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EcologicalEngineering177(2022)106558
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EcologicalEngineering
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Theeffectoftwotypesofgridtransplantationoncoralgrowthandthe
in-situecologicalrestorationinafragmentedreefoftheSouthChinaSea
JingquanXiaa,b,c,1,WentaoZhua,d,1,XiangboLiua,b,YuxiaoRena,b,JianzhongHuanga,d,
MingZhua,b,Zhong-qi-yueWub,AiminWanga,b,XiubaoLia,b,*
aStateKeyLaboratoryofMarineResourceUtilizationinSouthChinaSea,HainanUniversity,Haikou,China
bCollegeofMarineScience,HainanUniversity,Haikou,China
cHengxingSeedIndustryScienceandTechnologyLimitedCompany,Shouguang,China
dCollegeofEcologyandEnvironment,HainanUniversity,Haikou,China
ARTICLEINFOABSTRACT
Keywords:Duetoclimatechangeandhumanactivities,coralreefecosystemsarefacingacrisisofdegradationglobally.
CoralreefSomecoralreefsinthenorthernpartofWuzhizhouIsland(SoutheasternHainanIsland,theSouthChinaSea)
Coraltransplantationhavebeenfragmentedbecauseofcontinuousdisturbance,andwesystematicallyconductedin-siturestoration
Ecologicaleffect
experimentstoacceleratetheecologicalrestorationinthisarea.InSeptember2019,40reefswithhollow
Ecologicalengineering
Artificialrestorationstructureswereplacedintheexperimentalarea,andacontrolareawasselectedatthesamedepth.Twentyofthe
Fragmentationrecovery40reefswerecoveredbyacylindricalgridwithadiameterof0.5cm(GFngroup),andtheremaining20were
coveredbyaflatgridwithawidthof1cm(BFngroup).Atotalof1140coralcolonies,composedofAcropora
hyacinthus,Acroporamicrophthalma,Acroporaflorida,Montiporatruncata,andPoriteslutea,weretransplantedin
thisexperiment,withanoverallsurvivalrateof94.27%duetothecoraltransplantbaseofthecarryingreefs
beingofsufficientweight,hollowstructure,anddensegrid.ThesurvivalrateandannualgrowthrateofAcropora
intheGFngroupwithanarrowbutlargemeshandcylindricaldesignweresignificantlyhigher,andthefastest
growthratewasfoundinA.hyacinthus,growingat27.33±10.37cm2⋅month1.MontiporatruncataandP.lutea
intheBFngroupwithawidemeshandflatstructurehadhighersurvivalratesandsignificantlygreatergrowth
rates.Intheecologyofthecoralcommunity,coralcoverageintheGFngroupwassignificantlyhighercompared
withtheBFngroup,whichwasmainlyattributedtothedifferenceinthegrowthofAcropora.Comparedwiththe
reeffragmentationarea,thethree-dimensionalstructureofthehollowreefanditsradiationeffectsignificantly
attractedtheaccumulationoflargeinvertebratesandreeffishes.Seacucumbersandseaurchinsgatheredfaster,
formingastablecommunitystructure.Thedominantfishspeciesgraduallytransformedfromthelargealgae-
eatingfishSiganusfuscessenstotheterritorialalgae-eatingfishDascyllusreticulatusduetochangesinthe
three-dimensionalstructureofthegridsurfacecausedbycoralgrowth.Studieshaveshownthatthethree-
dimensionalstructureofareefcansignificantlyaffecttheaggregationofbenthicorganisms.Amongthe
selectedcorals,Acroporagrewmorerapidly,whichestablishedmorecomplexthree-dimensionalstructuresto
achieveabetterecologicalrestorationeffectinthereefarea.ThecombinationoftiledMontiporaandlumpy
Poritescouldincreasethebasecoverageandreducetheimpactofalgaeonthecorals.Ourresultssuggestthat
whentransplantingdifferenttypesofcorals,weshouldconsidertheuseofmultiplecomprehensivefactorssuch
asthetypeofthereef,thestructureofthegrid,thecharacteristicsofthetransplantedcorals,andtheinfluenceof
environmentalfactors.
1.Introductionecosystemsintheworld(JompaandMcCook,2002),andthisdiversity
providesreef-dwellingcreatureswithhabitat,foraging,andshelterfrom
Thecoralreefecosystemisoneofthemostcomplexanddiversepredators(Lindahl,2003;Zhuetal.,2021a).Particularly,abundant
*Correspondingauthorat:58RenminRoad,Haikou,HainanProvince570228,China.
E-mailaddress:xiubaoli@(X.Li).
1Theseauthorscontributedequallytothiswork.
/10.1016/j.ecoleng.2022.106558
Received20September2021;Receivedinrevisedform18January2022;Accepted24January2022
0925-8574/©2022ElsevierB.V.Allrightsreserved.
J.Xiaetal.
EcologicalEngineering177(2022)106558
biologicalresourcesplayanimportantroleinprovidingfoodprotein,experimentalarea.Thewaterdepthoftheexperimentalareawasbe-
extractingpharmaceuticallyactivesubstances,andpromotingtourismtween7and8m,andthecentercoordinateswereN18◦′′′
19008and
◦′′′
development(Branderetal.,2012;Pascaletal.,2016).InthepastfewE10945926(Fig.1).Thewaterqualityinthisareawassuitablefor
decades,climatechange(increasedseatemperature,oceanacidifica-coralgrowthandhadacoralrecruitmentof2.64ind⋅m2(Huangetal.,
tion,andmorefrequenttyphoons)andhumanactivities(over-2020b).Toensurethereliabilityoftheevaluation,a50mfixedtransect
exploitation,destructivefishing,seaeutrophication,etc.)havecausedwasselectedatthesamedepthofthereeffragmentationareaatadis-
seriousdamagetocoralreefs(Chengetal.,2014;De’athetal.,2012;tanceof10mfromthereef,and1mareasonboththeleftandrightsides
Edmundsetal.,2019;McManusetal.,2020;Rinkevich,2019;Ryanwereselectedasthecontrolarea,withatotalareaof100m2.
etal.,2008).NearlyhalfofthecoralreefsinthePacificCoralRegionAtotalof40reefsmadeofreinforcedconcretewereplacedintothe
havedegradedinthepast40years(Hughesetal.,2017).Thesituationexperimentalarea.Thereefswerearrangedinfivecolumnswithan
intheWesternAtlanticisevenmoreworrisome,and80%ofthecoralintervalof100cm.Theweightofthereefswasupto3tons,theouter
reefstherehavebeendegradedsincethemid-1970s(BrunoandSelig,dimensionwas200cm*100cm*100cm,andtheinnerhollowwas
2007).ThecoralcoverageofthereefsintheSouthChinaSeahasalsoconnectedbya20*20*20cmsupportingcolumn.Differentgridplates
droppedfromabout60%toabout20%inthepast10–15years(Hugheswereusedtocoverthereefstoprovideadequateattachmentandcreatea
etal.,2013),andeventhecoverageofreef-buildingcoralsintheSanyatransparentgrowthenvironmentforthetransplantedcorals.Onthe
CoralReefReserveisonly14.13%(Sunetal.,2018).Thedegradationofuppersurfaceof20ofthe40reefs,aglassfiber-reinforcedpolymer
coralreefswillcauseasharpdeclineinmarinelife,lossofbiodiversity,(GFRP)netwasfixed,andontheother20reefs,abasaltfiber-reinforced
coastalerosion,andreductionoffoodsources(Bongiornietal.,2011;polymer(BFRP)netwasfixedontheuppersurface.Thelengthand
McCauleyetal.,2015).widthofasinglepieceofthetwogridswereboth200*100cm.The
Tomitigatethedamagedonetocoralreefsinrecentyears,variousGFRPnetwasofacylindricaltypewithadiameterof0.5cmandamesh
methodshavebeenproposedtoacceleratetheirrecovery,includingwidthof4.5cm.Thevolcanicfiber/BFRPnetwasofaflattypewitha
improvementofbottomquality,removingpressuresources,coralwidthof1cmandameshwidthof4cm(Fig.2).Thereefscoveredbythe
nursery,coraltransplantation,andintroducingkeyspecies(Foxetal.,twogridswerenamedtheGFngroupandtheBFngroup,respectively.
2019;KheawwongjanandKim,2012;Ngetal.,2016;YanovskiandInSeptember2019,dominantlocalspecieswerecollectedfroman
Abelson,2019).Whentheintermittentdisturbanceofcoralreefsturnsestablishednurseryforcoraltransplantation(Lietal.,2019).Forthe
intocontinuousdisturbance,thedegreeofdamagetothereefscontinuesrapidconstructionofthree-dimensionalstructures,branchedAcropora
toexacerbate,andsomeareasaredifficulttorecoverwithouthumanhyacinthus,Acroporamicrophthalma,Acroporaflorida,tile-shapedMon-
intervention(Youngetal.,2012).Amongthem,thefragmentationofthetiporatruncata,andclumpyPoritesluteawereselected,whichcouldin-
reefdiscthataffectsthesurvivalofhealthycoralsandhindersthecreasethebiodiversityofthetransplantedarea.Atotalof1140plants
attachmentoflarvaeistheworstcase(Foxetal.,2019;Foxetal.,2005).weretransplantedonthe40reefs(Fig.3).Duetothefastgrowthof
Toimprovethefragmentedreefdisc,restorationmethodssuchasA.hyacinthus,24plantsofA.hyacinthusand30plantsfortherestofthe
removinggraveltorestorethereefdisc,coagulatinggravelwithviscouscoralsweretransplantedtoeachreef.
material,promotingcalcificationbyelectrodeposition,puttingreefto
buildarockybase,andgridcoveringbrokenbranchestostabilizethe2.2.Long-termmonitoringofambienttemperature
baseandraisecorallivingspace,havebeenappliedinpractice(Clark
andEdwards,1999;LirmanandSchopmeyer,2016;RachmilovitzandInOctober2019,aHobowatertemperaturelogger(UA-002-08)was
Rinkevich,2017;Raymundoetal.,2007;Rinkevich,1995;Williamsfixedonthereefinthemiddleoftheexperimentalarea(settorecord
etal.,2019;Zhengetal.,2021).Itisveryimportanttoselectappropriateonceevery15min).Attheendoftheexperiment,thedatawere
restorationmethodstoobtainsignificantcoralreefrestoration.analyzed,andthemonthlytemperaturewasusedintheanalysis.
InsomeareasinthenorthernpartofWuzhizhouIsland,reservoir
flooddischarge,tourismdevelopment,andhumanconstructionhave2.3.Coralgrowthsurvey
causedturbidwaterandincreasednutrients,affectingthesurvivalof
reef-buildingcorals(Huangetal.,2020b).ThisareaislocatedinThesurvivalandgrowthrateofcoralsweremonitoredevery3
southeasternHainanIsland,whichisaverygoodin-situexperimentalmonths(exceptforthe6thmonthduetotheepidemic)aftercoral
areabecausethesummerupwellingscanprovidepotentialrefugefromtransplantation(0,3,9,and12months).Moreover,576plantsontwo
globalwarming.Laddetal.(2018)havereviewed116coralrestorationreefsofeachcoralinthetwoexperimentalgroupswereselectedfor
articlesfrom1987to2017,andonly19%havereportedtheecologicallong-termmonitoring.Anunderwatercamera(Olympus-TG4)wasused
process(suchasrecruitment,predation,andherbivory).Furthermore,totakepicturesdirectlyaboveeachcoraltotrackandrecordtheir
therecruitmentoffishesandcoralshasbeenthemoststudiedprocessinsurvivalandgrowth.Thesurvivaloftheinvestigatedcoralswasjudged
thecontextofcoralrestoration,althoughtheycompriseonly5%ofallaccordingtothephotos,andanabsenceoflivingtissueorlossofcoral
restorationstudies.Only2.5%ofstudiesoncoralrestorationaddresswasrecordedasdeath.Thesurvivalrateofcoralwasexpressedasthe
herbivoryatall,withonlyonestudyfocusingonherbivorybyfishesorratioofthenumberofsurvivingcoralstothetotalnumberofsurveyed
seaurchins(Laddetal.,2018).Inthepresentstudy,weconductedcorals.Inaddition,20coralsofasimilarinitialsizewereselectedfor
continuousmonitoringaftertransplantingcoralsintheexperimentalgrowthanalysisindifferentgroups.ImageJ(NIH)wasusedtoanalyze
areaandrecordedtherestorationprocessofthelocalecologicalcom-theorthographicprojectionareaofthelivingpartofthecoralusingthe
munity.Moreover,wemainlyaimedto(1)exploretheeffectsoftwogridasaruler.Thecoralgrowthratewasdefinedasthedifferencebe-
gridswithdifferentsizesonthecoralgrowthandcoralsurvival;and(2)tweenthefinalareaandtheinitialareadividedbythenumberof
comparecoralcoverage,coralrecruitment,macroinvertebrate,andfishmonthsoftransplantation(thenumberofdaysoftransplantation
aggregationbetweenthereefexperimentalareaandthecontrolarea.dividedby30).Eachgroupofsurveyedgrowingcoralswasdividedinto
fourparts,thecoverageareaoffourcoralswasobtainedbydividingthe
2.Materialsandmethodsareaofeachpartofthecoralbytheareaofthecoveredgrid,andthen
theaveragevaluewasusedtocalculatethefinalcoverage.
2.1.Experimentaldesign
2.4.Investigationofthecoralreefcommunity
Topreventinterferenceduetohumanactivities,aflatfragmented
reefoutsidearecreationalscubadivingsitewasselectedastheFromOctober2019(1st,3rd,9th,and12thmonths),thelarge
2
J.Xiaetal.
EcologicalEngineering177(2022)106558
Fig.1.Amaptoshowthecoralrestorationsiteon(c)WuzhizhouIslandof(b)HaitangBayin(a)HainanIsland.ThemapissourcedfromGoogleEarth.
invertebrates(seacucumbers,seaurchins,crinoids,seasnails,andgroupsasduplicates.
starfishes)andreeffishcommunitiesweresimultaneouslysurveyed,and
real-timemonitoringandsynchronizedcamera(GoProHero7)2.5.Statisticalanalysis
recordingmethodswereadopted.Becausethereefhasathree-
dimensionalstructure,a1mmappingareaaroundthereefwasSPSS(IBMSPSSStatistics23)wasusedtoperformaone-wayanalysis
includedinthebiologicalcommunityrestorationarea,andthetotalofvarianceonthesurvivalandgrowthratesofthefivetransplanted
experimentalareawas224.4m2.Thecontrolareawaswithin100m2oncoralspeciesinthesamegroup,andTamhane’sT2multiplecompari-
bothsidesofthesamplingzone.Thetypesoforganismswereidentifiedsonswereconducted.Anindependentsamplet-testwasperformedon
basedonprevioussurveys,andthepossibleorganismswerepre-writtenthesurvivalandgrowthratesofthesamecoralspeciesindifferent
onthestatisticaltable.Toensureaccuratesynchronizationofthedata,groups(GFnvs.BFn).
thephotosandvideoswerereportedbacktothelaboratoryforverifi-
cationofbiologicalidentificationreferringto“Coralreeffishesofthe3.Results
SouthChianSea-TheXisha,NanshaandZhongshaIslands.”
At1yearaftercoraltransplantation(inSeptember2020),the3.1.Long-termtemperaturemonitoring
investigationofthejuvenilecoralrecruitmentandsubstratetypeofthe
controlareawasstarted,and24sampleframes(40*70cm)wereplacedAccordingtotheHOBOtemperaturerecords,theminimummonthly
onbothsidesofthefixedtransect.ThecoverageratewasdeterminedaveragetemperaturefromOctober2019toSeptember2020was
accordingtotheratioofthenumberofsubstratescorrespondingtothe◦
observedinFebruary(23.85C),andthehighestwasobservedinAugust
intersectionsinthesampleframetothetotalintersections.Thetypesof(30.65◦C).FromMaytoJuly,thetemperaturedecreasedunderthe
substratesincludedstonycoral,softcoral,sand,rock(15cm),rubbleinfluenceofQiongdongupwelling.InJuly,thetemperaturedifference
(0.5–15cm),deadcoral,zoanthids,macroalgae,andturfalgae.Thewaslargelyattributedtothecombinedinfluenceoftheupwellingand
replenishmentofcorallarvaeintheexperimentalareawasconductedsummerheat(Fig.4).
basedontheratioofthenumberofjuvenilecorals(0.4–5cmindiam-
eter)attachedtothedivingsurveygridtothegridarea.Thereplen-
3.2.Coralgrowthindicators
ishmentinthecontrolareawascarriedoutbasedontheratioofthe
numberofcorallarvaeinthesampleframetotheactualsampleframe
3.2.1.Coralsurvivalrate
area,andthenumberofsurveysampleframeswasdividedintofour
After12monthsoftransplantation,theoverallsurvivalrateofall
3
J.Xiaetal.
EcologicalEngineering177(2022)106558
Fig.2.(a)Reefshape;(b)Reefarrangement;(c)Glassfiber-reinforcedpolymer(GFRP)net;(d)Basaltfiber-reinforcedpolymer(BFRP)net.
coralspecieswas94.27%.Amongthem,thehighestsurvivalratewasgrowthrateaftertransplantation,andthegrowthratebetweenstages
foundinMontiporatruncata,andthelowestsurvivalratewasfoundinincreasedgradually(p0.05).ThegrowthrateofA.hyacinthusinthe
Poriteslutea.Aftercoraltransplantation,thesurvivalrateofcoralsGFngroupinthe9-12thmonthswasthelargest(61.26±32.73
graduallydeclined,withthefastestdeclineof2.08%inthe9–12-monthcm2⋅month1).ThegrowthrateofA.microphthalmaintheGFngroup
period.ThesurvivalratesofAcroporahyacinthusandAcroporamicro-(15.80±6.18cm2⋅month1)significantlyincreasedfromthe3rdtothe
phthalmaintheBFngroupweresignificantlylowerin3–9months,and9thmonth(p0.05),whilethegrowthrateintheBFngroupdidnot
theybegantoshowsignificantdifferencesfromtheGFngroup(pincreasesignificantlyuntilthe9thtothe12thmonth(15.57±8.23
21
0.05).MontiporatruncatawastransplantedintheBFngrouptomaintaincm⋅month)(p0.05).A.floridainthetwogroupshadslower
a100%survivalrate,whileitssurvivalrateintheGFngroupdecreasedadaptabilityuntilgrowthrateinthe9-12thmonthsincreasedsignifi-
steadilyinallstages.ThesurvivalrateofP.luteaintheGFngroupcantly(p0.05).MontiporatruncatawasstableintheBFngroup,and
decreasedby10.6%from9-12thmonths,whileitssurvivalrateinthethegrowthrate(4.16±2.59cm2⋅month1)of9–12monthswas
BFngroupremainedunchanged(Fig.5a).TheGFngrouphadahighersignificantlyaccelerated(p0.05).IntheGFngroup,thegrowthrateof
overallcoralsurvivalrate,withanaveragesurvivalrateof96.18%,Montiporatruncata(0.58±2.05cm2⋅month1)decreasedfrom9-12th
whichwashigherthanthevalueof92.36%observedintheBFngroup,monthsduetoalgaeinvasion,andsomecoralsshowednegative
althoughthisdifferencewasnotstatisticallysignificant(p0.05).Thegrowth.P.luteahadbetteradaptabilityintheBFngroup,anditsgrowth
survivalrateofA.microphthalmaandA.hyacinthusintheGFngroupwasratewashighercomparedwiththeGFngroup(Fig.6a,Fig.6b).
highercomparedwiththeBFngroup(p0.05).Thesurvivalratesof
P.luteaandMontiporatruncataintheBFngroupwerehigher,although
3.3.Communityecologicalindicators
thedifferencewasnotsignificant(Fig.5c).
3.3.1.Replenishmentofcorallarvae
3.2.2.Coralgrowthrate
At1yearaftertransplantation,thecorallarvaewerecollectedfor
Aftertransplantation,thegrowthrateofthesamespeciesofcoralsin
investigation.Thecorallarvaeintheexperimentalareaweremainlythe
differentgroupshadsignificantdifferences(Fig.6a).Thegrowthrateof
genusPocillopora.ThejuvenilecoralrecruitmentintheGFngroupwas
AcroporaintheGFngroupwashighercomparedwiththeBFngroup(p22
5.83ind⋅m,whichwassignificantlyhigherthanthe0.93⋅minthe
0.05),whilethegrowthratesofMontiporatruncata(2.03±0.91
2121BFngroup(p0.05).Accordingtotheanalysisofthephotostakenon
cm⋅month)andPoriteslutea(1.82±0.75cm⋅month)werehigher
thesampleframe,thelarvaeinthecontrolareaweresupplementedwith
intheBFngroup(p0.05).ThegrowthrateofAcroporahyacinthus
21thegenusPlatygyra.Thedensityofjuvenilecoralsinthecontrolarea
(27.33±10.37cm⋅month)intheGFngroupwassignificantlyfaster2
(0.60⋅m)wasnotsignificantlydifferentfromtheBFngroup,whileit
comparedwithotherspeciesofcorals(p0.05),suchasMontipora
21wassignificantlylowercomparedwiththeGFngroup(Fig.7a).
truncata(1.33±0.80cm⋅month)andP.lutea(1.12±0.78
21
cm⋅month).TherewasnodifferenceingrowthratebetweenAcropora
213.3.2.Coralcoverage
microphthalma(8.87±2.49cm⋅month)andAcroporaflorida(9.15±
21Thecoralcoverageintheexperimentalareaincreasedsignificantly,
2.15cm⋅month)intheBFngroup.
especiallythecoralcoverageintheGFngroupincreasedfromtheinitial
InthegenusAcropora,A.hyacinthusshowedasignificantlyhigher
1.85%to19.31%,andthecoralcoverageintheBFngroupincreased
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