanecanopyheightwasthe mostimportantfactordeterminingthehurricanedamagetomangroveforestasthecoefﬁcientsofthenormalizedcanopyheightintheequations(Table 4,Equation(5))werelargest comparedtootherfactors.

4.2.Elevation

Ouranalysesbothatasitelevelandacrosssitesusingpooleddatasupportedourhypothesisthatboththepre-hurricanemangrovecanopyheightandthecanopyheightreductionbythehurricanesdependonelevation,butonlypartlyonthedistancetorivers/canals andthedistancetocoast.Theresponsesofcanopyheightandthecanopyheightreduction toelevationanddistancetorivers/canalsandcoastwaterdependedheavilyontheregimes ofthesevariables.

Theresponsesofthepre-hurricanecanopyheightofToaBajaandCañoMartínPeña toelevationweresimilar(Table 3)asthesetwositeshadthesameelevationregimewitha meanelevationintherangeof0.36~0.39m(Table 2).Thequadraticfeatureimpliesthatthe pre-hurricanecanopyheightincreasedwithelevationwhenelevationwaslowerandthen decreasedwithelevationatahigherelevationrange.Themaximumpre-hurricanecanopy heightoccurredatamoderateelevationaround1maccordingtoourmodelanddata.The placeswithlowestelevationwereclosertothecoastwithredmangrove.Aselevation wentfromlowtomoderate,thespeciesshiftedtoblackorwhitemangroves.Aselevation continuedtoincreasebeyondthemoderaterange,thefreshwatersupplydecreasedand salinityincreased[44,45],therebydecreasingthepre-hurricanecanopyheight.Itseemsthat thispatterncanbeextrapolatedacrosssiteswithdifferentelevationregimes.LaParguera hadthelowestelevationrangewithameanof0.16mandmaximumof0.2m,suchthatthe pre-hurricanecanopyheightincreasedwithelevation.The Pterocarpus growinginbrackish wateratPalmadelMarhadameanelevationgreaterthan1msuchthatthepre-hurricane canopyheightdecreasedwiththeelevation.

ThecanopyheightreductionofallsitesexceptPalmadelMardecreasedwithelevationmostlybecausetheareaswithlowerelevationweremuddierandthestemsofthe mangroveswereeasiertofalldownorbeslantedbythewind[11].Inaddition,thelower elevationwasmorelikelytobeinundatedtocauseadditionaldamage[13].Whenelevation increased,thelowerpre-hurricanecanopyheightandthestrongerroot-soilanchorage allowedthesystemtoresistandreducethewinddamagetothecanopy.TheforestatPalma

delMarhadgreaterthan1mmeanelevationandwasclosesttotherivers/canals(Table 2), whichbothhelpedtodrainthehurricanewaterand,thus,reducedtheriskofprolonged inundation.However,thissitewasclosesttothehurricanelandingpointandexperienced thestrongestgustwind.Withtheincreaseinelevation,thedominant Pterocarpus withhigh canopywasexposedtostrongerwindand,thus,sufferedmoredamage.

4.3.DistancetoRivers/CanalsandtoCoast

Riversandcanalssupplyfreshwater,andcanalsofsewagepurposesdelivernutrients andfreshwatertothemangroveecosystemstoalleviatethesalinityandnutrientstresses, especiallyforplaceswithlowelevation.Ouranalysissupportedthehypothesisthatthe pre-hurricanecanopyheightandthecanopyheightreductiondecreasewiththedistance torivers/canals.However,thishypothesiswasonlyapplicabletopre-hurricanecanopy heightwithpooleddataandtothecanopyheightreductionatsiteswithmoderateelevation. LaParguerahadthelowestelevation,butnoriversorcanalspassingthrough,andthe nearestcanalswereabout1kmaway.ForFajardoandPalmadelMar,theelevationregimes weretoohightoretainthefreshwaterandnutrientsderivedbytherivers/canals.Hence, thedistancetorivers/canalsdidnotappearsigniﬁcantintheequationsforthesethreesites. Thedistancetorivers/canalsonlyappearedintheequationsforToaBajaandCañoMartín Peña,wheretheelevationrangewaslowtomoderate.Furthermore,themeandistances torivers/canalsareinthemoderaterange,andwithin-sitevariationsofthedistanceto rivers/canalswerethegreatestatthesetwosites(Table 2).Itseemsthattheconditions forthedistancetorivers/canalstocomeintoplayareatleastlowormoderateelevation andlargewithin-sitevariationofthedistancetorivers/canals.Theseconditionsdidnot concurrentlyexistforothersites.

Ourequationsshowthatareaswithashorterdistancetorivers/canalswereassociatedwithhigherpre-hurricanecanopy(Equation(4))andmorecanopyheightreduction (Table 4).Soilsnearrivers/canalsmaybeassociatedwithlowersalinityorbetternutrient status,whichnotonlysupportbettermangrovegrowth,butalsochangetheallocation pattern [4,46–48].Thechangedallocationpatternwouldincreasetheshoot/rootratioso thatthemangroveswouldinterceptmorewindforceduringhurricanesbuthaveless soil-rootanchorage.Theconsequenceisthatthetreeswouldbeeasiertofallortoslant. Thebetternutrientsupplymayalsochangetheleaftraitsofplantssuchthattheleaves maygrowthinner.Thinnerleavesareeasiertobetornbyhurricanewinds,thusincurring moredefoliation[49].Theﬂoodingmapdetectedfromradarimagesshowedgreaterinundationalongtherivers/canals(unpublisheddata).Thesefactsexplainwhytheareaswith closerdistancetorivers/canalssufferedmorecanopyheightreduction,whereasthosewith fartherdistancewereassociatedwithlesscanopyheightreduction.

Thedistancetocoastmaybeassociatedwiththeelevationandsalinitygradients.For coastalwetlandswithriverinemangroves,thesalinitygenerallyincreaseswiththedistance tothecoast[44,50].Thehighersalinityatfartherdistancesallowsmorerootgrowththan shootgrowthtoresistwinddamage.Thefartherdistancetothecoastwasalsoassociated withlowerpre-hurricanecanopyheightinCañoMartínPeña,ToaBaja,andLaParguera, aswellaslowercanopyheightreductioninCañoMartínPeña.Inaddition,placeswith fartherdistancetothecoastmaybelesspronetoinundationfromstormsurges.

4.4.TreeDensityandUnevennessofCanopy

Thealgorithm-derivedtreedensityappearedintheequationsforPalmadelMarand Fajardotoalleviatethecanopyheightreduction.However,therelationshipbetweenthe pre-canopyheightandthetreedensitywasnotconsistentacrossallsites.Largerandtaller treesmaybeassociatedwithlowertreedensityduetoself-thinning.However,highertree densitymayalsomakethetreesgrowtallertocompeteforlightsothathighercanopy heightmaybeassociatedhighertreedensityormaynotbesigniﬁcantlyrelatedtothetree density[11].

Treedensityhasbeenidentiﬁedasafactorthatmodulatesthewinddamagetoforests inseveralstudies:Treesgrowingtogethercansupporteachothermechanically[8]by increasingtheinteractionamongneighboringtreesthroughfrictionofleavesandbranches indissipatingthewindenergy.Hightreedensityisespeciallyimportantformangroves withlowstemdiameters.Theoreticalandpracticalstudiesofwindbreaksystemshave indicatedthatdensityisoneofthemajorparametersforeffectivewindreduction[51].On theotherhand,forestswithlowertreedensityoftenexperiencemoredeadtreesandbent trunksaftermajorhurricanes[52].AhybridmodelofForestGalesdevelopedforsimulation ofwinddamageriskofforestsusedaseriesofimportantparametersincludingspacing amongtrees,whichistheinverseofthetreedensity.Thesensitivityanalysisfoundthat thecriticalwindspeedofstemruptureisinverselyproportionaltotheaveragespacing amongtreessothathigherwindspeedisneededtorupturecloselyspaced(highdensity) trees[10,53].

Acloselyrelatedconceptistheunevennessofthecanopy,whichappearedinour equationforToaBajatoenlargethecanopyheightreduction(Table 4).Boundary-layer theoryindicatesthatroughsurfacesassociatedwithunevennessofcanopiescanmakethe boundarythinnertofacilitateverticalconvections[54]suchthatthewindcanmoreeasily traversetheforestcanopyandcausemoredamage.Unevennessofcanopyheightisalso relatedtothetreedensity.Inadditiontotheheterogeneoussalinity/nutrientconditionsand thecompetitionamongtreesthatgivesdifferentcanopygrowth,thespatialheterogeneity oftreedensityislikelytocreatetheunevennessofthecanopyaslowtreedensitiesare likelyassociatedwithgapsinthecanopytoincreasetheunevennessofthecanopyheight.

4.5.HurricaneWindsandRainfall

Hurricanewindisthemostimportantforcedamagingthecanopy.TheforestatPalmar delMarexperiencedthestrongestgustwindandconsequentlyencounteredthemostsevere canopydamage,i.e.,55%relativecanopyheightreduction(Table 2).Inaddition,forthe coastalmangrovesdistributedinalowelevationprofileand,thus,susceptibletovarious floodingdrivers(coastalsurge,fluvial,orpluvial),rainfallduringthehurricanesappeared tobeanimportantdriverofcanopyheightreduction(Equation(5)).Thedrainagecapacity ofmangroveecosystemscan,thus,playanimportantroleinrainfall-driveninundation. Ourongoingworkonradar-detectedinundationshowedinundationsalongthecoast, alongtherivers/canals,andinlow-lyingareasafterthehurricanewhichlastedaround 10days.TheforestsatCañoMartínPeñaandToaBajaexperiencedstronggustwindsand theheaviesthurricanerainfall(Table 2).Thesetwositeshadlowtomoderateelevation withclosedistancetothecoastortherivers/canals,thusbeingpronetocoastalsurgeand fluvialorpluvialflooding.Theinundationcausedbythedownpour,stormsurge,andriver overflowisanimportantfactorresultinginadditionaldamage.

Wetlandrecoveryfromhurricanedamagewillbeafuturesubject.AirborneLiDAR datafromcampaignsafter2018shouldbeincorporatedwithmultispectralandhyperspectralimagestofulﬁlthistask.InadditiontoairborneLiDAR,spaceborneLiDAR dataarebecomingavailablerecently.Forexample,GEDI(GlobalEcosystemDynamics Investigation)onboardtheInternationalSpaceStationprovidesanalternativedatasource withlonger-termdataatalargerscale[55].Verticalcanopystructureandcomplexity playanimportantroleinprovidingmicrohabitatsforotherspeciessuchasinsectsand birds[56,57].Therefore,theassessmentofcanopyheightusingLiDARmighthaveimplicationsinbiodiversitystudies,especiallyforthosespeciesrelyingonforestsaspartof theirhabitats.

5.Conclusions

UsingLiDARpoint-clouddatabeforeandafterthehurricanesinSeptember2017, weanalyzedthepre-hurricanecanopyheight,aswellasthecanopyheightreduction, duringthehurricanesforﬁvecoastalmangrovesites.Therewerethreegroupsofvariables thatmighthaveinterplayedtoaffectthevulnerabilityofmangroveforestsundertropical

stormdisturbance:(1)pre-hurricanecanopystructureincludingcanopyheightandits unevenness,treedensity,andallometrypattern,(2)thephysicalenvironmentincluding elevation,rivers/canalswithinorpassingthroughtheforests,anddistancetocoast,and (3)theexternalforcessuchaswindspeedandrainfallduringthehurricanes.Mangrove forestswithhigher,unevenercanopyandlowertreedensitytendtoexperiencemorecanopy damagethanthosewithlower,evenercanopyandhighertreedensity.Thisbiologicalgroup isshapedbythesecondfactor,i.e.,thephysicalenvironment.Spatialvariationofelevation, climate,anddistancetorivers/canalsandtocoasttendtomodifythecanopystructure,the allometry,andtheleaftraitsasthesephysicalenvironmentalvariablescontrolthespatial distributionofthesoilsalinity.Amongthesephysicalenvironments,elevationisthemost determinativeasitsregimegovernsthesigniﬁcanceofthedistancetorivers/canalsand tothecoast.Inadditiontowindspeed,wefoundrainfalltoalsobeanimportantfactor affectingthemangrovecanopydamagebythehurricanes,especiallyinlowlandprone toinundation.

TheestimateofcanopyheightbyLiDARpointcloudsisbasedonthereturnedsignals bythesource.Thus,thecanopyheightreductionmostlyreflectsthedefoliationandraptures ofbranches,but,toalesserextent,thefallandraptureofthetrunks.Thesignificanceofthe covariatesintheequationsseemedalsodependentonthescales.Forexample,thedistance torivers/canalswasnotsignificantintheequationofpre-hurricanecanopyheightforany site.However,itwassignificantintheequationforthepooledequation(Equation(4)). Correlationamongcovariatesmayalsocausedifferencesinresponseequationsamong sites.Futureeffortsshouldbemadeongroundfieldmeasurementsandscalingfromplotto landscapesothatLiDAR-basedanalysiscanofferamorecertainandcompletemechanistic understandingofmangrovevulnerabilitytohurricanedisturbance.

AuthorContributions: Conceptualization,Q.G.andM.Y.;methodology,Q.G.andM.Y.;formal analysis,Q.G.andM.Y.;writing—originaldraftpreparation,Q.G.;writing—reviewandediting,Q.G. andM.Y.Allauthorshavereadandagreedtothepublishedversionofthemanuscript.

Funding: ThisresearchwasfundedbytheNOAAPuertoRicoSeaGrantNA18OAR4170089.

DataAvailabilityStatement: AllthedatasetsarepubliclyavailableattheUSGS3DElevation Program(3DEP)dataportal(https://nationalmap.gov/3DEP/,accessedon15March2022)andthe NASAG-LiHTdataportal(https://glihtdata.gsfc.nasa.gov/,accessedon15March2022).

Acknowledgments: WeacknowledgeUSGSforprovidingtheLiDARafterthehurricanes,publicly availableattheUSGS3DElevationProgram(3DEP)dataportal(https://nationalmap.gov/3DEP/, accessedon15March2022),andNASAforprovidingtheLiDARdatabeforethehurricanes,publicly accessibleatNASAG-LiHT(https://glihtdata.gsfc.nasa.gov/,accessedon15March2022).

ConﬂictsofInterest: Theauthorsdeclarenoconﬂictofinterest.Thefundershadnoroleinthedesign ofthestudy;inthecollection,analyses,orinterpretationofdata;inthewritingofthemanuscript,or inthedecisiontopublishtheresults.

AppendixA

Theaerialphotosofriverinemangrovestakenbeforeandafterthehurricanes(https: //glihtdata.gsfc.nasa.gov/puertorico/index.html,accessedon15March2022).

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