Conservation status of the freshwater pearl mussel Margaritifera margaritifera in Portugal

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Limnologica

j ou rn a l h o m e pa g e :w w w . e l s e v i e r . c o m / l o c a t e / l i m n o

Conservation

status

of

the

freshwater

pearl

mussel

Margaritifera

margaritifera

in

Portugal

夽

Ronaldo

Sousa

a,b,∗

_,

_Ângela

_Amorim

b

_,

_Elsa

_Froufe

a

_,

_Simone

_Varandas

c

_,

_Amílcar

_Teixeira

d

_,

Manuel

Lopes-Lima

a,e

a_{Interdisciplinary}_Centre_of_Marine_and_{Environmental}_Research_{(CIIMAR/CIMAR),}_University_of_Porto,_Rua_dos_Bragas_289,_P_4050-123_Porto,_Portugal b_CBMA_–_Centre_of_Molecular_and_{Environmental}_Biology,_Department_of_Biology,_University_of_Minho,_Campus_de_Gualtar,_4710-057_Braga,_Portugal c_CITAB-UTAD_–_Centre_for_Research_and_Technology_of_{Agro-Environment}_and_Biological_Sciences,_University_of_{Trás-os-Montes}_and_Alto_Douro, ForestryDepartment,Apartado1013,5000-801VilaReal,Portugal

d_CIMO-ESA-IPB_–_Mountain_Research_Centre,_School_of_Agriculture,_Polytechnic_Institute_of_Braganc¸_a,_Campus_de_Santa_Apolónia,_Apartado_1172, 5301-854Braganc¸a,Portugal

e_ICBAS-UP_–_Institute_of_Biomedical_Sciences_Abel_Salazar,_University_of_Porto,_Rua_de_Jorge_Viterbo_Ferreira,_228,_4050-313,_Porto,_Portugal

a

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t

i

c

l

e

i

n

f

o

Articlehistory:

Received6February2014

Receivedinrevisedform15May2014 Accepted10July2014

Availableonline27August2014 Keywords: Conservation Margaritiferamargaritifera Pearlmussel Portugal River Threats

a

b

s

t

r

a

c

t

Basedonnewinformation,thecurrentconservationstatusofthefreshwaterpearlmusselMargaritifera margaritifera(Linnaeus,1758)inPortugalisrevised.Between2010and2013surveyswereconducted ineightdifferentriverstoassessdistribution,abundance,size-frequencyandpreferentialhabitatofthis species.RiversNeiva,CávadoandTervapresentedverylowabundances(intheCávadonospecimenswere found)andshowedacutesignsofageing,callingintoquestionthefuturesurvivalofthesepopulations. AlthoughabundanceswerelowinRiversBec¸a,PaivaandMente,juvenileswerepresentandpopulations mayimprovetheirconservationstatusinthefuture,ifappropriatemanagementmeasuresareapplied. RiversRabac¸alandTuelapresentedthehighestabundancesofadultsandjuvenilesandthesetworivers havethehighestpotentialfortheconservationoffreshwaterpearlmusselsinPortugal.However,these twopopulationshavesufferedseveredeclinesinseveralstretchesduetotheconstructionofdamsin recentyears.GiventhatthePortuguesepearlmusselpopulationsareatthesouthernrangeofthespecies distribution,theirconservationshouldbeapriority.Thiscurrentdescriptionoftheconservationstatus ofM.margaritiferainPortugalcanbeusedasareference,andguidefutureresearchandmanagement initiativestobetterconservethisspecies.

Introduction

Thefreshwater pearl musselMargaritifera margaritifera

(Lin-naeus,1758)hasawidespreaddistributioninEurope(fromthe

IberianPeninsulaintheSouthwest,toRussiaintheNortheast)and

wasonceabundantinmanyoligotrophicrivers(reviewedinGeist,

2010).However,inthelastcenturymanystudieshavereported

extensivespatialdeclinesandreductionsinabundanceinmany

rivers(reviewedinYoungetal.,2001).Sincepearlmusselsmay

bedescribedasindicator,ﬂagship,keystone,andumbrellaspecies

requiringalmostpristineconditions,andhavealifecycle

depend-entonsynchronouslydeclininghostﬁshspecies(salmonandtrout),

夽 Thisarticleispartofaspecialissueentitled“Thecurrentstatusandfuture chal-lengesforthepreservationandconservationoffreshwaterpearlmusselhabitats”.

∗ Correspondingauthorat:CIIMAR,RuadosBragas289,4050-123Porto,Portugal. E-mailaddress:ronaldo.sousa@ciimar.up.pt(R.Sousa).

signiﬁcantconservationinteresthasbeendevotedtothisspecies

inthelasttwodecades(Geist,2010).M.margaritiferaiscurrently

listedascriticallyendangeredinEurope(Cuttelodetal.,2011)and

protectedintheEuropeanUnion(EU)underannexesIIandVof

theEuropeanCommissionHabitatsDirective[92/43/EEC],which

requirethattheEUMemberStatesregularlyassessitsdistribution

andabundanceandreportitsconservationstatus(Reidetal.,2013).

InPortugal,theﬁrstcomprehensivereviewofM.margaritifera

distributionwaspublishedbyNobre(1941).Inthisworkthe

pres-enceofthisspeciesisdescribedinseveraltributariesoftheRiver

Douroandalsointwootherriversfurthersouth:theRiversUland

Mira(althoughthepresenceintheRiverMiraishighly

improba-blesincethissystemisatypicalMediterraneantemporaryriver,

whichhabitatcharacteristicsare,apparently,notsuitableforpearl

mussels).Afterthisﬁrstcomprehensiverevision,Bauer(1986)

vis-itedtheDourotributariesanddidnotﬁndanyindividuals;based

onthis information,Young et al.(2001) statedthat pearl

mus-selswereprobablyextinctinPortugal.Asecondcomprehensive

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Fig.1.MapshowingthelocationofsamplingsitesintheRiversNeiva,Cávado,Terva,Bec¸a,Paiva,Mente,Rabac¸alandTuela.

reviewonM.margaritiferadistributioninPortugalwascarriedout

byReis(2003)whoconﬁrmedthepresenceofM.margaritiferain

sixdifferentriversincludingverysmallpopulationsintheRivers

Neiva,CávadoandPaivaandlargepopulationsintheRiversMente,

Rabac¸alandTuela.Morerecently,Varandasetal.(2013)described

twomorepopulationsintheRiversBec¸aandTerva.Currently,allM.

margaritiferapopulationsarelocatedintheNorthofPortugaland

noreportsexistforitspresenceinthecentralandsouthernpartof

thecountry.

Giventheconservationimportanceofthisspecies inEurope,

including Portugal, the main objective of this study was to

summarize information about current distribution, abundance,

size-frequencyandhabitatpreferenceofPortuguesepearlmussel

populations.Thisdata,inadditiontothediscussionofthemain

threats,canbeusedasareferenceandguidefuturemanagement

initiativestobetterconserveM.margaritiferainPortugal.

Materialsandmethods

Studyarea

Allthe surveyed riversare locatedin the North of Portugal

(Fig. 1).Inthis regionthe climatereﬂects theproximitytothe

AtlanticOceanandaltitude,rangingfromtemperatenearthecoast

to Mediterranean more inland (Oliveira et al. 2012).

Precipita-tionlevelshavehighseasonalandinter-annualvariability,which

isreﬂectedin abruptchangesin thedischargeregimeof rivers.

Floodsmayoccurduringwinter/earlyspring,withagradualdecline

inriverdischargethroughouttheyear,reachingminimalvalues

inthelate summer/earlyautumn.Thislowerdischarge ismore

pronouncedinthecontinentalareas(incomparisontotheregions

near the sea) with usually longer droughts. The land use and

landscapevaryacrossthestudiedarea,withthelargesthuman

settlementsandindustrialandagriculturalactivitieslocatedinthe

coastalzonesandatloweraltitudes.Ontheotherhand,theareas

locatedinland,andathigheraltitudes,havelowhumanpressure

andaremostlyforested(Ferreiraetal.,2007).

Thestudyareacompriseseightdifferentrivers(Fig.1).TheRiver

Neivahasalengthof45km,withnodamsbutwithmanyweirs

present.TheRiverCávadohasalengthof118kmandseverallarge

damsforhydroelectricproductionarepresentwithinthebasin.The

RiversBec¸aandTervaaretributariesoftheRiverTâmega;Bec¸ahasa

lengthof46kmandTervaof27km(foradetailedcharacterization,

seeVarandasetal.,2013).TheRiverPaivahasalengthof108km

(foradetailedcharacterization,seeSousaetal.2013).TheRivers

Mente,Rabac¸alandTuelaaretributariesoftheRiverTuaandhave

averylowhumanpressure.TheRiverMentehasalengthof57km,

RiverRabac¸al88kmandRiverTuela102km;fourdamsarepresent

intheRiversRabac¸alandTuela,twoineachriver.

Samplingstrategyanddataanalysis

Assessment of the M. margaritifera conservation status was

carriedoutbetween2010and2013,duringspringandsummer

months.Surveysincludedatotalof92sites(7sitesinRiverNeiva,

5inRiverCávado,5inRiverTerva,6inRiverBec¸a,32inRiverPaiva,

9inRiverMente,12inRiverRabac¸aland16inRiverTuela;Fig.1).

Foreachsite,ariverstretchwithatotallengthof100mwasvisually

surveyedusingglassbottomedviewersandsnorkelling.However,

inriverswithverylowabundance,moreextensivelengthswere

surveyed;inRiverNeivaS1,S2,S3,S6andS7weresurveyedfor

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Fig.2.AbundanceofM.margaritiferainRiversNeiva(a),Terva(b),Beça(c),Paiva(d),Mente(e),Rabaçal(f)andTuela(g).Numberofindividualspersitewasexpressedper 100mriverstretch,withtheexceptionofsomesites:inRiverNeivaS1,S2,S3,S6andS7weresurveyedfor250mandS4andS5for500and3000m,respectively;inRiver TervaS1wassurveyedfor800m,S2for1750m,S3for800m,S4for900mandS5for1000m;andinRiverBeçaS1andS2weresurveyedfor750m,S3for250m,S4for 950m,S5for600mandS6for300m.

TervaS1wassurveyedfor800m,S2for1750m,S3for800m,S4

for900mandS5for1000m;andinRiverBec¸aS1andS2were

sur-veyedfor750m,S3for250m,S4for950m,S5for600mandS6for

300m.Thesesurveyswerealwaysperformedwithaminimumof

4peoplespendingaminimumof2hineachsite.

Musseldimensions(shelllength,heightandwidth)were

mea-suredtothenearest0.1mmwithaVerniercaliperandallspecimens

were carefully returned to the river in their original position.

M.margaritiferajuvenileswereconsideredusingthe

biologically-based deﬁnition(up to 60mm)described by SanMiguel et al.

(2004)forIberianpopulations.Accordingtotheseauthors,Iberian

M.margaritiferapopulationsreachmaturityearlierthannorthern

populationsandspecimenslargerthan60mminlengthcanbe

con-sideredadults.Possibledifferencesinmeanlengthsbetweenrivers

weretestedbyKruskal–Wallis,sincedatadepartfromnormality,

usingthesoftwareMinitab14.

Foratotalof1947musselspecimens(17inRiverNeiva;140

in River Bec¸a; 360in River Paiva; 210in River Mente; 484 in

River Rabac¸al and 736in River Tuela),ﬁve instream attributes

(overhead cover on the mussel location, predominant type of

riverbed substrate, current velocity, water depth and distance

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RiversNeiva(Fig.2a)andTerva(Fig.2b)presentedlow

abun-dances,andindividualswerescatteredandrestrictedtoverysmall

patches,particularlyintheRiverTervawherespecimenswereonly

foundatonesite.Atotalof21musselswerefoundinRiverNeiva

andsiteS5presentedthehighestnumberwith15individualsper

3000mofriverstretch.Atotalof14individualsper900mofriver

stretchwerefoundinRiverTervainS4.RiversBec¸a(Fig.2c),Paiva

(Fig.2d)andMente(Fig.2e)possessedintermediatemussel

abun-dances. However,intheRivers Bec¸a andMente theindividuals

wererestrictedtodownstream areas.InRiverPaiva,thespecies

waspresentalmostthroughouttheentireriverlength,withthe

exceptionofafewkilometresnearthemouthandthehead.Atotal

of183individualswerefoundinRiverBec¸awhereS1presentedthe

highestabundancewith99individualsper750mofriverstretch.

Atotalof353individualswerefoundinRiverPaiva,beingS24the

sitewhichcontainedthehighestabundancewith78individuals

per100mofriverstretch.Atotalof177individualswerefound

inRiverMente,withS2containingthehighestabundancewith60

individualsper100mofriverstretch.Thehighestabundancesof

pearlmusselsinPortugalwerefoundinRiversRabac¸al(Fig.2f)

andTuela(Fig.2g),withthespeciesbeingpresentinallsurveyed

sitesexceptintheareassubjectedtotheinﬂuenceofdams(S4in

RiverRabac¸alandS6inRiverTuela)andinS1inRiverRabac¸al.

Atotalof3411individualswerefoundinRiverRabac¸al,withthe

highestabundanceof1310individualsper100mofriverstretchin

S6.Atotalof1149individualswerefoundinRiverTuela,withthe

Tuelabeingclearlysmallerthanindividualsfromotherrivers,

espe-ciallyfromRiversTervaandBec¸a(Fig.3).

ThemajorityofM.margaritiferaspecimenswerefoundinsand

andgravelsubstrateinareastypicallycoveredbyriparian

vege-tationandcurrentvelocitiesbetweencategories1and3during

spring/summerconditions(Fig.4).Regardingwaterdepth,

mus-selswerefoundatdepthslessthan100cmwithmorethan80%of

thebivalvesbeingcollectedwithin3mfromthebanks,andvery

fewinthemiddleoftheriverchannel(Fig.4).

Discussion

Conservationstatus

Untilthebeginningofthe20thcentury,M.margaritiferawasa

commonspeciesintheNorthofPortugal,colonizingseveral

trib-utariesoftheDouroandVougabasins(Nobre,1941)andpossibly

alsootherriversdraining directlytotheAtlanticOceansuchas

theMinho and Lima(populationsstill existin thesetwo rivers

and upstreamtributariesontheSpanishside(Loiset al.,2014)

andsomeunpublishedsurveysalsoreporttheirhistoricalpresence

withinthePortugueseborders).Duetoanthropogenicdisturbance,

mainlyintheformofhabitatloss,habitatfragmentationand

pol-lution,M.margaritiferahasdeclinedrapidlyordisappearedfrom

severalPortugueserivers.Indeed,Bauer(1986)wasunabletoﬁnd

anyspecimeninRiversFerreira(12sitessurveyed),Sousa(8sites

Fig.3. ShelllengthdistributionofM.margaritiferainRiversNeiva(N=21),Terva(N=14),Bec¸a(N=183),Paiva(N=353),Mente(N=177),Rabac¸al(N=3411)andTuela (N=1149).Beanplotsshowmeanvalues(horizontalline)andthewidertheshapeatagivenshelllength,themorespecimensareassociatedwiththatvalue.

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Fig.4. PercentageofM.margaritiferaindividualsinrelationtohabitatcharacteristics(N=1947):cover(qualitativedata,1=rootsorvegetation,2=cobblesorbouldersand 3=bedrock),dominantsubstrate(qualitativedata,1=roots,2=sandandgraveland3=cobles,bouldersorbedrock),currentvelocity(qualitativedata,varyingfrom0to5 where0representanullvelocityand5averyhighvelocity);depth(cm);andnearestdistancetothebank(m).

surveyed),Paiva(10sitessurveyed)andTâmega(3sitessurveyed),

whichleadYoungetal.(2001)toconcludethatthespecieswas

possiblyextinctin Portugal.The maincausesfor this supposed

extirpationwereunknown,althougheutrophicationwasthemain

candidateforRiversFerreira,SousaandTâmegabutnotforPaiva

(Bauer,1986).However,during2001and2002,Reis(2003)

car-riedoutanationwidesurvey(including240sitesin131riversand

streams)toassessthedistributionofthis and otherfreshwater

bivalvespecies.ThisauthorwasabletoconﬁrmthepresenceofM.

margaritiferainsixPortugueseriversandalsostudieditspopulation

densityandstructureforsomeoftheserivers(seefurther

discus-sionbelow).Thepresentstudyprovidesamorerecentappraisalof

theconservationstatusofpearlmusselsinPortugal,re-surveying

previouslyidentiﬁedpopulationsandreportingthemainﬁndings

concerningrecentlydescribedpopulations(RiversBec¸aandTerva;

Varandasetal.,2013).

ThedecliningratesdescribedforPortuguesepopulationsfollow

thegeneraltrendsofmanyEuropeanM.margaritiferapopulations

(reviewedinGeist,2010).Incomparisonwiththesurveysmade

byReis(2003),this studyshows ahigher abundanceand more

extensivespatialdistributionintheRiversNeivaandPaiva.These

differences couldbe related to a higher sampling effortin the

presentstudy,whichsurveyedalmosttheentirelengthofthese

tworivers,incomparisonwiththerestrictedsurveysperformedby

Reis(2003).Suchanexplanationseemsmorerealisticthan

assum-ingtherecoveryofthesepopulationsinsuchashorttimeperiod.

Additionally,andcontrarytoReis(2003),nospecimenswerefound

intheRiverCávadodespiteanintensivesurveyconductedonﬁve

differentsiteswherespecimenswerepreviouslylocated.

Popula-tionsinRiversBec¸aandTervawererecentlydiscovered(Varandas

etal.,2013)andforthatreason,itisimpossibletomakeanykindof

comparisonwithearlierstudies.Finally,thepopulationsofRivers

Mente,Rabac¸alandTuelaseemtohavealowerabundancethan

thosereportedbyReis(2003).Thissituationmaybeexplainedby

twofactors:(1)thedifferentmethodologyusedinthetwostudies;

and(2)anextensivedeclineduetoincreaseofhumandisturbance

intheserivers,mainlyduetoconstructionofdams(seebelowfor

furtherdiscussion).Despite thepossibleincreaseof human

dis-turbanceinrecentyears,thelargestpopulationsstilloccurinthe

RiversRabac¸alandTuela,bothofwhichﬂowthroughareaswith

lowhumanpressure.

Thepearlmusselpopulationsize-frequencyintheRiversNeiva,

Terva,Bec¸aand Paiva revealedacute ageing,withaprevalence

ofindividualsmeasuringover80mminlength.Thissituationhas

alreadybeendescribedformanyIberianandotherEuropean

popu-lations and is the major factor concerning the survival of this

species(Álvarez-Claudioetal.,2000;Hastieetal.,2000;Geist,2010;

Österlingetal.,2010;Hastie,2011;Loisetal.,2014).Nevertheless,

withtheexceptionoftheRiverTerva,afewjuvenileswerepresent.

Ontheotherhand,theRiversMente,Rabac¸alandTuela,although

dominatedbylargeranimals,presentedahighnumberofjuveniles,

whichindicaterecentrecruitmentandshowthatthesepopulations

arestillfunctional.Althoughthecurrentstudysampleda much

largernumberofspecimens,acomparisonwithReis(2003)show

thatthepopulationstructureisstillverysimilarinRiversPaivaand

TuelaandslightlydifferentintheRiversMenteandRabac¸al.Inthe

RiverMente,thespecimensarecurrentlysmaller,dominatedby

the60–70mmsizeclassinsteadof70–80mm,whilstintheRiver

Rabac¸al,individualsarelarger,dominatedbythe70–80mmsize

class,insteadof60–70mm,withmuchlowerprevalenceofsizes

classessmallerthan60mm.

In thesurveyed rivers, M.margaritifera were predominantly

foundincleanoligotrophicriverstretches,colonizingareasnear

thebanksatlowdepths,insandandgravelsediments,withahigh

degreeofriparianvegetationcoverandamoderate-fastﬂowing

habitatsofrapids,runsandrifﬂes.Similarresultshavealsobeen

widelydescribed for other Europeanpopulations (Hastieet al.,

2003a;Moralesetal.,2004;Outeiroetal.,2008;Geist,2010).

Mainthreats

Contrary to some European countries (e.g. Finland, Ireland,

NorthernIreland,ScotlandandRussia;BeasleyandRoberts,1996;

Cosgroveetal.,2000;Makhrovetal.,2014)pearlﬁshingwasnever

aproblemforPortuguesepopulationsandthereisnoreportofthis

activityinthestudiedrivers.However,someanecdotal

informa-tionprovidedbylocalolderpeoplereportthecasualuseofthese

musselsasasourceofproteinforhumanconsumption.Evenso,it

seemsthatoverexploitationmayhaveaminorinﬂuenceexplaining

thedecliningtrendsinPortuguesepopulations.

Introductionofnon-nativespecies seemsalsotobeaminor

problemfor thesurvival ofM.margaritifera.AlthoughtheAsian

clamCorbiculaﬂumineaispresentinsomeofthesurveyedareas

(ﬁrst50km of theRiverPaiva and downstream areasof Rivers

Rabac¸alandTuela)itsdensitywasverylow,anditispossiblethat

thisspeciesonlyhasminorimpactsonM.margaritifera(Sousaetal.,

2013).TheNorth-AmericansignalcrayﬁshPacifastacusleniusculus

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probablyatthelimitoftheirphysiologicalcapacity(Sousaetal.,

2013)and(2)ifextremeclimaticeventsincreaseinfrequencyand

severity,thismayimposeagreatproblemtopearlmussel

popula-tions.Indeed,ﬂoodsanddroughtsmayincreaseinthefutureand

thissituationmaybeproblematicforpearlmussels.Mortalitiesof

M.margaritiferainseveralPortugueseriversweredescribedafter

ﬂoods(Sousaetal.,2012)andthesameispossibletooccurduring

droughts(Sousaetal.,2008).

Waterdeterioration,duetopollutionandchangesinlanduse,

hasbeenpointedoutasamajorthreattoM.margaritifera,

result-ingindrasticdeclines(Youngetal.,2001;Geist,2010).InPortugal,

riverssuchasFerreiraandSousa,knowntohavebeencolonized

byverydensepopulationsof pearlmusselsat thebeginningof

the20thcentury (Nobre, 1941)are nowadaysheavilypolluted.

Asaconsequence,M.margaritiferacompletelydisappearedfrom

theseriverssinceatleastthemid-1980s(Bauer,1986).Currently,

thePortuguesepopulationsarerestrictedtoriverswithverylow

humanpressureandwithlowlevelsofpollution.Theexceptionis

RiverTerva,sincethisriverisknowntohavesomeeutrophication

problems(Varandasetal.,2013).Inaddition,somestretchesinthe

RiversNeivaandPaivastillreceivesewagedischarges.

Habitatlossandfragmentationisusuallyconsideredthemost

importantthreattofreshwatermussels,includingM.margaritifera

(Cosgroveand Hastie,2001).Directphysicalhabitatdisturbance

resultingfromchannelizationofriversorthepresenceof

impound-ments,usuallyresultinpearlmusseldeclinesandadecreasein

connectivity,includinginthehostﬁshes(Muelleretal.,2011;Addy

etal.,2012).Particularlyimportant inPortugal arethechanges

mediatedbythepresenceofrecentlyconstructeddamsandweirsin

severaloftheriverssurveyed,whichmayberesponsibleforsevere

declinesinpearlmussels.Forexample,thetwodamspresentinthe

RiverRabac¸alwererecentlyconstructed(werenotpresentduring

thesamplingmadebyReis(2003))andare1.5kmupstreamofS4

and2kmdownstreamofS5(thislastdamalsoaffectsRiverMente).

Ontheotherhand,S6islocatedupstreamoftheinﬂuenceofthis

seconddamintheRiverRabac¸al.Acomparisonofthepearl

mus-sels’abundanceatS4andS5withS6andfurtherupstreamsites

showsacleardifference.Themaindrivingmechanisms

respon-sibleforthegreatdeclineinM.margaritiferanearthesephysical

structuresarenot knownbutmayinclude alterationsin depth,

ﬂow,temperature,sediments,organicmatter,amongotherfactors

(VaughnandTaylor,1999;Addyetal.,2012).Foraspeciessuch

asM.margaritifera,whichusuallycolonizessiteswitholigotrophic

andloticconditions,theirpresenceintheareasupstreamofthese

physicalstructuresishighlyimprobableduetoincreasedwater

depth,changefromlotictolenticconditions,accumulationofﬁne

sedimentsandchangesinoxygenandtemperatureproﬁles.Many

alterationsmayalsooccurdownstreamoftheseobstaclesandmay

includedirecteffectsthroughphysicalstressandindirecteffects

throughchangesinhabitat,foodandﬁsh-hostavailability(Vaughn

Conservationmeasures

M.margaritiferahasalifespaninexcessof100years,although

intheIberianPeninsulathespecies“only”reachesaround60years

(Outeiroetal.,2008);sexualmaturityisattainedatarelativelylate

stageandthedispersalcapacityisreduced.Whileadultmusselsare

sedentaryandhavealimitedtoleranceforanykindofdisturbance,

thejuvenilesarehighlydependentonthesubstratequalityand

sta-bilityandhaveverypoorsurvivalrates(Geist,2010).Theglochidia

larvaeareobligateparasitesofsalmonids,whichhaveexperienced

asynchronousdeclineoverthelastdecades(Geist,2010).Allthese

featuresmakethisspecieshighlyvulnerabletohabitatdisturbance,

afactthatmakesconservationmanagementmuchmorecomplex

(Beasleyetal.,1998).Onthecontrary,andduetotheirextendedlife

span,ifadultscansurviveinpresentdisturbedconditions,

conser-vationmaybepossibleiftheappropriatemanagementmeasures,

thatguaranteeeffectivereproductionandfuturerecruitment,are

implemented(Hastie,2011).Inthesamevein,andduetothehigh

fertility,captivebreedingandfuturestockinginthewildcanbea

viablesolutionifthesuitableconditionsarerestored(Prestonetal.,

2007;Bollandetal.,2010;Thomasetal.,2010;Gumetal.,2011).

Giventhisbackground,twomainoptionsfortheconservationof

M.margaritiferainPortugalarepossible,whichencompassin-situ

andex-situconservationmeasures.Forthemoreabundant

popu-lationsofRiversPaiva,Mente,Rabac¸alandTuelathemainoption

shouldbein-situconservation,protectingthesepopulationsagainst

themainthreatsdescribedabove.Someofthesitescolonizedby

thisspeciesarealreadyinsideprotectedareas.TheNaturalPark

ofMontesinhocoverstheupstreamareasofRiversMente,Rabac¸al

andTuelawherethehighesttotalabundanceandpresenceof

juve-nileswerereported.Assuch, itiscrucial thattheseecosystems

shouldbeconsideredforfullprotectionofthePortuguesebreeding

stock.Similarly,theRiverPaivaisclassiﬁedasaSiteof

Commu-nityImportancewithintheNatura2000network.However,asfar

asweknow,therearenospecialactionsfocusedontheprotection

offreshwaterpearl musselsoreven aspecialattentiondevoted

toconservationoftheseaquaticecosystems,withtheexception

oftheEcotoneLife+_project_partly_devoted_to_the_conservation_of

pearlmusselsintheRiverPaiva.IntheRiversCávado(whereno

specimenswerefoundrecently),Neiva,TervaandBec¸a,

popula-tionsarerestrictedtosmallareasandwithverylowabundances;

exsituconservationmeasuresshouldcomplementinsitu

interven-tions.Inthisregard,captivebreedingshouldbeanoptioninorder

toreleasejuvenilesinappropriatehabitatsorinrestoredstretches

oftheserivers.SomesuccessfulcaptivebreedingprogramsforM.

margaritiferaalreadyexistinEurope,andso,thesetechniquesare

alreadyavailabletobeusedinPortugal,takinginaccountthebest

practicesthatshouldincludegeneticinformation,careful

determi-nationofhabitatrequirements(fromthemacrotothemicroscale)

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tionmeasuresandinformationonthedistribution,basicecological

traits (e.g. reproduction rates, fecundity, age at maturity, host

infestationrates,growthratesandlifespan)andgeneticsofM.

mar-garitiferaarethemainoptionstoconservePortuguesepopulations.

Thedatacollectedduringthisstudyprovidesanuptodate

assess-mentoftheconservationstatusofM.margaritiferainPortugaland

canbeusedasareference,andguidefutureresearchand

manage-mentinitiativestobetterconservethisspecies.

Acknowledgments

Financial support was provided by Portuguese Foundation

forScienceandTechnology(FCT)and COMPETEfunds—projects

ECO-IAS (Contract: PTDC/AAC-AMB/116685/2010) and CONBI

(Contract: PTDC/AAC-AMB/117688/2010). This study was also

partially supported by the European Regional Development

Fund (ERDF) through the COMPETE, under the project

“PEst-C/MAR/LA0015/2011”.

TheauthorsthankAdrianaNovais,CarinaSobral,CátiaSantos,

CristinaPatrício,ErikaBódis,FranciscoCarvalho,JoaquimdeJesus,

MarianaHinzmann,MarisaLopes,MiguelSantos,PedroTeixeira,

RicardoAzevedo,SaraSarmento,Vera Dantas,VítorPereira and

WilliamMcDowellforvaluablehelpduringtheﬁeldcampaigns;

PedroFerreirafor thepreparationof Fig.1,AllanSouzaforthe

preparationofFig.3,andGethinRhysThomasforacarefulrevision

ofthemanuscript.

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