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ContentslistsavailableatBiologicalConservationjournalhomepage:www.elsevier.com/locate/biocon Creatingaconservationnetwork:RestorationofthecriticallyendangeredChinesecrestedternusingsocialattractionYiweiLu,DanielD.Roby,ZhongyongFan,SimbaChan,DonaldE.Lyons Correspondingauthorat:ZhejiangMuseumofNaturalHistory,Hangzhou,China.E-mailaddress:(S.Chen). etal.,2017).Withsocialattraction,decoys(modelsofadults,chicks,andeggs),playbackofrecordingsofvocalizations,mirrors,scent,andcialburrowsareusedtolureadultseabirdstorestorationsiteswiththegoalofestablishingbreedingcolonies(JonesandKress,2012Morethan95%ofseabirdspecies,especiallyterns(Sterninae),canbeattractedtobreedingsitesbythepresenceofconspecicsandotherseabirds(Rollandetal.,1998).Also,ternsfeedtheiryoungandprovideotherparentalcareforextendedperiodspost-edging,suggestingthatchicktranslocationswouldlikelynotresultinedgedyoungthatwouldsurvivetorecruitintothebreedingpopulation.Toassurethesuccessofarestorationprojectusingsocialattraction,someimportantproceduresshouldbefollowed,includingnestingha-bitatenhancement,deployingsocialattractionbeforethenestingseason,closemonitoringoftheincipientcolony,andcontrolofpre-datorsthatmaythreatenthecolony.Afullunderstandingofthebreedingbiologyofthetargetedspeciesisalsocrucial,especiallysocialfactorssuchascolonysize,nestingdensity,andnestingsynchrony,whichcanplaykeyrolesinrestorationsuccess(Kress,1983Robyetal.,JonesandKress(2012)listed82seabirdrestorationprojectsusingsocialattractiontechniquesworldwide,and44oftheseprojects(54%)wereconrmedtohavebeensuccessful.Restorationofabreedingcolonyofanendangeredspeciesusingsocialattractiontech-niques,however,wouldlikelyfaceparticularchallengesduetosmallpopulationsize.TheChinesecrestedtern(Thalasseusbernsteini)isperhapsthemostthreatenedseabirdspeciesintheworld.Itwasrediscoveredin2000aftera63-yearperiodwithnoconrmedsightings,whenthespecieswaspresumedextinct(Liangetal.,2000).Totalpopulationsizewasestimatedatnomorethan50individuals,anditwaslistedbytheIUCNasCriticallyEndangered(BirdLifeInternational,2017).Themostser-iousimmediatethreattothesurvivalofthespecieswasexploitationillegalharvestofeggsbyshermen(Chenetal.,2009).Beyondthedirecttakeofeggs,thedisturbanceassociatedwithshermenlandingonbreedingislandstocollecteggsorshellshapparentlycausedbreedingternstoabandonsuitablenestingsites.AnotherdocumentedcauseofnestfailureinChinesecrestedternsisill-timedsummerty-phoons(Chenetal.,2015).Long-termissuesofconservationconcernforthespeciesincludenestinghabitatlossduetodevelopmentonis-lands,theintroductionofmammalianpredators(e.g.,rats[spp.]),andthedegradationofforaginghabitatincoastalareasduetosewagedischarge,agriculturalchemicalruno,andindustrialpollu-tion.ThesethreatstotheChinesecrestedternhavenotbeenadequatelyevaluatedduetothelackofclosemonitoringandresearchsincethespecieswasrediscovered.Consideringtheextremelysmallpopulationsizeandseverethreatstosurvival,theprimaryconservationactionfollowingrediscoverywassafeguardingallChinesecrestedterns.Butuctuationsinpopulationcountssincerediscoveryofthespeciesimpliedthattheremightbeotherbreedingadultsbesidesthosenestingatthetwoknowbreedingcolonies.Whiletheextensiveknownbreedingrangeofthespeciesmadeitextremelydiculttondadditionalbreedingcolonies,thefrequentshiftsamongcolonysitesledtoseverechallengesinsafeguardingthebreedingpopulation(etal.,2011).IfChinesecrestedternscouldbeattractedtoasitewithsuitablenestinghabitatthatiscontinuouslymonitoredandsecuredagainsteggharvestandotherhumandis-turbances,however,themostseriousimmediatethreatstothespeciesmightbequicklyaddressed,andthespeciescouldreverserecentde-clinesandclimbbackfromthebrinkofextinction.In2013,aternrestorationprojectwasinitiatedintheJiushanIslands(Fig.1),thelocationofaformerbreedingcolonyofChinesecrestedternsthatwasabandonedin2007afterbreedingfailureduetoillegaleggharvest.TiedunDao,whichwasselectedfortherestorationproject,isneartheoriginalbreedingisland(Jiangjunmao),butwasnotknowntohavebeenoccupiedbybreedingseabirds.SocialattractiontechniqueswereconsideredessentialforestablishingabreedingcolonyofChinesecrestedternsonTiedunDao;however,thesetechniqueshadneverbeforebeenusedtorestoreabreedingcolonyofsuchanextra-ordinarilyrarespecies.Toimprovethechancesforsuccess,weusedsocialattractiontechniquestotrytoestablishanewbreedingcolonyofgreatercrestedterns(T.bergii).Sincetheirrediscovery,Chinesecrestedternshadonlybeenfoundnestinginlargecoloniesofgreatercrestedterns(Chenetal.,2011);therefore,wehopedthatChinesecrestedternswouldsubsequentlyrecruittoanewbreedingcolonyofgreatercrestedUsingthisapproac

2 h,andmonitoringtherestorationsiteclosely
h,andmonitoringtherestorationsiteclosely,wesoughttoachievethreeobjectives:(1)attractgreatercrestedternstonestatanewbreedingsitebyusingsocialattractiontechniques;(2)establishanewcolonyofChinesecrestedternswithinacolonyofthecommonsympatriccongener;(3)provideamorerobustestimatetheglobalpopulationofChinesecrestedterns;ifthesuccessfulrestorationofamixedbreedingcolonyofgreatercrestedternsandChinesecrestedternsintheJiushanArchipelagodidnotnegativelyaectthesizeoftheothertwoknownbreedingcoloniesforChinesecrestedterns,itwouldindicatethatthereareotherbreeding-ageChinesecrestedternsandasyetundiscoveredbreedingcoloniesforthespeciessomewhereinthenorthwesternPacic.Achievingtheseobjectivesisacrucialrststepforthelonger-termgoalofestablishingawell-protectedandclosely-monitorednetworkofbreedingislandsforgreatercrestedternsandChinesecrestedterns,whichwouldaddressthedicultiesinthecon-servationofthiscriticallyendangeredspeciesandsaveitfromextinc-2.Methods2.1.StudyspeciesandareaTheChinesecrestedternhasbeenapoorly-knownspeciessinceitrstdescribedin1863.Followingthecollectionof21specimensin1937alongthecoastofShandongProvince,China,therewerenormedrecordsuntilfouradultsandfourchickswerefoundamongalargecolonyofgreatercrestedternsintheMatsuIslands,Taiwan,alongtheFujianProvincecoastofChinain2000(Liangetal.,2000).Priortothisdiscovery,manyornithologistshadpresumedtheChinesecrestedternwasextinct.Sincerediscoveryin2000,breedinghasnowbeenconrmedinlocations.Threeoftheselocationswerefoundbefore2013andarealongtheChinesecoast:theMatsuIslands(Liangetal.,2000etal.,2019),theJiushanIslands,andtheWuzhishanIslands(etal.,2010Fig.1).In2016,twoothersmallbreedingcoloniesofChinesecrestedternswereconrmedforthersttime:anuninhabitedislandothesouthwesterncoastofSouthKorea(Songetal.,2017),andthePenghuIslandsofTaiwan(LiuandHetherington,2016ThecontinentalcoastlineofZhejiangProvinceextendsover2200kmfrom27°06to31°11N,andthereare3061islandsocoastofZhejiangProvince,2886ofwhichareuninhabited.TheJiushanArchipelago(29°26N,122°10E)issituated19kmothecoastofXiangshanCounty,easternZhejiangProvince(Fig.1)andconsistsof76uninhabitedislandsthatwereincludedintheJiushanIslandsNationalNatureReservein2011.In2004,abreedingcolonyofChinesecrestedterns,thersttobediscoveredaftertherediscoveryofthespeciesnestingintheMatsuIslands,wasfoundonJiangjunmaoIslandintheJiushanArchipelago.About1020adultChinesecrestedternswerefoundnestingamongca.4000greatercrestedterns(Chenetal.,2009In2005and2006,noChinesecrestedternswerefoundnestingintheJiushanIslands,butin2007eightChinesecrestedternswereagainobservedbreedingamongnestinggreatercrestedternsonJiangjunmaoIsland.IllegaleggharvestapparentlycausedallcrestedternstoabandontheJiushanIslandsafterthe2007breedingseason.TiedunDaoisa2.58-haislandwithamaximumelevationof26.8maslthatwaschosenasaterncolonyrestorationsiteintheJiushanArchipelago.TiedunDaoislocatedabout1kmfromJiangjunmaoIsland,thesitewherenestingbyChinesecrestedternswasrstdetectedY.Lu,etal. intheJiushanIslands,andiswithinthecoreprotectedareaoftheNatureReserve(Fig.1).Itwasselectedbasedonseveralcriteria,in-cluding(1)absenceofhumanoccupationandmammalianpredators,(2)accessibilityforsitepreparationandmonitoring,(3)presenceofdensevegetationontopoftheisland,allowingcolonymonitorstoliveontheislandwithoutdisturbingnestingseabirds,and(4)proximitytoJiangjunmaoIsland,theformersiteofamixedspeciesterncolony.TheWuzhishanArchipelago(30°13N,121°50E)islocatedatthemouthofHangzhouBay,7kmoshoreofthelargestislandintheZhoushanGroup(Fig.1).Itconsistsof7uninhabitedislandsthatwereincludedintheWuzhishanIslandsProvincialNatureReservein2001.Since2008,twotosixpairsofChinesecrestedternshavebeenobservednestingamonggreatercrestedternsatlargecoloniesintheWuzhishanIslands(Chenetal.,2011).Theterncolonyshiftedamongfourislands,dependingonthebreedingseason,includingMantoushan,Yaqueshan,Longdongshan,andWumaoshan.In2014,however,thismixed-speciesbreedingcolonydisappeared.In2015,wechoseYaqueshanasasecondrestorationsitewheresocialattractionwouldbedeployedinanetostabilizethebreedingcolonythere.Yaqueshanisa1.08-haislandwithamaximumelevationof18.5masl;theislandisrelativelyatandcoveredbyshortgrasscomparedtotheotherislandsintheWuzhishan2.2.SocialattractiontechniquesSocialattractionaimstolureadultbirdstorestorationsiteswiththegoalofestablishingorre-establishingbreedingcolonieswherenonecurrentlyexists.Mostseabirdspeciesaregregariouscolonialnesters,excellentcandidatesforrestorationbecausetheycanbeluredusingsocialattractiontechniquesthatseektoreplicatefeaturesofanestab-lishedcolony(Kress,1983Robyetal.,2002Jonesa

3 ndKress,2012Mostternspeciesareamenableto
ndKress,2012Mostternspeciesareamenabletotheuseofsocialattractiontolurethemtoasitewheresuitablenestinghabitatisavailable.Decoysaredeployedacrossaprospectivecolonysiteandrecordingsofcallsareplayedusingautomatedaudioplaybacksystems.Thevisualandaudiocuescauseprospectingadultternstoinvestigatethesiteandremainuntilotherpotentialmatesarealsoattracted.Thistechnique,coupledwithintensivemonitoringandmanagementofanyproblemsthatarise(e.g.,predators)hasbeensuccessfulinrestoringbreedingcoloniesofnearly50dierentseabirdspeciesaroundtheglobe(JonesandKress,Zhouetal.,2017Inearly2013,beforethebreedingseason,weusedbaitstationsandtrackplatestosurveyforpotentialmammalianpredatorsatTiedunDao.Lesserriceeldrats(Rattuslosea)weredetectedonTiedunDao;consequently,weusedtherodenticideBromadiolonedispensedatbaitstationstoeradicateratsfromtheisland.AccordingtoChenetal.,thepreferrednestsubstrateofmixedcoloniesofgreaterandChinesecrestedternsincludesgrassyareas,barerock,andazoneofinterspersedbarerockandlowgrassdevoidoftallvegetation.WeedtheeasternpartofTiedunDaoashavingsubstratemostsuitablefornestingternsandtheprospectivesiteforanewternbreedingcolony;thispartoftheislandincludesanextensiveareaofbarerockthatslopesdowntotheshoreline,providingaccesstothewater'sedgeforolderchicks.InlateAprilof2013,onemonthbeforetheternbreedingseasonstarted,wedispensedrodenticidetoeradicateratsfromtheisland.Thenweclearedvegetation,uprootedtallgrasses,andcutshortergrassesinarectangularareaabout60m×200masthepredeterminedsitefortheprospectiveterncolony.Toprovidesocialattractionatthenewcolonysite,wesecurelyinstalled350plasticgreatercrestedterndecoysand50Chinesecrestedterndecoys.Wealsodeployedthreeaudioplaybacksystems(MurremaidMusicBoxes,SouthBristol,Maine,USA)ontheprospectivecolonysite,eachincludingtwopatiospeakersandpoweredbysolarpanels.Theaudioplaybacksystemsbroadcast Fig.1.Thestudyarea,includingthetwositesinZhejiangProvincewhereChinesecrestedternrestorationprojectshaveusedsocialattractiontechniques:TiedunDaointheJiushanArchipelagoandYaqueshanintheWuzhishanArchipelago.Y.Lu,etal. digitalrecordingsofthecallsofgreatercrestedternsthathadbeenrecordedatabreedingcolonyontheWuzhishanIslands.Afterthebreedingseason,weremovedalldecoys,audioplaybacksystems,andsolarpanelsfromtheterncolonysiteforcleaning,maintenance,andstorageduringthenon-breedingseason.Wefollowedthisprocedureeachyearduring20142.3.MonitoringanddatacollectionIn2013,therstyearoftherestorationeortintheJiushanIslands,wesetupavideosurveillancesystemattherestorationsiteonTiedunDao,andthecolonymonitorslivedonanearbyisland,Jigushan,andmonitoredthecolonysitewithbinocularsandspottingscopesfromadistanceofabout600m.Becauseofthedicultyofcloselymonitoringtherestorationsitefromsuchadistance,beginningin2014thecolonymonitorslivedintentsorportablebuildingssetupontheoppositesideofTiedunDaofromtheterncolonysiteandseparatedbyadensepatchofvegetation.Theresidentcolonymonitorsmonitoredtherestorationsiteandbreedingcolonyfromobservationblindsthatwereinstalledattheperipheryofthenestingarea.Ingressandegressfromtheobservationblindswasviaconcealedpathwayscutindensevegetationadjacenttotheareaclearedasnestinghabitat.Thisset-upfacilitatedtheclosemonitoringofthebreedingcolonywithoutdisturbingnestingterns.Thetasksoftheresidentcolonymonitorsincluded(1)deterringdisturbancetotheterncolonyduetoillegaleggharvestorotherhumanvisitationtotheisland;(2)detectingotherpotentialfactorsthatmightlimitcolonyrestoration,suchasdisturbancefrompredators;(3)monitoringuseoftheislandbygreaterandChinesecrestedterns,includingvisitation,breedingbehavior,egg-laying,incubation,andchick-rearing;and(4)respondingtoanyfactorsthatmightlimitcolonyrestorationasap-propriate(e.g.,predatorremoval). Fig.2.NumbersofChinesecrestedternsandgreatercrestedternsattendingtheTiedunDaocolonyrestorationsiteintheJiushanIslandsandtheYaqueshancolonyrestorationsiteintheWuzhishanIslands,ZhejiangProvince,Chinaduringthe20132018breedingseasons.RestorationeortswereinitiatedonTiedunDaoin2013andonYaqueshanin2015.Y.Lu,etal. AttheWuzhishanIslands,thecolonymonitorsdidnotliveonthenestingisland,butvisitedYaqueshan,thenestingisland,duringthedayviawatercraft,weatherpermitting.ThecolonymonitorsobservedthenestingareaandterncolonyfromanobservationblindsetuponthenortheasternsideofYaqueshan.DataontheestimatednumberofgreaterandChinesecrestedternspresentoneachcolonyandthecausesofanyternnestingfailurewerecollecteddailyonTiedunDaoand,weather-permitting,onYaqueshan.Thenumbersofgreatercrestedternsonthebreedingcolonieswereestimatedfromtheblindsbycountingthenumbersofincubatingandnon-incubat

4 ingternsinplots(3m×3m)thatweremarkedont
ingternsinplots(3m×3m)thatweremarkedonthenestingareapriortothebreedingseason.Becausetheentirebreedingcolonycouldnotbeobservedfromtheblinds,theseestimateswereextrapolatedtotheentirecolonyareabyadjustingtheplotcountsbasedontheratioofternsinplotstothetotalnumberofactiveternnestscountedduringwalk-throughsoneachcolonyinmid-June,lateintheincubationperiod,whenpeaknumbersofbreedingpairswerein-cubatingeggs.Tocountthetotalnumberofternnestson-colony,68teammemberswalkedthroughtheentirecolonyandtookphotographsofalleggsineachnestingplot.Fromthephotography,wecoulddistinguishactivenestsfromabandonedonesbecauseunattendedeggsweregen-erallycoveredinmudandrolledtogetherinwindrows.Bycomparingphotographytakenduringmid-JunewithphotographytakeninlateAugust,onceallternshadnishednestingandleftthebreedingcolony,wecouldalsoestimatethenumberofeggsthathatchedineachplotandthroughouttheentirecolonyaswell.Thisestimateislikelyaminimumbecauseafeweggswerelaidonthecolonyaftermid-Junebyadultsthathadlosteggsearlierintheseason.Thenumbersofhatchedeggsminusthosetakenbypredatorsandthoseaddledonthenestingareawereconsideredthebestestimateofthenumbersofyounggreatercrestedternsraisedtoedgingageateachterncolony.ThenumberofChinesecrestedternswasaccuratetothenearestindividual,whilethenumberofgreatercrestedternswasconsideredaccuratetothenearest100individuals.3.Results3.1.SizeandproductivityofbreedingcoloniesTheestimatednumbersofadultChinesecrestedternsandgreatercrestedternsonthetwocolonyrestorationsitesduringthestudyperiodareshowninFig.2.In2013,twocolonymonitorsbeganmonitoringtheTiedunDaocolonysiteon7May.On1June,vegreatercrestedternsrstobservedonthecolonysitenearthesocialattraction.From3Juneto19June,28greatercrestedternswereoccasionallyobservedontheTiedunDaocolonysite,butabreedingcolonyfailedtoform.Onemonthlater,on18July,about50greatercrestedternssuddenlyappearedontheTiedunDaocolonysiteand,inthefollowingdays,thenumbersofternsincreasedrapidlyandegg-layingwasinitiated.ThenumbersofgreatercrestedternscontinuedtoincreasethroughoutmuchofAugust,peakingatanestimated3300individualson27Au-gust.By23JulyatleastsixChinesecrestedternshadjoinedthenewlyformedcolonyofgreatercrestedterns,andthenumberofChinesecrestedternscountedonTiedunDaopeakedat19individualson27August(Fig.2).Morethan800pairsofgreatercrestedternsandatleasttwopairsofChinesecrestedternslaideggs.Ultimately,thisnewlyes-tablishedterncolonysuccessfullyproducedover600greatercrestededglingsandatleastoneChinesecrestedternedglingbyearlyIn2014,ternsarrivedatTiedunDaoinearlyMayandmostlaidtheireggsbytheendofMay.Atitspeak,theTiedunDaocolonyin-cludedabout4000greatercrestedternsand43ChinesecrestedternsFig.2),andatleast13youngChinesecrestedternsandabout1000younggreatercrestedternswereedgedbytheendofthe2014nestingseason.AttheWuzhishanIslandsin2014,asmanyas500greatercrestedternsappearedinMay,butallabandonedthenestinggroundlaterinthemonth.ThiswastherstyearthatthemixedspeciesbreedingcolonyofcrestedternsabandonedthecolonyintheWuz-hishanIslandssincethecolonywasrstdiscoveredin2008.In2015,inaneorttorestoreacrestedternbreedingcolonyattheWuzhishanIslandsandstabilizeit,wedeployedsocialattractiononYaqueshanintheWuzhishanArchipelago.YaqueshanhadbeenthesiteofamixedspeciesbreedingcolonyofgreaterandChinesecrestedternsin2008,2010,and2012;in2009,2011,and2013theterncolonywasonadiislandintheWuzhishanArchipelago.Thesocialattrac-tionatYaqueshanconsistedofinstalling300greatercrestedternde-coysandtwoaudioplaybacksystemsdistributedovertheformernestingarea.Atthepeakofthenestingseasonabout3200greatercrestedternsand10ChinesecrestedternswereattractedtothecolonysiteonYaqueshan(Fig.2),andabout1200younggreatercrestedternsand4youngChinesecrestedternswereedgedbytheendofthe2015nestingseason.Duringthesamenestingseason,atotalofabout2500greatercrestedternsand52ChinesecrestedternsattemptedtonestonTiedunDaointheJiushanIslands(Fig.2).About1000younggreatercrestedternsand16youngChinesecrestedternswereedgedfromtheTiedunDaocolonyin2015.In2016,asmanyas100greatercrestedternsappearedatthecolonysiteonTiedunDaoinearlyMay,buttheTiedunDaocolonywasun-expectedlyabandonedbytheendofthemonth(Fig.3).Theearliestarrivinggreatercrestedternslaidtwosmallbatchesofeggs,15and7eggseach,buttheseeggsdisappearedsoonaftertheywerelaid,andadultternsdidnotattendthecolonyovernight.Usingvideosurveil-lanceequipment,wediscoveredthattheterneggswerebeingcon-sumedbykingratsnakes(Elaphecarinata)atnight,andthatthispre-datordisturbancewaslikelythecauseofcolonyabandonmentearlyinthe2016breedingseason.MeanwhileatYaqueshanintheWuzhishanIslands,atotalofabout4000greatercreste

5 dternsandatleast14Chinesecrestedternswer
dternsandatleast14Chinesecrestedternswerecountedduringthepeakofthenestingseason(Fig.2),andthecolonyatYaqueshanproducedabout1200greatercrestedternedglingsand6Chinesecrestedternedglingsbytheendofthe2016breedingseason.In2017,after18kingratsnakesweretrappedandremovedfromTiedunDaobeforetheternbreedingseason,themixedspeciesterncolonyreformedonTiedunDaoamidstthedeployedsocialattraction.About2500greatercrestedternsand26ChinesecrestedternswerecountedontheTiedunDaocolonyduringthepeakofthebreedingseason,andabout1100greatercrestedternedglingsand6Chinesecrestedternedglingswereproducedbytheendofthe2017nestingseason.ConcurrentlyatYaqueshan,about2600greatercrestedternsandatleast12Chinesecrestedternsnestedamidstandnearsocial Fig.3.TimelineofattendancebygreatercrestedternsofthecolonyrestorationsiteonTiedunDao,JiushanIslandsduringthe2016breedingseason,wheninvasivekingratsnakesweredetectedonandremovedfromthecolonysite.Thenumbersofgreatercrestedterneggspresentonthecolonyrestorationsiteeachdayarealsoshown.Y.Lu,etal. attraction,andabout1000greatercrestedternedglingsand4Chinesecrestedternedglingswereproducedbytheendofthenestingseason.In2018,theternbreedingcoloniesformedatthecolonysitesinthetwoislandgroupsinearlyMay,asin2017.About4200greatercrestedternsand42ChinesecrestedternswerecountedattheTiedunDaocolonybymid-June,andabout5300greatercrestedternsand35ChinesecrestedternswerecountedconcurrentlyattheYaqueshancolony(Fig.2).BylateAugust,about1600greatercrestedternchicksand13ChinesecrestedternchickshadedgedatTiedunDao,andabout1900greatercrestedternchicksand12ChinesecrestedternchickshadedgedatYaqueshan.3.2.ThreatstobreedingChinesecrestedternsIllegaleggharvestandassociateddisturbancetobreedingadultshavebeenidentiedasthegreatestthreattoChinesecrestedternsChenetal.,2015);however,noterneggcollectionoccurredateithertheTiedunDaoortheYaqueshancoloniesduringthe6-yearrestorationperiod.Duringthebreedingseasonsof20132018,thecolonymonitorsfortheTiedunDaorestorationsitepreventedatotalof13attemptsbyshermentolandontheisland,includingoneinstancein2014whenaedtheislandjustafterenteringthebreedingcolonyandnoticingacolonymonitorwasinanobservationblind.Thecolonymonitorsalsodeterredanadditional28vesselsfromapproachingthecolonysitesocloselyastoushadultterns.On11July2015,aSuperTyphoonnamedChan-hom(Category4stormwith210km/hwinds)passednearbothTiedunDaoandYaqueshan,killingatleastsixgreatercrestedternchicksatTiedunDaoandatleast184greatercrestedternchicksatYaqueshan,butnoChinesecrestedternswereknowntohavebeenkilledduringthisty-AsinglelesserriceeldratwasdetectedonTiedunDaoinboth2015and2016,andthreelesserriceeldratsweredetectedatYaqueshanin2015and2016.DespitethepresenceofsmallnumbersofthiswidespreadandomnivorousratspeciesonTiedunDaoandYaqueshan,noharmtotheternbreedingcoloniesontheseislandsfrominvasiveratswasdetectedordocumentedduringourstudy.Oneormoreperegrinefalcons(Falcoperegrinus)wereobservedvisitingtheternbreedingcolonyonTiedunDaoduringthebreedingseasonsof2014,2015,2017,and2018,andfalconsweredocumenteddepredatingatleastsixadultgreatercrestedternsonornearthecolony.NoChinesecrestedternswereobservedbeingdepredatedbyperegrinefalconsduringthestudyperiod,however.KingratsnakeswereobservedonTiedunDaoduringboththe2014and2015breedingseasons,butthiscommonandwidespreadspecieswasnotdocumentedtoeatterneggsuntil2016.Therst23eggsthatwerelaidbygreatercrestedternsontheTiedunDaocolonyin2016wereallapparentlyeatenbykingratsnakes,andthebreedingcolonywassubsequentlyabandonedduringthe2016nestingseason(seeFig.3).Onlyafter18kingratsnakeshadbeentrappedandremovedfromTiedunDaobeforethe2017nestingseasondidthemixed-speciesternbreedingcolonyreformonTiedunDao.NokingratsnakesweresubsequentlydetectedonTiedunDaoduringthe2017nestingseason.However,snaketrappingearlyinthe2018nestingseasonrevealedthatatleastfourkingratsnakeshadre-colonizedTiedunDao.4.Discussion4.1.SocialattractionandtheconservationchallengesfortheChinesecrestedternSinceChinesecrestedternswererediscoveredintheMatsuIslandsin2000,thespecieswasregardedfor13yearsasbreedinginonlytwolargecoloniesofgreatercrestedterns,andtheglobalpopulationofChinesecrestedternswasconsideredverylow,likelylessthan50in-dividuals(Chenetal.,2009Chenetal.,2015).SmallpopulationsizeandseverethreatstoreproductivesuccessfromillegaleggharvestandtyphoonsapparentlydrovethespeciestotheverybrinkofextinctionChenetal.,2015).Althoughalarmoverthespecies'statushasat-tractedworldwideconservationattention,savingthiscriticallyen-dangeredspeciesstillfacesmanychallenges.theonehand,thebreedingrangeoftheChinesecrestedternislargeandextensive,acrossmo

6 stoftheEastChinaSea,makingitex-traordina
stoftheEastChinaSea,makingitex-traordinarilydiculttodetectandmonitorallbreedingattemptsbythespecies.EvenforthethreeknownlargerbreedingcoloniesintheMatsu,Jiushan,andWuzhishanarchipelagos,largeuctuationsinnumbersofbreedingindividualshavebeenrecordedamongyears,andfrequentshiftsoccuramongdierentislandswithineacharchipelagoChenetal.,2009Hungetal.,2019;thisstudy).Thesenestingchar-acteristicsmakeitverydiculttomonitorandsafeguardtheveryfewknownbreedingindividuals.Ontheotherhand,twomajorthreatstothespecies'persistence,eggharvestandhumandisturbance,arestillwidespreadatislandsalongthecoastoftheEastChinaSea.Eliminationofthesethreatsdependsonincreasedpublicawarenessoftheconservationneedsofthespecies,whichrequiresalong-termeorttowardpubliceducationandout-reach.Intheshortterm,however,savingsuchacriticallyendangeredseabirdrequiresamoreimmediateandactiverestorationeort.Ourresultsindicatedthatsocialattractiontechniquescanprovideanim-portanttooltoaddresstheimmediatechallengesforconservationoftheChinesecrestedtern.First,itispossibletoattractChinesecrestedternstonestatselectedislands.Evenso,theChinesecrestedternissorarethatthesuccessofsocialattractiondependsonusingthetechniquetorestorelargebreedingcoloniesofgreatercrestedterns,whichthenlureChinesecrestedternstorecruittothosecolonies.Second,theuseofsocialattractiontechniquestoestablishorrestoremixedspeciesterncoloniesonparticularislandsprovidesanopportu-nityforclosemonitoringofthosecolonies,iftheislandsareselectedcarefullytofacilitatemonitoringeorts.Closemonitoringofactiveterncoloniescaneectivelydeterillegaleggharvestandotherhumandis-turbance,enhancingtheprospectsforbreedingsuccessatthecolony.Furthermore,closemonitoringprovidesanopportunitytoidentifythosefactorsthatlimitcolonysizeandnestingsuccess.Forexample,closemonitoringatTiedunDaoallowedthedetectionandeliminationofamajorthreattothatcolony,theinvasionofkingratsnakes,whichisawidely-distributedspeciesonislandsalongthecoastoftheEastChinaSea(Huang,1990)thatcancauseabandonmentofterncolonies.Third,throughtheuseofsocialattraction,weobtainedamoreaccurateunderstandingofthesizeofthepopulationofChinesecrestedterns.UsingarelativelycompletesurveyofpotentialnestingislandsalongthecoastofShandong,Zhejiang,andFujianprovinces,thetotalnumberofChinesecrestedternswasestimatedtobenomorethan50individualsin2008(Jiangetal.,2005Liuetal.,2009Chenetal.,Hungetal.,2019).Becausethesesurveyswereconductedovermultiplebreedingseasons,however,theaccuracyofthispopulationestimatewassomewhatinquestion.Thenumberofbreedingin-dividualsthatwererecordedduringthesix-yearrestorationproject2018)wasconsiderablymorethanthepreviousestimateFig.4).Forexample,in2015theminimumtotalnumberofbreedingadultChinesecrestedternsreached75individuals,basedondatacol-lectedduringmonitoringattheMatsu(Hungetal.,2019),Wuzhishan,andJiushanarchipelagos.Thedramaticincreaseinthecensusnumberofbreedingadultssince2012impliesthatrestorationprojectsattheJiushanandWuzhishanarchipelagosattractedbreedingindividualsfromcoloniesotherthanthethreeknowncolonies.Twonewbreedingsitesthatwerediscoveredin2016supportourhypothesisthatotherpreviouslyundetectedbreedingcoloniesofChinesecrestedternswerethesourceoftheunprecedentednumbersofadultscountedin2015.InveChinesecrestedternswerediscoverednestinginalargeblack-tailedgullcolonyonasmallislandothesouthwestcoastofSouthKorea,andtwopairsofChinesecrestedternswerediscoveredatY.Lu,etal. thePenghuIslandsinTaiwan(Songetal.,2017LiuandHetherington,).Regardless,thebreedingcoloniesattheJiushan,Wuzhishan,andMatsuarchipelagosstillincludedmostoftheknownbreedingin-dividualsofChinesecrestedterns.Finally,thesuccessoftherestorationprojectsusingsocialattractionattheJiushanandWuzhishanarchipelagosgeneratedconsiderablepublicattention.Afour-episodedocumentarylmonthisternre-storationprojectwastelevisedbyChinaCentralTelevision(CentralTelevision,2016).Thispublicitygreatlyenhancedtheaware-nessofthisconservationprojectbygovernmentalagencies,scientists,andthegeneralpublicinashortperiodoftime,andcontributeden-ormouslytotheconservationoftheChinesecrestedterninChinaanditsprospectsforfuturerecovery.TheseabirdbreedingcoloniesintheJiushanIslandsNatureReservewerefrequentlysubjectedtoillegaleggharvestandhumandisturbancebefore2013(Fanetal.,2011etal.,2015),butintrusionbyboatsintotheprotectedareadecreasedcantlyfollowingtheinitiationofterncolonyrestorationandil-legaleggharvesthasnotbeenreportedsincethen.TherecordednumberofadultChinesecrestedternshasincreaseddramaticallysinceweinitiatedtherestorationprojectin2013(Fig.4In2018,weattractedatotalof77breedingadultChinesecrestedte

7 rnstotheTiedunDaoandYaqueshancolonysites
rnstotheTiedunDaoandYaqueshancolonysites,or88.5%oftheknownnumberofbreedingadultsintheglobalpopulationinthatyear.Alsoin2018,25ChinesecrestedternchicksedgedfromtheTiedunDaoandYaqueshancolonies,whichaccountedfor96.2%oftheknownnumberofChinesecrestedternedglingsproducedrange-wideinthatyear.Consequently,wenowknowforthersttimeinhistorythattheglobalpopulationofChinesecrestedternsexceeds100.Thepopulationin-creasefromlessthan50tomorethan100individualsisacautiouslyhopefulsignthatthiscriticallyendangeredspeciescanbebroughtbackfromtheverybrinkofextinction.AnewthreattotheChinesecrestedternhas,however,beenre-vealedbasedonmolecularstudies(Yangetal.,2018).EvidencefromthisstudyindicatesthathybridizationbetweenChinesecrestedternsandgreatercrestedternshasoccurred,andthatthehybriddescendantsarelikelyfertile.Geneticintrogressionmayrepresentaseriousthreattosuchacriticallyendangeredspecies.ThathybridizationhasoccurredisperhapsnotsurprisinggiventheverysmallpopulationsizeofChinesecrestedternsandtheirhabitofnestinginlargegreatercrestedterncolonies.Forthisandotherreasons(avoidinggeneticdriftandin-breedingdepression),rapidpopulationexpansionisfundamentaltotheconservationofChinesecrestedternsandsurvivalofthespeciesinthe4.2.Conservationnetworks:arestorationapproachforChinesecrestedternsandotherbreedingseabirdsinChinaAneectivepopulationrecoveryplanforanendangeredspeciesreliesoncompleteknowledgeofitslifehistory,ecology,andgeneticsCampbelletal.,2002).Forsomecriticallyendangeredspecies,directmanagementintervention,suchasarticialpropagationandexsituconservation,arenecessary(Fiedler&Groom,2006).Amongternsingeneral,andChinesecrestedternsinparticular,extendedpost-parentalcareisalifehistorytraitthatposesnearlyinsurmountableobstaclesforcaptivebreedingprograms.InthecaseoftheChinesecrestedtern,whosebreedingpopulationissosmallandwidelydis-tributedoveranextensivebreedingrange,andtheseverityofthethreatsstillfacingthespecies,creatingaconservationnetworkofmonitoredbreedingsitestosafeguardallnestingattemptsisregardedasthebestimmediateconservationaction.OurresultsindicatedthatitispossibletoestablishnewmixedspeciesbreedingcoloniesofgreaterandChinesecrestedternsusingsocialattractiontechniques.Closemonitoringandsafeguardingofthesenewcoloniescanprotectthecoloniesfrommostmajorthreatsandtherebyenhancebreedingsuccess.Althoughtheuseofsocialattractionatonecolonysitemightimpactthenumbersofbreedingadultsatan-othersite,itispossibletoachievebalancedcolonysizesthroughco-operationandcoordinationofsocialattractioneorts.ThisapproachwassuccessfullyusedtosustainmixedspeciesbreedingcoloniesonTiedunDaoandYaqueshanin2015and2017.Withthepopula-tionsofbothgreatercrestedternsandChinesecrestedternsapparentlyincreasing,morenewbreedingcoloniescouldbecreatedusingsocialattraction.Bypersistinginthisapproach,awell-protected,closely-monitored,andextensiveconservationnetworkofternbreedingislands Fig.4.CountsofindividualadultandedglingChinesecrestedternsatextantbreedingcoloniesduringthe20002018breedingseasons.DatafromtheMatsuIslandsiscourtesyofHung(2018),datafromthePenghuIslandsiscourtesyofQianxunZheng,anddatafromKoreaiscourtesyofYunkyoungLee.Y.Lu,etal. couldbedevelopedintheEastChinaSea,andpotentiallyintheYellowSeaaswell,wheretheChinesecrestedternwasoriginallydescribed.SuchanextensiveconservationnetworkofprotectedcolonysiteswouldhelpspreadtheriskfrommajortyphoonsintheEastChinaSeaduringthenestingseason,typhoonswhosestrength,frequency,andoverlapwiththeternnestingseasonareknowntobeincreasingwithclimatechange(Chenetal.,2015Inthefuture,aconservationnetworkshouldincludemigratorystopoversitesandwinteringsitesacrosstheAustralasian-EastAsiaFlyway,aswellasbreedingsitesintheEastChinaSeaandYellowSea.Currently,thereisstillonlyaverylimitedunderstandingandknowl-edgeofthemigratorystopoversitesandwinteringrangeoftheChinesecrestedtern,andmoreresearcheortsareneededtoelucidatethespecies'habitatrequirementsduringthenon-breedingperiod.Althoughrestorationofacriticallyendangeredspeciesisusuallyadicult,long-term,andsystematicmissionwithmanyrisksoffailurealongtheway,creatingaconservationnetworkthroughsocialattractionoersanopportunitytoconsolidateconservationachievementsstepbystep,andenhancetheprospectsofsavingtheChinesecrestedternfromextinc-ManagingaconservationreliantspeciesliketheChinesecrestedterninthelongtermwillalwaysbeamajorchallenge,especiallysus-tainingthefundingsupportforcrucialresearchandconservationef-forts.Inrecentyears,however,associalattractionhasbeenappliedtomoresitesinaneorttorestorethepopulationofChinesecrestedterns,thefundingstreamsfromgovernmentalandnon-governme

8 ntalorga-nizationsfortheconservationofth
ntalorga-nizationsfortheconservationofthiscriticallyendangeredspecieshaveincreasedsubstantially.Weremainoptimisticthatasthepublicbe-comesmoreawareoftheplightofChinesecrestedternsandascon-servationawarenessincreasesinChinagenerallythattheresourcestosustainthisrestorationeortwillbeavailable.Therearevariouswaystocreateanewbreedingcolonyfordispeciesdependingontheirspecicbreedingecology.Itcouldbeachievedthroughsocialattraction,orchicktranslocation,orevenbyacombinationofthesetwotechniques.Itcouldalsobeachievedbyfo-cusingonjustonespeciesindependentlyor,asinthecaseofChinesecrestedterns,byfocusingonspeciesthatareclosely-relatedorcolonyassociates.Nevertheless,wehaveshownthatestablishingawell-mon-itoredandprotectednetworkofbreedingsiteshaswidespreadcon-servationimplicationsformostseabirds.Amongthe171activeseabirdrestorationprojectsconductedin16countries/regions,atleast75projectsweredeterminedtobesuccessfulinhelpingrestore34diseabirdspecies(Zhouetal.,2017).Throughtheuseofactiverestora-tiontechniques,robustconservationnetworksofbreedingsiteshavegraduallybeendevelopedforsomeseabirdspecies,includingAtlanticns(Fraterculaarctica),Caspianterns(Hydroprognecaspia),roseateterns(Sternadougallii),commonterns(Sternahirundo),andArcticternsSternaparadisaeaRobyetal.,2002Kressetal.,2009JonesandKress,2012Zhouetal.,2017China'scoastlineextendsover18,000km,spanningtemperate,subtropical,andtropicalregions.Itincludesrockycoastsandislets,rapidlyaccretingsoftshorelines,mangroves,andcoralreefs.Thereareatotalofca.6500uninhabitedislandsalongtheChinacoastwithintheBohai,Yellow,EastChina,andSouthChinaseasin13dierentpro-vincesordistricts.Theseislandsprovideawidevarietyofpotentialbreedinghabitatsforseabirds.Currently,atotalof77seabirdspecieshavebeenrecordedalongtheChinacoast.Amongthesespecies,37(48%)havebeendocumentedasbreeding(Chenetal.,2018).AswithoftheChinesecrestedtern,mostbreedinghabitatsandcoloniesarefacingseverethreats,includingillegaleggharvest,humandis-turbance,habitatdegradationandloss,marinepollution,decliningfoodavailability,andincreasingfrequencyandseverityoftyphoons.Thesethreatshaveresultedinthewidespreadlossofbreedingcoloniesandpopulationdeclines(Chenetal.,2009Fanetal.,2011Chenetal.,Chenetal.,2018).Therestorationprojectforthecriticallyen-dangeredChinesecrestedternistherstattemptinChinaatactiverestorationofaseabirdpopulation.Itpromisestoprovidemuchin-valuableexperiencefortheconservationofbreedingseabirdsandfa-cilitateseabirdrestorationthroughoutChina.CRediTauthorshipcontributionstatementYiweiLu:Conceptualization,Investigation,Datacuration,Writing-originaldraft.DanielD.Roby:Methodology,Writing-review&editing.ZhongyongFan:Conceptualization,Methodology,Investigation,Datacuration.SimbaChan:Conceptualization,Investigation,Fundingacquisition.DonaldE.Lyons:Conceptualization,Methodology.Investigation,Datacuration.SiyuWang:Investigation,Datacuration,Resources.JiaYang:Investigation,Datacuration,XiaoZhou:Investigation,Datacuration.Investigation,Datacuration.Hsiao-WeiYuan:ShuihuaChen:Conceptualization,Methodology,Writing-review&editing,Supervision,Projectadministration,Fundingacquisition.DeclarationofcompetinginterestTheauthorsdeclarethattheyhavenoknowncompetinginterestsorpersonalrelationshipsthatcouldhaveappearedtoinencetheworkreportedinthispaper.WearegratefultoYunkyoungLeeandQianxunZhengfromtheNationalInstituteofEcologyintheRepublicofKorea,andthePenghuWildBirdSocietyforprovidingdata,andtotheadministrationoftheZhejiangJiushanArchipelagoProvincialMarineEcologicalNatureReserveandtheadministrationoftheZhejiangWuzhishanArchipelagoProvincialBirdNatureReservefortheirassistance.WethankStefanieCollar,QinHuang,PengDing,ChaoChen,HonamLeung,AndyLee,ChunFaiLo,LiweiLiu,XinjieJin,XiaojianYu,YiningChen,JiangWang,PengZhang,XiaosongZhuang,XudongJiang,YanhaoTian,HuaizhenDing,QianmengGuo,KunTan,JieGen,ZhiwenYan,VivianFu,YatTungYu,KirstenBixler,YasukoSuzuki,ZhongdeWang,TingkeLu,JunchengYang,AnkangZhang,ZhijunLou,andGuanChenforassistancewitheldwork,andtoStephenKressandPingDingforadvice.ThisstudywasfundedbytheNationalNaturalScienceFoundationofChina(grantnos.30570251and31572291),theZhejiangTechnologicalResearchProjectforPublicWelfare(LGN18C030001),theNationalKeyR&DProgramofChina(2017YFC1403500),theBiodiversityInvestigation,ObservationandAssessmentProgram(2019-2023)oftheMinistryofEcologyandEnvironmentofChina,ZhejiangRareandEndangeredWildlifeRescueandConservationProject(2017-2020),theEndangeredSpeciesMonitoringFundfromtheStateForestryAdministrationofChina,theOceanParkConservationFoundation(HongKong),thepopularsciencefundfromtheChinaAss

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