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ORIGINALPAPER

Status,trendsand driversofkelp forestsinEurope:

anexpertassessment

R.M. Arau´jo

1

J.Assis

2

R.Aguillar

3

L.Airoldi

4

I.Ba´rbara

5

I.Bartsch

6

T.Bekkby

7

H.Christie

7

D.Davoult

8,9

S.Derrien-Courtel

10

C.Fernandez

11

S.Fredriksen

12

F.Gevaert

13,14

H.Gundersen

7

A.LeGal

10

L.Le´veˆque

9,15

N.Mieszkowska

16

K.M.Norderhaug

7,12

P.Oliveira

1

A.Puente

17

J.M.Rico

11

E.Rinde

7

H.Schubert

18

E.M.Strain

19

M.Valero

9,20

F.Viard

8,9

I.Sousa-Pinto

1,21 Received:15 December2015 /Revised:29April2016/ Accepted:12May2016 !SpringerScience+Business MediaDordrecht2016 AbstractAcomprehensiveexpert consultationwas conductedinorder toassessthe status, trendsandthe mostimportant driversofchange intheabundance andgeographicaldis- tributionofkelp forestsinEuropean waters.Thisconsultation includedanon-line ques- tionnaire,resultsfrom aworkshopand dataprovidedby aselectedgroup ofexperts workingonkelp forestmapping andeco-evolutionaryresearch. Differencesinstatus and

CommunicatedbyStefanSchindler.

Thisispart ofthe specialissueon NetworkingBiodiversityKnowledge. &R.M.Arau ´jo ritaraujo@ciimar.up.pt 1 InterdisciplinaryCentreofMarine andEnvironmental Research,(CIIMAR/CIMAR), Universityof

Porto,Ruados Bragas289,4050-123 Porto,Portugal

2 CentreofMarine Sciences,University ofAlgarve(CIMAR-Algar ve),Campusof Gambelas,

8005-139Faro,Portugal

3

Oceana,Madrid,Spain

4 DipartimentodiScienzeBiologic he,Geologicheed Ambientali,(BIGEA) &Centro InterdipartimentalediRicercaperle ScienzeAmbientali (CIRSA),University ofBologna, UO

CoNISMa,ViaS. Alberto163, 48123Ravenna,Italy

5

GrupoBioCost,Departamento deBioloxı ´aAnimal,Bioloxı ´aVexetale Ecoloxı´a,Facultadede

Ciencias,Universidade daCorun˜a,Campus deACorun˜a,15008A Corun˜a,Spain 6 Alfred-WegenerInstitute,Helmholtz-Center forPolarand MarineResearch,AmHandelshafen12,

27570Bremerhaven, Germany

7 NorwegianInstituteforWaterResearch, Gaustadalle´en21,0349 Oslo,Norway 8 CNRS,UMR7144 AD2M,Station, Biologique,PlaceGeorges Teissier,29680Roscoff ,France 9 UPMCUniv. Paris6,Station Biologique,SorbonneUniver site´s,PlaceGeorges Teissier,

19680Roscoff,France

123

BiodiversConserv

DOI10.1007/s10531-016-11 41-7

trendsaccordingto geographicalareas, speciesidentityand small-scalevariationswithin thesamehabitat whereshown byassemblingand mappingkelpdistribution andtrenddata. Significantdatagaps forsomegeographical regions,likethe Mediterraneanandthe southernIberianPeninsula, werealsoidentified. Thedataused forthis studyconfirmeda generaltrendwith decreasingabundance ofsomenative kelpspeciesat theirsouthern distributionalrangelimits andincreasingabundance inotherparts oftheirdistribution (SaccharinalatissimaandSaccorhizapolyschides).Theexpansion oftheintroduced speciesUndariapinnatifida wasalsoregistered. Driversofobserved changesinkelp forestsdistributionand abundancewereassessed usingexperts'opinions. Multiplepossible driverswereidentified, includingglobalwarming, seaurchingrazing, harvesting,pollution andfishingpressure, andtheirimpact variedbetweengeographical areas.Overall,the resultshighlightmajor threatsforthese ecosystemsbutalso opportunitiesfor conservation. Majorrequirementsto ensureadequateprotection ofcoastalkelp ecosystemsalong Europeancoastlinesare discussed,basedon thelocalto regionalgaps detectedinthe study. KeywordsKelpforests!Expertconsultation!Statusandtemporal trends!Long-term changes!Europe

Introduction

Itisgenerally acceptedthatglobal researchandconservation questionsrelatedto biodi- versityandecosystem servicesneedto betackledat national,regional, andlocalgeo- graphicalscalesrelevant tomanagementand policyactivities(Petes etal.2014;Helmuth etal.2014).Usingthe bestscientificinformation availabletosupport decision-makingis fundamentaltothe implementationofnational andinternationalpolicies onconservation ofbiodiversityand sustainableuseof resources.Reliableinformation andadequate sci- entificdatato supporttheknowledge needsofdifferent groupsofstakeholders anddeci- sion-makersisnot, however,always available(Airoldiand Beck2007). 10 StationMarine,Muse ´umNationald'Histoire Naturelle,Placede laCroix,BP 225,

29182,Concarneau,France

11 Dpto.B.O.S.(Ecologı ´a),University ofOviedo,33071 Oviedo,Spain 12 Departmentof Biosciences,University ofOslo,P.O. Box1066,Blindern,0316Oslo,Norway 13 UMR8187LOG, UnivLilleNord deFrance,Universite ´Lille1,62930Wimereux ,France 14

UMR8187LOG, CNRS,62930Wimereux, France

15 FR2424,CNRS,Station Biologique,PlaceGeorges Teissier,29680Roscoff, France 16 TheMarineBiologic alAssocia tionoftheUK,CitadelHill, PlymouthPL12PB,UK 17 EnvironmentalHydraulicsInstitute(IH Cantabria),Universidad deCantabria,Avda. IsabelTorres,

15,ParqueCientı ´ficoyTecnolo ´gicodeCantabria ,39011Santander, Spain

18 UniversityRostock,Bioscienc es,Albert-Einst einstrasse3,18059Rostock,Germany 19 SydneyInstituteof MarineScience,19 ChowderBayRoad, MosmanNSW2088, Australia 20 UMI3614EBEA, UC,UACH,CNRS, StationBiologique,29680 Roscoff,France 21
DepartmentofBiology, Facultyof Sciences,Universityof Porto,Porto,Portugal

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123
Processesatthe interfacebetween scienceandpolicy canalsohave verydifferent structuresand approaches.Wherea topicrequiresan in-depthanalysisand aconsolidated viewpointfromthe scientificcommunityand otherknowledgeproviders, integrated activitiesarerequired inorderto synthesizeandanalyze existingknowledge.Using sucha framework,anEU-funded CoordinationAction,' 'DevelopingaKnowledge Networkfor Europeanexpertiseon biodiversityandecosystem servicestoinform policymaking eco- nomicsectors(KNEU)' 'wasconducted withtheobjectiveofdesigninga Networkof knowledge(NoK)on biodiversityand ecosystemservicesto informpolicy-makingand economicsectorsin Europe(www.biodiversityknowledge.eu/)(seeNeßho ¨veret al.2016). TheNoKprovided aninterfacewhere knowledgeholderswere identifiedandinvited to synthesizetheavailable knowledgeongiven topicsidentifiedin arequest-driven, science- policyknowledgeexchange process(Livoreilet al.2016).Thefunctioning andopera- tionalizationof theNoKwas testedwithinthe KNEUproject,by examiningdifferentcase- studiesandevaluating results,challengesand mainachievementsfrom arange of methodologicalapproaches(Schindler etal.2014;Dickset al.2016;Pullinet al.2016; Schindleretal. 2016).Withinthis frameworkthequestion: ''Whatis thecurrentstatus of kelpforestsin Europeandwhat istheevidence thattemporaltrends indistribution will affectkelp ecosystems'biodiversityand theprovisionof ecosystemservices?'' was selectedasone ofthecase studies.Thiswas abroadquestion coveringdifferentsub-topics andwasconsequently addressedby sub-questionsansweredusing threemethodological approaches:expertconsultation, systematicreview andadaptivemanagement. Theexpert consultationapproach (whichisdescribed inthismanuscript) wasusedto assessthestatus andtrendsof kelpforestsin Europe,givingalso someinitialinsights tothe questions addressedbythe othermethodological approaches. Kelpforestsdominate subtidalshallow rockycoastsand arekeycomponents ofcoastal ecosystemsintemperate topolarparts oftheworld, contributingtotheir production, biodiversityandfunctioning (Mann2000;Stenecket al.2002;Smaleet al.2013;Krause- JensenandDuarte 2014).Theseecosystems includehabitat-formingprimary producers (bothkelpsand associatedalgaespecies) thatsupportcomplex foodwebsin coastalzones andprovidefood, shelterandhabitat fora varietyofassociated organismssuchas apex predators(seamammals andseabirds),fish andinvertebrates(Duggins etal.1989;Mann

2000;Norderhauget al.2005;Reisewitzet al.2006;Christieet al.2009;Leclercet al.

2013,Bertocciet al.2015).Kelpforests provideseveral otherimportantecological

functions,supportinghigh primaryproductionand biomassinthe formofdetritus thatis exportedtoother ecosystems,includingdeep-sea sediments,shallowcoastal areas,and intertidalrockyshores (e.g.Dugginset al.1989;Mork1996;Krumhansland Scheibling

2012).Finally,kelps havethe potentialtoplay animportantrole inC-sequestration(Chung

etal.2013),sincea significantamountof carbonismaintained withinkelpforests atany onetime(Smale etal.2016),and somekelp-derivedorganic matterisexported toother habitatswhereit maybeburied andstoredfor aconsiderableamount oftime, thereby contributingto naturalcarbonsequestration (Hilletal. 2015).Collectively,kelp forestsare amongstthe mostdiverseand productiveecosystemsof theworld(Mann 1973)providing manyvaluableecosystem services(Costanzaet al.1997). Overthepast twocenturies,overfishing hasdrivenwidespread declinesofkelp forests insomeregions throughcascadingeffects onseaurchin abundance(e.g.Jackson etal.

2001;Watsonand Estes2011;Leleuet al.2012;Stenecket al.2013).Lossesof kelpforest

systemshavealso beenreported duetoclimate changeinthe lastfewdecades, especially nearthelow latitudelimitsof kelpranges,where theycanbecome eco-physiologically stressed(Stenecket al.2002;Norderhaugand Christie2009;Wernberget al.2010;

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Ferna´ndez2011;Oppliger etal.2012;Assiset al.2013;Brodieet al.2014).Recent modellingstudiespredicted severedeclineof kelpsalonga greatpart oftheEuropean coastlineandprogression intocold temperatetopolar areas(Mu¨lleretal. 2009;Krause- Jensenetal. 2012;Assiset al.2013;Raybaudet al.2013).Onthe otherhand,the increase inseawatertemperature hasalsoresulted inunfavourableconditions insomeareas for overgrazingbysea urchins,resultingin kelpforestrecovery inlargeareas ofthe NE Atlantic(e.g.Norderhaug andChristie 2009;Rindeet al.2014).Stormsaffect kelpmor- tality(Christieet al.1998,Smaleand Vance2015),andfuture increasesin stormfre- quenciesdueto changesin climatearealso likelytoaffect kelpforestdistribution. Other localfactorsreported tonegativelyaffect kelpforestabundances arekelpharvesting (Christieetal. 1998;Lorentsenet al.2010),declineof waterquality(e.g. pollution, eutrophication,sedimentation) (Airoldi2003;Delebecqet al.2013;Strainet al.2014), diseasesandpresence ofnon-nativeand invadingspecies(Ellertsdo ´ttirandPeters 1997;

Williamsand Smith2007).

Thedominantseaweed speciesalongthe Europeancoastlineare brownalgaemainly belongingtothe Laminariales(kelp)and Tilopteridales(kelp-like)which aredistributed fromthelower intertidaldownto, approximately30m inthesubtidal zone,depending on theclarityof thewater. InEurope,these ordersincludethe nativespeciesAlariaesculenta J.V.Lamouroux,L.hyperborea (Gunnerus)Foslie,L.ochroleuca Bachelotdela Pylaie,L. rodrigueziiBornet,L.solidungula J.Agardh,Saccharinalatissima(Linnaeus)C.E.Lane, C.Mayes,Druehl andG.W.Saunders, Phyllariopsisbrevipes(C.Agardh)E.C. Henryand G.R.South, P.purpurascens(C.Agardh)E.C. HenryetG.R.South,Saccorhizapoly- schides(Lightfoot)Batters,S.dermatodea (Bachelotdela Pylaie)andthe introducedkelp Theaimof thisstudywas toassembleand analyseEuropeankelp expert'sknowledge anddataon statusandtrends ofkelpdistribution throughtheestablished NoKon biodi- versityandecosystems inthe KNEUproject(Schindler etal.2016).Inspite ofthe importanceofkelp forestsfor thefunctioningof coastalecosystems(Steneck etal.2002), thereiscurrently nocoordinatedmonitoring ofkelpforests atEUlevel, andonly limited monitoringandhence fewdata onkelpdistribution atlocal,regional ornationalscale. The availableinformationabout Europeankelpforests, suchascurrent distribution,temporal trendsandimportant drivers,isthus fragmentedandoutdated (Smaleetal. 2013).Inthis studyavailableknowledge wasassembleddirectly fromkelpexperts throughaquestion- naireondifferent aspectsrelatedto kelpforestdistribution andtemporaltrends inEurope. Additionaldata andinformationon driversofchange andgapswere collatedthrougha workshopanda mappingexercise.

Materialsandmethods

Expertopinionsurvey

Scoping

Forty-sixknowledgehubs werecontactedvia e-mailandasked toidentify agroupof relevantexpertson Europeankelp forests.Theselection oftheknowledge hubswasbased

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ontheirconnection toenvironmental conservation,marineenvironment andresearchon natural/environmentalsciences and/ormarinerelated topics.

Questionnairedesignand distributionamongexperts

Aquestionnaire(Table 1)wasdeveloped comprisingsevenquestions ondifferent aspects ofcurrenttrends inkelpdistribution inEurope,and themaininvolved driversand ecosystemimpacts.The expertsansweredthe questionsfortheir geographicalworking area.Question7 aimedtoassess theexpert'sopinion ofthetrends ona globalscale.For all questions,exceptno 6,theexperts hadthepossibility tochoosemore thanone categoryof thepredefined answers,andfive ofthequestions includedtheexpert's lackofknowledge onthesubject. Inquestion6, theaimwas toidentifyconservation effortsand management programsforkelp forestwithin theexpertsworking area. Thequestionnairewas madeavailableon-line andtheexperts weregiven3 weeksto answer.Reminderswere sentonceto thosewhodid notreplythe firsttime.

Workshop

Followingthecompletion ofthequestionnaire, aworkshopwas organizedtopresent the resultsandto discussthenext stepsofthe studywithina workinggroup ofexperts.Fifty- Table1Listofquestions comprisingthequestionnai regivento theexpertgroup, coveringdifferent aspectsofthe statusand currenttrendsof kelpforestsin Europeaswell astheirdrivers andecosystem impacts

Question

no.

QuestionPossibleanswers

1Currenttrends inkelpforests (regarding

extensionanddensity)

Fourcategoriesof answers:increasing,

decreasing,stable,I don´tknow

2Sourceof informationused byexpertsto

answertoquestion 1

Fivecategoriesof answers:scientific works,

ownquantitativedata, non-scientific informationobtainedfromlocals, fisherman's,divers,harvesters,others

3Opinionabout therelevantstressors actingin

eachgeographicalregion

Sevencategoriesof answers:pollution,fishing

pressure/gear,kelpharvesting,biological invasions,seaurchins/h erbivores,global warming,others

4Opinionon theeffectsof theobservedkelp

trendsinfisheries

Fourdifferentcategories ofanswers:increase,

noeffects,decrease, Idon´tknow

5Identifythe ecosystemcharacteris ticsor

servicesaffectedby theobserved trendsin kelpforests

Fourdifferentcategories ofanswers:

biodiversity,interest ofdivers(tourism), waterquality,others.

6Identifyconservation efforts/management

programsfor kelpforestscurrently running intheirstudy area

Threedifferentcategories ofanswers:yes (if

theparticipantschoose thisoptionthey were furtheraskedto succinctlydescribe these programs),no,I don´tknow

7Describethe currenttrendsin kelpforestsat a

globalscale

Fivepossible categoriesofanswers:

increasing,stable,decreasin g,increasing in someregionsand decreasing inothers,I don´t know

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fiveexpertswere invitedto participateinthe workshopandeight (insomecases repre- sentingagroup ofexperts)from sixdifferentcountries (Portugal,Spain,Italy, France, GermanyandNorway) attended(15% oftotal).At theworkshop, theknowledgeand data providedby thequestionnairewere discussedanda workinggroupwas organizedto finalizethesubsequent collectionofrequired data. Fromtheinitial listofexperts indicatedbythe knowledgehubsand invitedfor the workshop,20representative expertswere contactedtobe partofthe workinggroupthat wasincharge ofminingany dataavailableon kelpdistribution(past andpresent) andkelp abundancewithin theirstudyarea. Thisinformationwas combinedandrepresented ina mapillustratingthe currentscientificknowledge aboutkelpforests distributionandtrends inEurope.Three additionalexpertswere contactedtoprovide dataandknowledge, either becausetheyrepresented missingcountrieswith kelpforestsor dueto theirexpertisein the field.

Mapping

Ageoreferencedgrid (resolutionof0.25 ")was senttothe 20expertsthat participatedinthe secondphaseof theexpertconsultation tomapkelp forestdistributionin theirassigned area.Eachcell hada uniqueidentificationnumber, tofacilitatethe subsequentunification inageneral gridforEurope. Anexcelfile (Table2)wasalso senttoeach expertsgroupto compilegeoreferencedinformation/data aboutpastand currentpatterns ofoccurrenceand abundance(e.g.area, biomass,density,depth distribution)foreach knownkelp speciesin theirarea.The informationwassummarized inone ofthefollowing categories:''reduc- tion'',''expansion'',' 'stable''(whenadecreaseorincreasetrendor astablepopulation respectively,hasbeen documentedbyabundance data,recordedin atleasttwo different pointsintime), or''extinction' '(whenavailable presence/absenceorabundance datahad documentedthecomplete disappearanceofa speciesfroma gridcell inwhichit was previouslypresent).For gridcells wherenodata ontemporaltrends wereavailable (presence/absencedata) thecategories' 'presence-nostatus'' (whenpresencedata were availablefor onlyonetemporal record)and' 'presence-stable''(when presencedatawere availablefrommore thanonetemporal record)wererepresented. Forgridcells whereno trendsorpresence datawere availablethecategories ''absence'' (whentheabsence ofthe Table2Fieldsincludedin theexcel filetobe filledwithinformat ionaboutthe gridcell(s)in themap

Categories

Nameofthe speciesthe informationapplies to

Numberofgrid cell(s)inthe map

Nameoflocation/reg ion

Modeofdata (modelbased/observation)

Dateofrecord

Dateofcompariso nwith(if available)

Typeofdata: presenceortrend, inarea,biomass, density,depthdistribution ,or anyotherrecorded change

Bibliographicreference

Contactinstitutionand contactperson

Otherremarks

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specieswasrecorded andno previousrecordof presencewasavailable) and''no data'' (wheninformationabout thespecieswas notavailable)were represented.GISmaps summarizedtheexpert informationforeach cellandspecies. Ascale wascreatedto classifythedegree ofcertaintyof thedataprovided byexperts,comprising thethree followingclasses:1 (highcertainty): databasedon fieldobservations;2 (mediumcer- tainty):databased onstatisticaland rulebasedmodels; 3(lowcertainty): databased on expertjudgement oronold recordsnotconfirmed byrecentsurveys.quotesdbs_dbs27.pdfusesText_33

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