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Whole-Community Facilitation Regulates Biodiversity on Patagonian Rocky Shores
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Title: Whole-Community Facilitation Regulates Biodiversity on Patagonian Rocky Shores
Series Title: Plos One V 6, Issue 10, e24502
Physical Description: Journal Article
Creator: Silliman, Brian
Bertness, Mark D.
Altieri, Andrew H.
Griffin, John N.
Bazterrica, M. Cielo
Hidalgo, Fernando J.
Crain, Caitlin M.
Reyna, Maria V.
Publisher: PloS One
Publication Date: October 13, 2011
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Abstract: Background: Understanding the factors that generate and maintain biodiversity is a central goal in ecology. While positive species interactions (i.e., facilitation) have historically been underemphasized in ecological research, they are increasingly recognized as playing important roles in the evolution and maintenance of biodiversity. Dominant habitat-forming species (foundation species) buffer environmental conditions and can therefore facilitate myriad associated species. Theory predicts that facilitation will be the dominant community-structuring force under harsh environmental conditions, where organisms depend on shelter for survival and predation is diminished. Wind-swept, arid Patagonian rocky shores are one of the most desiccating intertidal rocky shores ever studied, providing an opportunity to test this theory and elucidate the context dependency of facilitation. Methodology/Principal Findings: Surveys across 2100 km of southern Argentinean coastline and experimental manipulations both supported theoretical predictions, with 43 out of 46 species in the animal assemblage obligated to living within the matrices of mussels for protection from potentially lethal desiccation stress and predators having no detectable impact on diversity. Conclusions/Significance: These results provide the first experimental support of long-standing theoretical predictions and reveal that in extreme climates, maintenance of whole-community diversity can be maintained by positive interactions that ameliorate physical stress. These findings have important conservation implications and emphasize that preserving foundation species should be a priority in remediating the biodiversity consequences of global climate change.
Acquisition: Collected for University of Florida's Institutional Repository by the UFIR Self-Submittal tool. Submitted by Brian Silliman.
Publication Status: Published
Funding: A grant from the Mellon Foundation (www.mellon.org) to M. D. Bertness supported this work as well as an NSF award (#0542822) to M. D. Bertness and B. R. Silliman. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Publication of this article was funded in part by the University of Florida Open-Access Publishing Fund.
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This item is licensed with the Creative Commons Attribution License. This license lets others distribute, remix, tweak, and build upon this work, even commercially, as long as they credit the author for the original creation.
Resource Identifier: doi - 10.1371/journal.pone.0024502
System ID: IR00001310:00001

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Whole-CommunityFacilitationRegulatesBiodiversityon PatagonianRockyShoresBrianR.Silliman1* ,MarkD.Bertness2,AndrewH.Altieri2,JohnN.Griffin1,M.CieloBazterrica3, FernandoJ.Hidalgo3,CaitlinM.Crain2,MariaV.Reyna3,41 DepartmentofBiology,UniversityofFlorida,Gainesville,Florida,UnitedStatesofAmerica, 2 DepartmentofEcologyandEvolutionaryBiology,BrownUniversity, Providence,RhodeIsland,UnitedStatesofAmerica, 3 DepartmentofBiology,UniversityofPatagonia,PuertoMadryn,Chibut,Argentina, 4 DepartamentofBiology, NationalUniversityofMardelPlata,MardelPlata,ArgentinaAbstractBackground:Understandingthefactorsthatgenerateandmaintainbiodiversityisacentralgoalinecology.Whilepositive speciesinteractions(i.e.,facilitation)havehistoricallybeenunderemphasizedinecologicalresearch,theyareincreasingly recognizedasplayingimportantrolesintheevolutionandmaintenanceofbiodiversity.Dominanthabitat-formingspecies (foundationspecies)bufferenvironmentalconditionsandcanthereforefacilitatemyriadassociatedspecies.Theorypredicts thatfacilitationwillbethedominantcommunity-structuringforceunderharshenvironmentalconditions,whereorganisms dependonshelterforsurvivalandpredationisdiminished.Wind-swept,aridPatagonianrockyshoresareoneofthemost desiccatingintertidalrockyshoreseverstudied,providinganopportunitytotestthistheoryandelucidatethecontextdependencyoffacilitation.Methodology/PrincipalFindings:Surveysacross2100kmofsouthernArgentineancoastlineandexperimental manipulationsbothsupportedtheoreticalpredictions,with43outof46speciesintheanimalassemblageobligatedto livingwithinthematricesofmusselsforprotectionfrompotentiallylethaldesiccationstressandpredatorshavingno detectableimpactondiversity.Conclusions/Significance:Theseresultsprovidethefirstexperimentalsupportoflong-standingtheoreticalpredictionsand revealthatinextremeclimates,maintenanceofwhole-communitydiversitycanbemaintainedbypositiveinteractionsthat amelioratephysicalstress.Thesefindingshaveimportantconservationimplicationsandemphasizethatpreserving foundationspeciesshouldbeapriorityinremediatingthebiodiversityconsequencesofglobalclimatechange.Citation: SillimanBR,BertnessMD,AltieriAH,GriffinJN,BazterricaMC,etal.(2011)Whole-CommunityFacilitationRegulatesBiodiversityonPatagonianR ocky Shores.PLoSONE6(10):e24502.doi:10.1371/journal.pone.0024502 Editor: SteveVollmer,NortheasternUniversity,UnitedStatesofAmerica Received April4,2011; Accepted August11,2011; Published October13,2011 Copyright: 2011Sillimanetal.Thisisanopen-accessarticledistributedunderthetermsoftheCreativeCommonsAttributionLicense,whichpermits unrestricteduse,distribution,andreproductioninanymedium,providedtheoriginalauthorandsourcearecredited. Funding: AgrantfromtheMellonFoundation(www.mellon.org)toM.D.BertnesssupportedthisworkaswellasanNSFaward( # 0542822)toM.D.Bertness andB.R.Silliman.Thefundershadnoroleinstudydesign,datacollectionandanalysis,decisiontopublish,orpreparationofthemanuscript.Publi cationofthis articlewasfundedinpartbytheUniversityofFloridaOpen-AccessPublishingFund. CompetingInterests: Theauthorshavedeclaredthatnocompetinginterestsexist. *E-mail:brs@ufl.eduIntroductionBiodiversityandthecriticalservicesitprovidesareunderglobal siegefromhumanimpacts[1–4].Climatechange,habitat destruction,over-harvesting,pollution,andspeciesintroductions areleadinganthropogenicforcesdrivingdeclinesinspecies populations,diversityandecosystemservices[1,5–8].Recognition ofthesegrowingthreatstobiodiversityhassparkedadded attentiontobothelucidatingthekeybiologicalandphysical factorsthatstructurelocalspeciesrichnessandevenness[9–10], andthecontext-dependencyoftheirrelativeimpacts.Refined understandingoftheseissueswillbecriticalforpredictingnotonly howbiodiversitywillbeimpactedbyanincreasinglyvariableand changingenvironmentbutalsothepotentiallycompoundingeffects oflosingkeydiversity-regulatingspeciesinteractions[11–12]. Whilenegativespeciesinteractions(e.g.,competition,predation) havelongbeenrecognizedasimportantcontrolsoflocal biodiversity[13–15],theroleofpositiveinteractions(mutualisms, commensalisms;i.e.,facilitation)hashistoricallyreceivedfarless attention[16].Dominanthabitat-formingorganisms(foundation species sensu [17];e.g.,oysters,corals,treesandgrasses)are perhapsthemostconspicuousexamplesofspeciesthatplaycritical rolesinstructuringecologicalcommunitiesviapositiveinteractions.Throughtheformationofphysicalstructureandoften complexinterstitialspaces,foundationspeciesbufferotherspecies againstbioticandabioticstressandproduceanarrayofmicrohabitatsthatcanfacilitatepersistenceofassociatedorganisms,and thereforepromoteincreasedbiodiversityinthecommunitiesthey dominate[17–19].Theimportanceoffoundationspeciesfor communitystructurevariesamongsystemsandcontexts,butcan beconceptualizedasfunctionsoftheproportionofspeciesinthe communitythatarefacilitated(breadth)bythefoundationspecies andthestrengthofthosepositiveinteractions.Atoneendofthis continuum,asmallproportionofspeciesmayderiveweak, facultativebenefitsfromafoundationspecies,andattheother end,whole-communityfacilitationoccursandco-existingspecies areobligatelydependentonafoundationspecies[20].Theory (i.e.,theenvironmentalstressmodel)suggeststhattheimportance PLoSONE|www.plosone.org1October2011|Volume6|Issue10|e24502

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offoundationspecies(breadthandstrengthoffacilitation) increaseswithenvironmentalstress[16,21,22]asmorespecies becomeincreasinglydependentonbufferedconditionsfor survival.Underhighlystressfulenvironmentalconditions,foundationspeciesarethusexpectedtoplayacriticalrolein structuringcommunitiesandmaintainingbiodiversity. Whilefoundationspeciesfacilitateassociatedspecies,their dominanceofprimaryresources(e.g.,space)canalsoresultinthe competitiveexclusionofspecieswithoverlappingresource requirements[13,23].Bysuppressingcompetitivelydominant foundationspecies,‘keystone’predatorshavebeenshownto facilitateco-existenceofcompetitorsinavarietyofecosystems (e.g.,[13,24]).Theimportanceofkeystonepredationinstructuringcommunitiesisexpectedtoshiftwiththelevelofenvironmentalstress;incontrasttofacilitation,itispredictedtodiminish instrengthandimportancewithincreasingenvironmentalstressas predatorsbecomelessabundantandeffective[21]underhigh levelsofphysiologicalstress.Toourknowledgehowever,no studieshaveconcomitantlyexaminedtheimportanceofdiversityfacilitationbyfoundationspeciesandtheeffectsofpredatorsunder highlevelsofphysicalstress.Ifindeedtheimportanceof foundationspeciesbufferingrampsupatthesehigherlevelsof stresswhilekeystonepredationslowsorshutsdown,then conservationmanagerswouldbecompelledtoconsiderallocating increasedeffortintoconservingandrestoringfoundationspeciesin aworldwherehuman-inducedglobalchangesarerapidly ratcheting-upenvironmentalstressors. Weperformedthecurrentstudyontherockyshoresof ArgentineanPatagonia(41–55 u S,63–70 u W).Theseshoresare subjectedtodry,persistentwindsof‘‘TheRoaring40s’’,which flowrelativelyunimpededbylandmassesaroundmuchofthe SouthernHemisphere.Theseintensewindsbringunrivaled climaticconditionstoArgentineanPatagoniashorelineswithdaily averagewindspeeds 30km/h(commonly 60km/h),annual rainfall 18cm/yr,andhumiditytypically 40%[25].Combined,theseatmosphericforcesgenerateadesiccationstress higherthanthatmeasuredonanyotherpreviouslystudiedrocky shoresystem[25].Inlightofthepredictionsofenvironmental stressmodels(seeabove),wehypothesizedthatfacilitationby foundationspeciesratherthanpredationwouldplaythemost criticalroleincontrollingbiodiversityontheexposedrockyshores ofPatagoniawheretheintertidalcommunitiesaresubjectedtoa diverseregimeofstressfulclimaticconditions. InitialobservationsandexperimentsattheNaturalProtected AreaofCaboDosBahias(44 u 44 9 S,65 u 40 9 W),revealedadiverse communityof 40animalspecies,includingmussels,amphipods, isopods,anemones,chitons,snails,crabs,limpets,polycheates, nudibranchs,brittlestars,nemerteans,barnacles,andseastars (Fig.1).Allbutoneoftheseorganisms(aninvasivebarnacle)were foundexclusivelywithinornestledtightlyontopof(2limpets)a biogenicmatrixcreatedbythemussel( Perumytiluspurpuratus ). Withinthisbiomatrix,therewasampleintra-musselspaceforthe shelterandmovementofsymbionts,asitwasbetween2–4shell layersthick,predominantlysediment-free,andcoverednearlythe entireintertidalzone( 95%)ofexposedheadlands,fromthelow tohightidemarks(Fig.1;[25]).Inaddition,wefoundno evidenceforthepresenceofabundantpredators(e.g.,large seastars,crabsanddrillingsnails)ontherockandmusselbed surfacesthataresocommononotherexposedrockyshores throughouttheworld[26–29].Giventheseinitialobservations, andrecentworkshowingtheprominenceofwhole-community facilitationunderhighenvironmentalstress[20,30],wehypothesizedthatthisintertidalmusselcouldbeactingasanobligate foundationspeciesonwind-sweptPatagonianshorelinesby providingcommunity-widerefugiafrompotentiallylethalclimaticstressors. Tobegintotestourhypothesisthatfacilitationbymusselbeds (viadesiccationstressamelioration)regulateslocalbiodiversityon ArgentineanPatagoniarockyshores,weinitiallyusedan observational,comparativeapproachandsampledspeciesdiversityinthemusselmatrixandadjacentbareareasinhighandlow intertidalhabitatsattwowave-exposedheadlandsinCaboDos Bahiasand8otherexposedrockycoastsitesalongthePatagonian coast,spanning 2100km.Toexperimentallytestourhypothesis, weconductedbothfieldsurvivorship(with7species)and disturbance-recovery(withtheentirecommunity)experiments bothwithandwithoutmusselbedsandconsumersatreplicated exposedrockyshoresitesinCaboDosBahiasfrom2003–2005. Totesthowpredators(seastars)withinthemusselmatriximpact communitydevelopment,weperformeda1.5yrseastarremoval experimentatbothCaboDosBahiassitesinthelowintertidal zonewhereseastarabundanceishighest.Finallytotesthow musselsmitigatedesiccationstressonPatagonianshoresandto parseouttherelativeimportanceofsunvs.windblockbymussels inreducingphysicalstress,weperformedasponge-evaporation studyattheinterfacebetweenthemidandlowintertidalzonesat twoexposedheadlandsitesintheCaboDosBahiaspreserve.MaterialsandMethods SiteDescriptionWeobtainedpermitsforourworkonArgentineanshorelines fromtheArgentineanDepartmentofNationalParks.Foracopy ofthepermit(nopermitnumberwasissued),pleasecontactF. Hidalgo(fernandohidalgo2003@yahoo.com.ar).Theprimarysite ofthisstudywasintheNaturalProtectedAreaof‘‘CaboDos Bahias’’(44 u 44 9 S,65 u 40 9 W),onthenorthendoftheGulfofSan Jorge,Patagonia,Argentina.Thisprotectedareaisaland-to-sea reservesituatedalongthePatagoniansteppeandcharacterizedby anaridanddesert-likeclimatewithlowprecipitation( 18cm/ yr),meantemperaturesof12.5C u (maximumof39C u and minimumof 2 7.5C u ),andstrong,dry,southwestwinds,with meanvelocitiesof25–35km/handmaximumsroutinely 60km/h.Desiccationstressisaccordinglysevereandamong thehighestrecordedforrockyshorecommunities[25].Tidesare semi-diurnal,withaverageamplitudeof3.4m,andwavestresson exposedheadlandsiscomparabletothatexperiencedonrocky shoresonthewestcoastoftheU.S. Insummer2002,weexploredtherockyshorelinesofCaboDos Bahias.Fromthehightolowintertidalontheexposedheadlands, 95%oftherockyshore’ssurfacewascoveredbyonespecies,the tiny( 2cm)mussel, Perumytiluspurpuratus (Fig.1;[25]).The diverseintertidallifeandzonationcharacteristicofmostexposed rockyshoresystemsthroughouttheworldwerenoticeablymissing, aswerelarge,mobileinvertebratepredators.However,embedded andlivingwithinthe2–3mussel-thick,rock-coveringbio-matrix, wefoundadiverseassemblagecompletewithdiminutive representatives(0.5–3cminlength;seeFig.2A)ofthemost commonrockyshoreanimalgroups(seeabove).Uponexposureto theintensePatagonianwinds,crabs,polycheatesandchitonslaid onnearbybarerockquicklydied,whilethebodymassofseastars recedednoticeably.Basedonthesefieldobservations,we hypothesizedthat:(1)thethickmusselmatrixcoveringthe exposedrockyshoresofPatagonia,Argentinaprotectsassociated animalsfromlethal,wind-drivendesiccationstressand(2) maintenanceofbiodiversityofrockyshoreinvertebratesdepends exclusivelyonfacilitationbyfoundationspecies,ratherthan keystonepredation,underintenseclimatestress.BiodiversityRegulationunderHighStress PLoSONE|www.plosone.org2October2011|Volume6|Issue10|e24502

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GeneralitySurveysTotestthegeneralityofourinitialobservationsatCaboDos Bahiasthatrockyshoreinvertebratecommunitiesaredependent onlivinginsidethemusselmatrixforpersistence,wesurveyed8 rockycoastsitesfromsoutherntonorthernPatagonia,spanning over2100kminrange.OurinitialsitewasnearthecityofRiode GallegosadjoiningtotheStraightsofMagellaninsouthern Patagonia.Ourmostnorthernsitewas 200kmnorthof Viedma,acityinnorthernPatagonia.Exactlatitudesaregiven inFig.2,andeachrepresentedanunshaded,basalticrockor sandstoneoutcropping.Ateachsite,werandomlyplacedandthen surveyed10,50 6 50cmquadratsinbothmusselandnon-mussel occupiedareasatornearmeanlowwater.Fornon-mussel coveredareas(whichwereuncommon),werecordedallspecies present,thedensitiesofthosespeciesandtheaveragesizeofthe firstfiveindividualsofeachspeciescollected.Formussel-covered areas,themusselmatrixwascarefullyexcavatedanddissected, andallcontentsputintodishpansandsortedtodetermineall speciespresent,theirdensities,andaveragesize(i.e.,meanlength offirstfiveindividuals).SurvivorshipexperimentsTotest:(1)thehypothesisthatmusselsfacilitateanimal persistenceinthePatagonianrockyintertidaland(2)therelative roleofdesiccationvs.consumerprotectionprovidedbymusselsin thisfacilitativeprocess(althoughwedidnotfindobservational evidencethatmusselsprotectedmatrixassociatesfrompredation, wetestedthismechanismaswellbecauseitisverycommonin othermussel-dominatedsystems),weperformedcontrolled experimentsatbothexposedheadlandsitesandoneadditional site 1kmawayinthelatespringof2003.Theexperiment consistedofsixtreatments(n=15replicatesofeachtreatment):1) musselmatrixremoval(bareareas),2)musselmatrixremoval +consumerexclusion(bareareas + cage),3)musselmatrixremoval + cagecontrol(bareareas + cagecontrols),4)musselmatrix removal + consumerexclusion + musselmatrix(bareareas + cagefull ofmussels),5)musselmatrixremoval + consumerexclusion + mussel sun-blockmimic(bareareas + cagewithshade),and6)mussel matrixremoval + consumerexclusion + musselsun-and-wind-block mimic(bareareas + cagewithmussel-sizedrocksorsponge).Bare areashadnocagestructures.Totalconsumerremoval(i.e.,caged) Figure1.Imagesofhabitatcreatedbymussels,andtheanimalsshelteredwithin. (A)Seacapeviewofmussel-dominated,Patagonian exposedrockyshores.(B)Typicaldiminutive,invertebratespecieslivingonlywithinthemusselmatrix. doi:10.1371/journal.pone.0024502.g001 BiodiversityRegulationunderHighStress PLoSONE|www.plosone.org3October2011|Volume6|Issue10|e24502

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plotswerecoveredwithastainless-steelmesh(5mm),consumer exclusioncage(15 6 15 6 4cm,LxWxH)boltedtothesubstrate withastainless-steel,centeredbolt.Cagecontrolplotswere coveredwithsimilarcages,butwithtwosidesremovedtogive consumersaccess.Shadedplotshadcageswithtwolayersof 0.62cm2Vexarmeshstrappedtothetop.Forbareareas + cage withmoistspongetreatments,thematrix-mimickingspongewas thesamesizeasthecageand,beforebeingplacedinthecage,it wassoakedinseawaterandthensqueezeddrip-drytomimic climatebufferingbymussels.Forbareareas + cagefullofmussel treatments,cageswerepackedfullofexcavatedmusselsandthen fastenedtotherock.Liveorganismsinallplotswereinitially scrapedfromthesurfacewithpaintscrapers.Forthisstudy,we usedthemostabundantorganismsinthesystemamenableto transplanting:limpets,snails,chitons,scaleworms,seastars, anemones(attachedtomusselshells)andcrabs.Becauseall organismsmoved 6cmafterbeingplacedontherocksurfacein apreliminarystudy(30minutes),wedidnotuselineandglueto attachanimalstothesurfaceandthusavoidedassociatedartifacts withlinetethering.Instead,wesimplyplacedeachorganisminits assignedtreatmentfreeofartificialattachment.Experimental organismswereremovedfromanearbymusselmatrix onehour beforethestudy,immediatelyplacedinseawater,andkept immerseduntilbeingplacedintoassignedtreatments.Thestudy ranfortheentirelengthofdiurnallowtideineachzone( 3hours inthelowintertidaland5hoursinthehighintertidal).Aftersetup( 30minutes),weleftthesitescompletelytoallowforanybird predationthatmayoccurasbothgullsandoystercatchers occasionallyvisitthesesites( 1seagull/500mofexposed shorelineand1pairofoystercatchersateachexposedheadland site,Sillimanetal., pers.obs. ).However,beforeleavingthesitesand beforetheexperimentcouldbefullyset-up,allcrabs,seastars,and Figure2.Diversityandstructureoftheintertidalcommunitydependentonmusselmatrixforshelterfromharshclimate. (A)Average bodylengthofthemostcommoninvertebratesfoundlivinginsideorembeddednextto(onlylimpets)musselbeds.Scientificnamesofspecies measured,withx-axislabelsinparentheses,were: Anasteriasminuta (seastar), Plaxiphoraaurata (chiton), Pareuthriaplumbea (snaila), Trophon geversianus (snailb),juvenile Perumytiluspurpuratus (mussel), Exosphaeromalanceolata (isopod),multiplespeciesincluding HalosyndnaPatagonica Mapphysaaenea and Platynereismagalhaensis (scaleworm),speciesnamesofamphipodspecies a and b areunknown, Siphonarialessoni (limpeta), Nacellamagellanica (limpetb), Cyrtograpsusaltimanus and Halicarcinusplatinus (crab);.(B)Speciesrichnessofinvertebratesfoundlivinginsidemussel matrixandonbaresurfacesat8differentsitesspanning2100kmofArgentineancoastline,fromNorthernPatagoniatoRiodeGallegos,Tierradel Fuego.(C)Cumulativespeciesrichnessatthosesamesites.Barsare + / 2 1SE. doi:10.1371/journal.pone.0024502.g002 BiodiversityRegulationunderHighStress PLoSONE|www.plosone.org4October2011|Volume6|Issue10|e24502

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anemonesappearedextremelydesiccatedanddead(e.g.,crabs couldnolongermovetheirlegsafter 10minutesandtheirdorsal carapacehadsunkin).Attheendoftheexperiment,werecorded whetherorganismswerealiveordead.Finally,werecorded changeindrip-free,wetweightofpolycheates,seastars,andcrabs overthelengthofthestudyusingabattery-poweredscaleinthe field.Foranalysis,weusedsurvivorship(%ofanimalssurvivingin the15replicatesateachofthethreesites)asonedatapointvalue forthatsiteandthencomparedmeansurvivorshipacross treatmentsatthethreesites.Thus,forthisexperiment,n=3.Disturbance-RecoveryExperimentsTotest:(1)thehypothesisthatmusselbedsfacilitaterockyshore communitydevelopmentand(2)therelativeroleofdesiccationvs. predationprotectionprovidedbymusselsinthisfacilitativeprocess, weperformeddisturbance-recoveryexperimentsatbothexposed headlandsitesinlatespringof2002.Theexperimentconsistedof sixtreatments(n=8pertreatment):1)musselmatrixremoval/ disturbance(bareareas),2)musselmatrixremoval/disturbance + consumerexclusion(bareareas + cage),3)musselmatrixremoval/ disturbance + cagecontrol(bareareas + cagecontrols),4)mussel matrixremoval/disturbance + consumerexclusion + mussels(bare areas + cagefullofmussels),5)musselmatrixremoval/disturbance + consumerexclusion + musselsun-blockmimic(bareareas + cage withshade),and6)musselmatrixremoval/disturbance + consumer exclusion + musselsun-and-wind-blockmimic(bareareas + cagewith mussel-sizedrocks).Mussel-sizedrockswerecollectedfromanearby field.Beforeuse,musselswerethoroughlyrinsedinfreshwaterand onlymusselswithin0.2cmofthemeanwidthandlengthofadult musselswhereusedinthecagingexperimentasmusselmimics. Rockswerepackedtightenoughinsidecagessothattherewasno movementofrockswhenwavescrashedovertopofthecages,which mimickedconditionsinmusseltreatments.Bareareashadnocage structures.Totalconsumerremovalplotswerecoveredwitha stainless-steelmesh(5mm),consumer-exclusioncage(15 6 15 6 4cm, LxWxH)boltedtothesubstratewithastainless-steel,centeredbolt. Cagecontrolplotswerecoveredwithsimilarcages,butwithtwosides removedtogivepredatorsaccess.Shadedplotshadcageswithtwo layersof0.62cm2vexarmeshstrappedtothetop.Rocksusedinthe mussel-sizedrockcageweretakenfromanearbyroad.Cageswith musselswerestockedwithmusselsthathadbeencleanedwith seawaterindishpansandcleanedofallassociatedinvertebrates.Live organismsinallplotswereinitiallyscrapedfromthesurfacewith metalpaint-scrapersandrocksurfacescleanedwithablow-torch.All plotswereestablishedinNovemberof2002,andtheexperimentran fortwoyears.Cageswerecheckedandmaintainedmonthlyfor limpetinvasionandfoulingaspreviouslydescribed.Attheendofthe experiment,werecordedspeciesrichnessineachplot. Totesthowseastarsimpactdiversityofinvertebrateswithinthe musselmatrix,weperformeda1.5yrpredatorremoval experimentatbothexposedsitesattheinterfacebetweenthe lowandmidintertidalzoneswhereseastarabundancewashighest. Theexperimentconsistedoftwotreatments(n=8pertreatment): 1)controlmussels(cage + mussels)and2)seastarremoval (cage + mussels 2 seastars).Ateachsite,16–20 6 20cmmusselplots wereexcavated,andallseastarswereremovedfromtheexcavated mussels.Allotherinvertebrateswereretained.Excavatedmussels withassociatedassemblageswerethenputintocages(asdescribed above).Inhalfofthe16cages,4seastarswereaddedtothemussel matrixtomimicnaturaldensities.The16cagesfullofmusselsand associatedcommunitieswerethencarefullyfastenedtotherockas describedabovesothatnoanimalsescaped.Seastardensities werecheckevery2months.Onaverage,0.42 + / 2 0.12small seastars( 1cminlength)wereremovedfromexclusionplots,and 0.56 + / 2 0.39smallseastarsfrominclusionplotstomaintain treatmentdensities.Theexperimentranfor1.5yearsand,atthe endoftheexperiment,allcagedplotswereexcavatedandspecies richnessanddensitieswererecorded.DesiccationassaysTotesthowmusselsmitigatedesiccationstressonPatagonian rockyshoresandtoparseouttherelativeimportanceoftheeffectsof sunblockandsun + windblockbymusselsinreducingdesiccation stress,weperformedasponge-evaporationstudyattheinterface betweenthemidandlowintertidalzonesattwoexposedheadland sitesintheCaboDosBahiaspreserve.Theheadlandsareseparated by 1km,andweconductedtheexperimentinboththespringand fallof2003.Theexperimentconsistedoffiverandomlyassigned treatments(n=8/treatment):1)bareareas(controls),2)bare areas + cagewithshade(sunblockonly),3)bareareas + cage(asa cagecontrol),4)bareareas + cagewithmoistsponge(sunblock + wind block),and5)bareareas + cagefullofmussels.Barecontrolareashad nocagestructures.Cagedplotswerecoveredwithastainlesssteel mesh(5mm)cage(15 6 15 6 4cm,LxWxH)boltedtothesubstrate withastainless-steel,centeredbolt.Shadedplotshadcageswithtwo layersof0.62cm2vexarmeshstrappedtothecagetop.Forbare areas + cagewithmoistspongetreatments,thematrix-mimicking spongewasthesamesizeasthecageand,beforebeingplacedinthe cage,itwassoakedinseawaterandthensqueezeddrip-drytomimic climatebufferingbymussels.Forbareareas + cagefullofmussel treatments,cageswerepackedfullofexcavatedmusselsandthen fastenedtotherock.Liveorganismsinallplotswereinitiallyremoved fromthesurfacewithmetalpaint-scrapersandwirebrushes.Onthe rocksurfaceineachtreatmentatthebeginningofthestudy,we placedanumbered,wet,5 6 10 6 2cmsponge.Thedryandwet weightofeachspongewasdeterminedbeforetheexperiment.The studyranfor2.5honacleardaywith 10%cloudcoverandwith anaveragewindspeedof43.2km/h + / 2 5.4km.After2.5h,each spongewascollectedandimmediatelyweighedinthefieldwitha battery-poweredscale.Percentwaterlosswasdeterminedby:[(initial wetweight 2 finalwetweight)/(initialwetweight 2 dryweight)]*100.StatisticalanalysesLatitudinalsurveydata(bodylengthandrichness)were analyzedwithatwo-wayANOVA(latitude 6 substratetype)or withchisquareanalyses(cumulativerichness-latitude 6 substrate type)anddesiccationdatawithatwo-wayANOVA(season 6 cage type).DatafromtetheringexperimentswereanalyzedusingatwowayANOVA(tidalelevation 6 cagetype).Cagingdatafromthe disturbancerecoveryexperimentwereanalyzedusingathree-way (site 6 zone 6 cagetype)andfromtheseastarpredationexperiment usingatwo-wayANOVA(predatorpresence 6 site).Inanalyses, dataeitherexhibitedhomogeneityofvarianceandwerenormally distributedorweretransformedusinglogtransformationsfor assumptionconformity.Onlylinearcontrastswerecompared, usingTukey’sposthoctest.Becausewefoundnosignificanteffect ofsite(P 0.26allcases)onanyresponsevariableinall experiments,datawerepooledacrossallsitesforallexperiments.Results GeneralitySurveysAnalysisofourspeciesrichnesssurveydatarevealedthatthere wasnointeractionbetweenfactors(musselpresence 6 latitude; P 0.35)orimpactoflatitude(P 0.17),onlyasignificanteffectof musselpresence(P 0.01).Ateachsite,onaverage,28.9species werefoundwithinmusselbedswhileonly2.7specieswerefound onrocksurfacesfreeofmussels(Fig.2).ThenumberofspeciesperBiodiversityRegulationunderHighStress PLoSONE|www.plosone.org5October2011|Volume6|Issue10|e24502

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quadratwasnearly6 6 higherwithinmusselbeds(Fig.2).Species abundancedifferencesbetweenbarerockandmussel-covered areaswereevenmoredramaticthanspeciesrichness(Fig.3).As wasthecaseforspeciesrichness,forspeciesabundances,therewas nointeractionbetweenfactors(P 0.42)orimpactoflatitude (P 0.19),onlyasignificanteffectofmusselpresence(P 0.01). Speciesdensitieswithinmusselbedsrangedfrom2–7640ind./m2, whileonthebaresurfacestheyrangedfrom0–262ind./m2(invasivebarnaclesprimarily,andsomelimpets).Typicalrocky shoreconsumersthatforageonbarerockandovertopmusselbeds suchasseastars,chitons,crabs,andshell-drillingsnailswereonly foundwithinthemusselmatrix(Fig.2,3),whileonly2limpet species(whichspendmostoftheirtimeontheshorenestledinto theedgeofthemusselmatrixandforageonopenrockspace duringhightides),andaninvasivebarnacle,occurredin significantnumbersoutsideofmusselbeds(Fig.3).The associationalrelianceoflocalspeciesrichnessandabundanceon musselbedswasconsistentacrossallintertidalheights(Figs.2,3). Bodysizemeasurementsrevealedthatallorganismswerelessthan 2.5cminmeanbodylengthandthedominantadultseastarand crabwereonaverage1.83and0.84cmlong,respectively(Fig.2A).SurvivorshipAssaysInoursurvivorshipexperiments,forlimpets,therewasnoeffect oftidalelevationorcagingtreatmentonsurvivorship(P 0.33) andsurvivorshipwas100%acrossalltreatments(Fig.4).For chitons,thereweresignificantmaineffects(P 0.05,bothcases)of cagingandtidalelevation,withchitonssurvivingbetteratlow elevationsandundercageswithaddedshade,mussels,orsponges. Forscaleworms,snails,seastars,anemonesandcrabstherewas onlyasignificanteffectofcagingtreatment(P 0.01,allcases; Fig.4),withsurvivorshipbeinghigherundercageswithadded shade,mussels,orsponges.Importantly,cageswithshadeincreased survivorshipforallanimals(exceptlimpets)onlymoderately,from0 Figure3.Densityofinvertebratesfoundlivinginsidemusselmatrixatthemainexperimentalsites. Densitiesofamphipods,snailsand limpetsallconsistedofaggregatesof2species(i.e., a and b );scientificnamesoftaxanotfoundinFig.2are Oulactismuscosa Aulactiniasp. and Phymactissp. (anemone), Mytilusedulis (mussel)Nemertea(ribbonworm),Nudibranchia(nudibranchs),Ophiuiridea(brittlestar), Balanusglandula and B.laevis (barnacle).Allotherx-axislabelscorresponddirectlytospeciesnameslistedinFig.2legend.Barsare + / 2 1SE. doi:10.1371/journal.pone.0024502.g003 BiodiversityRegulationunderHighStress PLoSONE|www.plosone.org6October2011|Volume6|Issue10|e24502

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to 10–40%,whileaddingeithermusselsoramoistspongetocages placedontopoftetheredorganismselevatedsurvivorshiptonearly 100%forallnon-limpetorganisms(Fig.4).Fordrip-freeweight changes,polycheates,seastars,andcrabsalllostgreaterthan60% oftheirbodyweightafter1.5hours(P 0.01).Disturbance-recoveryandPredationExperimentsInour2-yeardisturbance-recoveryexperiment,therewasa significanteffectofbothcagetype(P 0.001)andzone(P 0.05) onspeciesrichness,butnointeraction(Fig.5A).Speciesrichness increasedwithincreasingprotectionfromclimaticextremes,while therewasnopositiveeffectofremovingconsumersonrichness thatcouldnotbeexplainedbythepositiveeffectsofphysical-stress bufferingaffordedbycagestructure(cagevs.cagecontrols). Cage + shadingtreatmentsprovidednopositiveeffectonspecies richness,anditwasonlywhencageswerefilledwiththreedimensionalobjects(musselsandrocks)didthecommunity significantlyrecoverfromdisturbance.Acrossalltreatments, beinglocatedatlowerelevationsincreasedspeciesrichnessby 25%.After1.5years,therewasnoeffectofseastarremoval (P 0.48)onspeciesrichnessinsidethemusselmatrix(Fig.5B).DesiccationstresstestFortheevaporationpotentialexperiment,therewasa significanteffectofcagetype(P 0.001)andnoeffectofseason (P 0.46).Lossofwaterfromsmallwetspongesplacedinthe intertidalwasintense( 90%)inplotswithnoprotectionfrom windorsun.Bycontrast,desiccationstresswasdramatically reducedwithinthemusselmatrix,aswellasinthemusselbed mimicofalargewetsponge.Inshadingplots,waterlosswas reducedbyonly 10%,revealingthatprimarylossofwaterwas drivenbywind,notsunstress. Figure4.Survivorshipassaysdemonstratingthedependenceofmarineinvertebratesonfacilitationbymussels. Effectsofmussel presenceandmimicsofthepositiveeffectsofmusselpresence(predatoranddesiccationrefuge)onsurvivorshipofthemostcommoninvertebrates livinginthemusselmatrixonPatagonianexposedshorelinesinboththe(A)highand(B)lowintertidal.Invertebratetaxaconsistedofsingleor multiplespecies.Barsare + / 2 1SE. doi:10.1371/journal.pone.0024502.g004 BiodiversityRegulationunderHighStress PLoSONE|www.plosone.org7October2011|Volume6|Issue10|e24502

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DiscussionOursurveysacross15 u oflatitudeofwind-sweptPatagoniarocky shorelinesrevealedastrikingexampleofwhole-community facilitation.Diversitywas20-foldhigherinplotswheremusselswere present;intheabsenceofmussels,therockysubstratewasvirtually bare.Thiswhole-community,mussel-beddiversityrelationship occurredacrosstheentireintertidalzoneanddidnotdiminish acrossthedecreasingevaporativestressgradientfromhightolow intertidalthatcharacterizeswave-exposed,rockyshoresystems(i.e., decreasingdesiccationstressatlowerelevations).Oursurveyalso revealedthatthedominantmusselanditsinvertebrateassociatesare extremelydiminutiveinbodysize(Fig.2-allorganismswereless than2.5cminmeanbodylength),anorderofmagnitudesmaller thanotherrockyshoreassemblageswithsimilartaxa[31]. Concomitantwithreducedbodysizeandtheobservedpositive musselbed–speciesdiversityandabundanceassociation(Fig.2,3), desiccationstressinthissystemisthehighesteverrecordedforany rockyintertidalsystem[25].Experimentalmanipulationofsunand windexposureinbothhighandlowintertidalhabitatsduringspring andfallof2003combinedwithmathematicalestimatesof desiccationstressfromdailylocalweatherdataovera3-yearperiod [25]revealedthattheprimaryforcedrivingevaporativewaterlossin thissystemwasexposuretolow-humidity,high-intensitywinds ( 90%ofevaporationduetowinds),notsun(Fig.6). Experimentalexaminationofthepositivemusselbed–local diversityassociationconfirmedourhypothesesthatmussels facilitatetheentirelocalcommunitybybufferingagainstharsh, lethalclimaticconditions.Survivalassaysrevealedthatambient desiccationstresswasquicklylethaltonativeintertidalanimals andthatdiversitywasdependentonmusselfacilitation(Fig.4). Localcrabs,seastars,chitons,scaleworms,andanemonesalldied within5–180minutesofairexposureonrocksurfaceswithout mussels.Ourresultsshowthatexcludingconsumershadnoimpact onthesurvivorshipoforganisms,astherewasnodifference betweencagedandopenareasthatcouldnotbeexplainedbythe small,positiveeffectsofcaginggeneratedbyslighthabitat ameliorationprovidedbycagecontrols.Incontrast,when intertidalanimalswerecoveredwithmussels,ormoistsponges, survivorshipwasnearly100%forallspecies,atbothhighandlow elevations,demonstratingthatwaterlossistheprimarymechanismleadingtodeathofexposedinvertebrates. Likepersistence,communityresilience(abilitytorecoverfrom disturbance)wascompletelydependentonfacilitationbymussels (Fig.5A).Aftertwoyears,nosignificantrecoverytookplacein bareplotswithoutmussels.Onlythefewspeciescommonlyfound outsidemusselbeds(e.g.barnaclesandlimpets)werefoundinbare areas,huddledonmusselmatrixedgesoutsideofthedisturbance plot.Bycontrast,inmusselareasclearedofinterstitialorganisms, diversityaftertwoyearsofrecoverywas6 6 timeshigher,with 17.8speciesperplot.Cumulatively,acrossdisturbance-recovery plots,5specieswerefoundinbareareas,whereas36werefoundin musseltreatments.Removingallconsumershadnoimpacton communityrecovery(Fig.5A),exceptforthesmallbenefitsthat cage-edgesprovidedinfullcagesandcagecontrolsinreducing desiccationstress[25].Shadingalsohadnoimpactoncommunity recovery(Fig.5A).Mussel-mimickingrocks,however,increased speciesrichnessby4 6 ,nearlythesamepositiveeffectgenerated bythemusselbed.Thiscontrastingresultofnoimpactofshading butstrong,positiveimpactsofbothmusselbedsandmusselmimicscombinedwiththeresultsfromevaporation-potential experiments(Fig.6)andcalculations[25]demonstratesthat crevicespaceamongmusselsfacilitatescommunitydevelopment Figure5.Importanceoffacilitationbymusselsforthe resilienceandpersistenceofPatagonianintertidalrockyshore community. (A)Effectsofmusselpresenceandmimicsofthepositive effectsofmusselpresence(i.e.,refugefrompredatorsanddesiccation) onrecoveryofinvertebratecommunityafterexperimentaldisturbance. (B)Effectofseastarremovalondiversityofinterstitialinvertebratesin musselbeds.(C)Schematicoftrophiccascadenetworkthatregulates diversityonmoist,rockyshoresthroughouttheworld.(D)Schematicof shiftinbiodiversitymaintenancetoafacilitationnetworkundera regimeofintenseclimaticstress.Barsare + / 2 1SE. doi:10.1371/journal.pone.0024502.g005 Figure6.Facilitativeeffectsofmusselandmusselmimicson reducingdesiccationstress. Barsare + / 2 1SE. doi:10.1371/journal.pone.0024502.g006 BiodiversityRegulationunderHighStress PLoSONE|www.plosone.org8October2011|Volume6|Issue10|e24502

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bydecreasinglethaldesiccationstressgeneratedbythedry, intense,Patagonianwinds. Experimentalremovalofdiminutivepredatoryseastarsfromthe musselmatrixalsohadnodetectableeffectonspeciesrichness (Fig.5B),confirmingthatundertheintensifiedclimaticstressatour studysitespredationisnotplayinganimportantdiversity-regulating role.Thisresult,togetherwitharecentstudyonthesesame shorelinesshowingthatthePatagonianmusselsexperiencealmost nopredationovertheentireyear[32],revealsthatpredation pressureonmusselsisweakinthisintertidalsystem.Indeed,theonly native,marinepredatorsfoundtoforageintheintertidal,andthen onlyduringhightides,weretinydecapodcrabs(1–2cminbody length)andntothenidfish( 9cminbodylength);examinationof theseanimals’gutcontentsrevealedamphipodsandpolycheates, andnotmussels,weretheirprimarysourceofnutrition.Our observationoftheabsenceofmobileconsumersfromthiscoastline couldhavemultipleandpotentiallyinteractingcauses.Intense physicalstresscouldpreventmanyrockyshorepredators(e.g.,large seastars)fromemergingontheshorelinesorpreventtheir establishmentafterrecruitment.Alternatively,intertidalpredators couldbeabsentfromthissystemduetohistoricalcontingencies(L OrensanzandM.Adami,unpub.manus.).Finally,large,sub-tidal mammalian(sealions,porpoises),bird(penguins),molluscan (octopus)andfishpredatorsintheareacouldsuppressdensitiesof intertidalpredators,suchascrabsandseastars.Despitefindingno experimentalevidenceforstrongpredatoreffectsinourstudy systemandnoobservationalevidenceforthepresenceofeffective intertidalpredatorsoverlargespatialscalesinoursurveys,we cautionagainstalarge-scalegeneralizationthatpredationis functionallyabsenceonPatagonianshorelines.Indeed,this hypothesisneedstobetestedexperimentallyacrossmanysites beforesuchbroadconclusionscanbemade.Inotherintertidal Argentiniancommunities,forinstance,consumershavebeenshown tobeimportantoverlargespatialscales[33,34]. Musselbedsonwave-exposedrockyshoresworldwidehavebeen showntohavebothsuppressiveandfacilitativeeffectsonlocal diversity.Forexample,intheabsenceofkeystonepredationbysea starsmusselbedscompetitivelydisplaceothercommonintertidal space-holderssuchasbarnacles,anemones,andalgaebypreempting space,whichleadstonegativeimpactsofmusselsonthediversityof otherdominantspace-holdingspecies[13].Byprovidinghabitatand protectionfromdesiccation,musselbedsalsofacilitateorganismslike worms,echinoderms,andcnidarians,extendingtheirdistributions higherintotheintertidalzonebyreducingdesiccationstress[35]. Onwind-sweptPatagonianshorelines,ourexperimentsandlargescalesurveyrevealthatcompetitiveexclusionofotherspeciesby musselsbecomesirrelevantbecausemusselsarethe only dominant spaceholdercapableofenduringthephysicalconditions;indeed, virtuallyallotherintertidalorganismsarecompletelydependenton musselsforprotectionfromlethaldesiccationstressfortheir persistence(evenlimpetscannotsurvivethedryingwindswithout accesstomusselmatrixedgesoverextendedperiods)[36]. Furthermore,predationpressureatourtwostudysitesisweakeven inthepresenceofbufferedconditionsprovidedbymussels.Our resultsthereforeagreewithpredictionsofenvironmentalstress models[21,22,37]andsuggestthatwithincreasinglysevereclimatic conditions,localdiversitymaintenancetendstowardswholecommunityfacilitationwhiletheroleofpredationisdiminished. Mutualisticandfacilitativeinteractionsthatformnetworks(3or moreinteractingspecies)arekeyforgeneratingandmaintaining patternsofbiodiversity[38,39],andconsumershavethepotentialto dictatetherelativeimportanceofthesepositiveinteractionnetworks forthemaintenanceofdiversity[40].Ourexperimentalworkreveals thepersistenceofadiversecommunityonexposed,aridPatagonian shorelinesdespitethefunctionalabsenceofkeystonepredation.Our findingsprovideexperimentalevidencefortheoreticalpredictions thatbasalspeciesinecologicalnetworkscanstillpersistwhennot regulatedbypredation,competition,orresourceavailability[41],as thediverseinhabitantsofmusselbeds(chitons,anemones, amphipodsetc.)onexposed,Patagonianshorelinesareinstead controlledbyharshclimacticconditionsandthepositiveinteraction networkthatamelioratesthoseconditions.Physicalfactorshavebeen showntodampenthestrengthofkeystonepredation[21,42].Our studyexpandsthisknowledgetoshowthatclimacticextremescan notonlysuppresskeystonepredationentirely,butalsofosterthe dominantroleoffacilitationincommunityorganizationand diversitymaintenance(Fig.5C,D). Overthepastdecade,ecologistshaverecognizedthatfoundation speciesameliorationofphysicalstressmaintainslocaldiversityin manynaturalcommunitiesthataresubjecttocontinuinghuman impact(e.g.,saltmarshes,coralreefs,forests)[43].Failureto appreciatetheincreasinglyimportantrolethatfoundationspecies willplayinmaintaininglocalbiodiversityasclimaticstress intensifiescouldhavedireconsequencesforthepersistenceand resilienceofnaturalecosystems.Recentclimaticmodelspredicta doublingofthemostrecent,best-estimatesofglobaltemperature increasesoverthenext100years[44].Thissteepandrapid temperatureriseisexpectedtoincreaseevaporationandwindstress inmanynaturalandmanmadeecosystemsaroundtheglobe, includingeconomicallyimportantshorelinecommunities,suchas dunes,mangroves,andmarshesandinlandcommunities,suchas grasslands,farmlandsandsavannahs.Ourresultssuggestthat conservationeffortsintheseareaswhereincreasedclimatestressis expectedshouldincorporateandpromotepositivespeciesinteractions,especiallywhole-communityfacilitationbyfoundation species,thatcanbufferbiodiversityfromharshphysicalconditions.AcknowledgmentsWethankChristineAngelini,RobertPaine,JoseOrensanzandMichael McCoyfortheirfeedbackonearlierversionsofthiswork.Wealsothank JoseOrensanzforlogisticalsupportwhileworkinginPatagonia.AuthorContributionsConceivedanddesignedtheexperiments:BRSMDB.Performedthe experiments:BRSMDBMCBFJHMVRCMC.Analyzedthedata:BRS. 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