59Adulttreescausedensitydependentmortalityi

LETTERAdulttreescausedensity-dependentmortalityinconspecificseedlingsbyregulatingthefrequencyofpathogenicsoilfungiMinxiaLiang,1XubingLiu,1*GregoryS.Gilbert,2,3YiZheng,1ShanLuo,1FengminHuang1andShixiaoYu1*AbstractNegativedensity-dependentseedlingmortalityhasbeenwidelydetectedintropical,subtropicalandtemperateforests,withsoilpathogensasamajordriver.Hereweinvestigatedhowhostden-sityaffectsthecompositionofsoilpathogencommunitiesandconsequentlyinfluencesthestrengthofplant-soilfeedbacks.Infieldcensusesofsix1-hapermanentplots,wefoundthatsurvivalwasmuchlowerfornewlygerminatedseedlingsthatweresurroundedbymoreconspecificadults.Therelativeabundanceofpathogenicfungiinsoilincreasedwithincreasingconspecifictreedensityforfiveofninetreespecies;moresoilpathogensaccumulatedaroundrootswhereadulttreeden-sitywashigher,andthisgreaterpathogenfrequencywasassociatedwithlowerseedlingsurvival.Ourfindingsshowhowtreedensityinfluencespopulationsofsoilpathogens,whichcreatesplant-soilfeedbacksthatcontributetocommunity-levelandpopulation-levelcompensatorytrendsinseedlingsurvival.KeywordsHostdensity,Janzen–Connelleffect,seedlingsurvival,soil-borneplantpathogens,subtropicalforest.EcologyLetters(2016)INTRODUCTIONManytheorieshavebeenproposedaboutwhatmechanismsregulatetheabundanceandcoexistenceofdifferentspeciesinplantcommunities(Chesson2000;Hubbell2001;AllesinaandLevine2011).OneofthemostofteninvokedmechanismsisknownastheJanzen–Connellhypothesis(Janzen1970;Con-nell1971;Comitaetal.2014;Beveretal.2015),whichpro-posesthathost-specificnaturalenemies(predators,herbivoresandpathogens)oftreespeciescouldcausedisproportionatelyhighmortalityofseedlingsathighdensityneartheirparenttrees,makingresourcesavailableforlocallyrarespeciesthatareresistanttothosenaturalenemies,helpingtomaintainhighspeciesdiversityintheforests.AccordingtotheJanzen–Connellhypothesis,thesurvivalprobabilityofseedlingsshouldincreasewithdistancefromparents(distancedepen-dence)anddecreasewithconspecificseedlingdensity(densitydependence).Suchnegativedensity-dependenteffectshavebeenwidelydetectedinforestcommunities.Long-termdemographicdataandshort-termexperimentsshowthatseedlingsurvivalisinverselyrelatedtoconspecificseedlingand/oradultdensity(e.g.Webb&Peart1999;Packer&Clay2000;Comitaetal.2010;Metzetal.2010;Johnsonetal.2012;Jansenetal.2014;Zhuetal.2015).Somestudiesidentifiedsoilpathogensaskeyagentsofdensity-dependenteffectsthroughsoilsterili-sationorfungicidetreatments(Belletal.2006;Bagchietal.2014),andnumerousagriculturalstudieshaveshownhowhostplantdensitycanincreaselossestosoil-bornepathogens(Burdon&Chilvers1975;Renetal.2008).However,toourknowledge,nopreviousstudyinnaturalecosystemshasdirectlymeasuredhowhostdensityaffectsthecompositionofsoilpathogencommunitiesandtheconsequentstrengthofplant-soilfeedbacks.Thepathogenicimpactofsoilmicrobesdiffersconsiderablyamongplantspecies,individualplantsandsites(Augspurger&Kelly1984;Liuetal.2015);sitedifferencesaredrivenbyenvironmentalconditions,functionaldissimilarityamonghosttrees,andspeciescompositionofneighbours.Similarly,soilmicrobialdiversityandcompositionishighlydynamicandvariablealongthosesameaxes(Mitchelletal.2010;Liuetal.2015).Becausedensity-dependentdiseasedevelopmentistheproductofeaseoftransmissionofpathogensamonghostindividuals,variationinthedispersalmodesorkernelsofdif-ferentpathogens(Burdon&Chilvers1975;Fittetal.1987)shouldcreatedifferentialresponsestohostdensityamongpathogens.Theobserveddensityofsomehostsmaybepartlycausedbyplantspeciestraitsthatmakesomespeciesmoresusceptibletopathogensthanothers;seedlingsofrarespeciesappeartobemoresusceptibletodensity-dependentmortalityandnegativesoilfeedbacks(Comitaetal.2010;Manganetal.2010).Finally,becauseadulttreescanbereservoirsforpatho-gensthatarethentransmittedtounderstoryseedlings,thedensityofoverstorytreesmaycontributetodiseaseofconspecificseedlingsintheunderstory(Schweizeretal.2013).Althoughweexpectthatlocalhostswillaffectthecomposi-tionandstructureofthesoilfungalcommunityandthatseed-lingswillsuffermorediseaseathighdensityandwhenclose1DepartmentofEcology,SchoolofLifeSciences/StateKeyLaboratoryofBiocontrol,SunYat-senUniversity,Guangzhou510275,China2EnvironmentalStudiesDepartment,UniversityofCalifornia,1156HighStreet,SantaCruz,CA95064,USA3SmithsonianTropicalResearchInstitute,Balboa,Anc
on,Panama*Correspondence:E-mails:[e-mail]@mail.sysu.edu.cn©2016JohnWiley&SonsLtd/CNRSEcologyLetters,(2016)doi:10.1111/ele.12694toconspecificadults,itremainsunclearhowpredictableandstrongaretheeffectsofadulthostdensityonthesoilpatho-gencommunity.Recentdevelopmentsinnext-generationpar-allelsequencingtechnologyallowunprecedentedviewsintothecompositionanddynamicsofevenunculturablesoilmicrobesthatmaycontributetonegativedensitydependenceinplantcommunities.Inthisstudy,weexaminetherelationshipsamongadulttreedensity,pathogencompositionandseedlingperformance.Wetestforpredictablechangesinfungaldiversityandcomposi-tionalonggradientsofparentaldensityforeachofninetreespecies.Wecomplementedthesesurveyswithashade-houseex