Article
Reference
Perspectives on the link between ecosystem services and biodiversity: The assessment of the nursery function
LIQUETE, Camino, et al.
Abstract
The relationship between biodiversity and each ecosystem service or bundle of ecosystem services (e.g. win−win, win−lose or win−neutral) is an active field of research that requires structured and consistent information. The application of that research for conservation and decision-making can be hampered by the ambiguity found in the definition of the nursery function under the ecosystem service perspective. In this paper, we review how the role of nursery habitats is included in the ecosystem services literature, covering conceptual, biophysical and economic reflections. The role of ecosystems as nurseries is mostly analyzed in coastal environments. The main observation is that there is no consensus on the consideration of the nursery function as a service (e.g. which species or habitats) or on how to assess it (e.g. which indicators or valuation methods). After that review, we analyze three different interpretations given to the nursery function, namely the ecological, conservationist and economic point of view; and we distinguish between different types of assessment that may consider the nursery function. We [...]
LIQUETE, Camino, et al . Perspectives on the link between ecosystem services and biodiversity:
The assessment of the nursery function. Ecological Indicators , 2016, vol. 63, p. 249-257
DOI : 10.1016/j.ecolind.2015.11.058
Available at:
http://archive-ouverte.unige.ch/unige:97000
Disclaimer: layout of this document may differ from the published version.
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ContentslistsavailableatScienceDirect
Ecological Indicators
jou rn al h om ep a g e :w w w . e l s e v i e r . c o m / l o c a t e / e c o l i n d
Perspectives on the link between ecosystem services and biodiversity:
The assessment of the nursery function
Camino Liquete
∗, Núria Cid, Denis Lanzanova, Bruna Grizzetti, Arnaud Reynaud
EuropeanCommission,JointResearchCentre(JRC),InstituteforEnvironmentandSustainability(IES),ViaEnricoFermi2749,21027Ispra,VA,Italy
a r t i c l e i n f o
Articlehistory:
Received30July2015 Receivedinrevisedform 17November2015 Accepted29November2015 Availableonline31December2015 Keywords:
Nurseryhabitats Fisheries Ecosystemservices Biodiversity Conservation Ecosystemassessments
a b s t r a c t
Therelationshipbetweenbiodiversityandeachecosystemserviceorbundleofecosystemservices(e.g.
win−win,win−loseorwin−neutral)isanactivefieldofresearchthatrequiresstructuredandconsistent information.Theapplicationofthatresearchforconservationanddecision-makingcanbehamperedby theambiguityfoundinthedefinitionofthenurseryfunctionundertheecosystemserviceperspective.
Inthispaper,wereviewhowtheroleofnurseryhabitatsisincludedintheecosystemservicesliterature, coveringconceptual,biophysicalandeconomicreflections.Theroleofecosystemsasnurseriesismostly analyzedincoastalenvironments.Themainobservationisthatthereisnoconsensusontheconsideration ofthenurseryfunctionasaservice(e.g.whichspeciesorhabitats)oronhowtoassessit(e.g.which indicatorsorvaluationmethods).Afterthatreview,weanalyzethreedifferentinterpretationsgiven tothenurseryfunction,namelytheecological,conservationistandeconomicpointofview;andwe distinguishbetweendifferenttypesofassessmentthatmayconsiderthenurseryfunction.
Weconcludethatthenurseryfunctioncanbeconsideredanecosystemserviceonitsownrightwhenit islinkedtoaconcretehumanbenefitandnotwhenitisrepresentedwithindicatorsofgeneralbiodiversity orecosystemcondition.Thus,theanalysisofthedeliveryofecosystemservicesshouldbedifferentiated fromtheanalysisofecologicalintegrity.Onlywiththisdistinctionsciencemaybeabletoquantifythe linkbetweenbiodiversityandecosystemservicesandpolicymaybeeffectiveinhaltingbiodiversityloss.
Similarconsiderationscouldapplyforotherbiodiversityconstituentsthatmaybetreatedasecosystem services.
©2015TheAuthors.PublishedbyElsevierLtd.ThisisanopenaccessarticleundertheCCBYlicense (http://creativecommons.org/licenses/by/4.0/).
1. Protectingbiodiversitythroughecosystemservices
Ecosystemservicesbecamea policytool toprotect biodiver- sity mainlyas a resultof theglobal strategic plan 2011−2020 oftheConventiononBiologicalDiversity(Aichibiodiversitytar- gets),beforescientific consensusaboutthemutual relationship betweenecosystemservicesandbiodiversitywaswellestablished.
Stilltoday,althoughtherearenumerousevidencessupportinga positiverelationshipbetweenbiodiversity,ecosystem functions, andthedeliveryofparticularecosystemservices(Egohetal.,2009, Cardinale,2011,Isbelletal.,2011,Maceetal.,2012,Harrisonetal., 2014),thereisnotmuchconsensusonwhatthelinksareandhow theyoperate(Loreauetal.,2001,Harrisonetal.,2014).
Ecosystem services have, by definition, an anthropocentric focus.Theyarethedirectorindirectcontributionsfromecosystems tohumanwelfare.Toconsidersomethingasanecosystemservice,
∗Correspondingauthor.
E-mailaddress:camino.liquete@gmail.com(C.Liquete).
thismusthavehumandemandoridentifiedbeneficiaries(Haines- Young & Potschin, 2013). Nevertheless, it does not mean that ecosystemservicespromoteautilitarianviewofnature;theyrather aimathighlightingtheprocesses andoutputs fromecosystems thatcontributetohumanwell-beingand thatare usuallyover- looked,especiallyinsectorsnotrelatedwithnatureconservation orinareaswherenatureprotectionisnotthefirstpriority.
Biologicaldiversityatspeciesandpopulationlevelsisclosely linkedtoecosystemfunctioningand it isassumed topositively influence the provision of particular ecosystem services across scales (Naeem et al., 1995, Wormet al., 2006,Cardinale etal., 2012).Atthesametime,biodiversityandecosystemfunctioning areinfluencedbyinteractionsbetweenindividualsorspecies(see Grayetal.,2014and referencestherein),whichdirectlyrelyon habitatavailabilityandcondition.Forexample,theecosystemser- vicesthatimprovewaterquality(i.e.waterpurification)andflow regulation(i.e.floodprotection)areenhancedbyincreasesincom- munityandhabitatarea(Harrisonetal.,2014).Biodiversityisalso allegedtostabilizethedeliveryofecosystemservicesthroughtime (Tilman,1996,Chapinetal.,2000,Hooperetal.,2005,Schindler http://dx.doi.org/10.1016/j.ecolind.2015.11.058
1470-160X/©2015TheAuthors.PublishedbyElsevierLtd.ThisisanopenaccessarticleundertheCCBYlicense(http://creativecommons.org/licenses/by/4.0/).
250 C.Liqueteetal./EcologicalIndicators63(2016)249–257 etal.,2010)andthisisevenmoredemandedinecosystemsthat
areexpectedtoprovidemultiplefunctions(Hector&Bagchi,2007).
Consequently,thereisabigconcernabouttheeffectsofbiodiversity loss,notonlyfortheecosystems,butalsoforhumanwell-beingand livelihood(Hoekstraetal.,2005,Duffy,2009,Schindleretal.,2010, Tremletal.,2015).Inthiscontextwherebiodiversityisbeinglinked tohumanwell-being,severalinitiativespromotetheecosystem serviceapproach(e.g.MA,2005,UNEP,2007,TEEB,2010,IPBESin Díazetal.,2015),whichaimsatintegratingbothnaturalandsocial systemsprovidingamorecomprehensiveapproachfordecision- making.
Amajorchallengetoapplytheconceptsofecosystemservices inmanagementanddecision-makingistohaveclearassessment frameworksthatallowmeasuringeachserviceandlinkingthem tohumanwell-being.Duringourinvolvementinsomeinitiatives that trytooperationalize ecosystem services (e.g.MAES, 2014, OpenNESS,2014,MARS,2015),severalconceptualdiscrepancies andempiricalchallengeshavearisenwhentryingtoquantifypar- ticularecosystemservices.Oneofthemostcontroversialservices istheso-called“maintenanceofnurserypopulationsandhabitats”
intheCommonInternationalClassificationofEcosystemServices (CICES,2015)or“habitatsforspecies”inTheEconomicsofEcosys- temsand Biodiversity(TEEB)(see Appendix).Themainreasons behindarethat,ontheonehand,thisecosystemservicecouldbe interlinkedorcorrelatedwithotherservicesthatdirectlyrelyon it(e.g.fisheries)and,ontheotherhand,itreferstobiodiversity componentsandecosystemfunctions(i.e.nurseryfunction).Inthis context,ourmainquestionswere:Canthenurseryfunctionbecon- sideredanecosystemservice?Ifso,howshoulditbeadequately assessed?Whatarethedifferentoptions?
Thispaperpresents,first,ashortreviewofexistingapproaches thatanalyzethenurseryfunctionasanecosystemservice(Section 2);then,acriticalanalysisoftheseapproachesdiscussingdiffer- entperspectivesinconsideringbiodiversitycomponents(Section 3);andfinallyaproposalofspecificoptionstotacklethenursery functioninecosystemserviceassessments(Section4).Theanalysis isespeciallyimportantwhenaimingtoassessthelinksbetween biodiversityandthedeliveryofecosystemservices.
2. Nurseryhabitatsandtheecosystemserviceapproach 2.1. Definitionsandclassifications
Anurserycanbedefinedasahabitatthatcontributesmorethan theaverage,comparedwithotherhabitats,totheproductionof individualsofaparticularspeciesthatrecruittoadultpopulations (Becketal.,2001).Themainfactorsthatfacilitatethereproduc- tionandrecruitmentaredensity,growthandsurvivalofjuveniles, movementtoadulthabitats,oracombinationofthose(Becketal., 2001).Inthissense,experimentalstudieshavedemonstratedhow thenurseryfunction(i.e.theproductionofindividualsthatrecruit toadultpopulationsperunitareaofjuvenilehabitatsensuBeck etal.,2001)decreasedwithnurseryhabitatloss(Cheminéeetal., 2013).
Inanecosystemservicecontext,itisunclearwhetherthenurs- eryhabitatsandfunctioncouldberegardedasadistinctecosystem serviceorasabiodiversitycomponent.Forexample,TheEconomics ofEcosystems&Biodiversityfoundations(TEEB,2010)proposed
“maintenanceoflifecyclesofmigratoryspecies”asanecosystem service,postulatingthatwhenthemigratoryspecieshavecommer- cialvalueandreproduceinacertainhabitat,thatnurseryfunction shouldbevaluedbyitself(e.g.mangrovesusedasspawningand nurseryareasoffishandcrustaceansharvestedfaraway)(Table1).
Still, both TEEB (2010) and MA(2005) state that theso-called habitator supportingservices(such as“habitats forspecies”or
“photosynthesis”,seeAppendix)arenecessaryfortheproduction
ofmostoftheotherecosystemservicesand,thus,haveonlyindi- rectimpactsonpeople.Similarly,evenifnotsoexplicit,theCICES descriptionofthe“lifecyclemaintenance,habitatandgenepool protection”class(whichincludespollinationandthemaintenance ofnurserypopulationsandhabitats,seeAppendix)seemstobe restrictedtothereproductionandnurseryfunctionsthatsupport provisioningservices(e.g.pollinationasasupporttocommercial crops) (Haines-Young &Potschin, 2013).Within this classifica- tion, the“maintenance of nursery populations and habitats” is anindependentservicedefinedashabitatsforplantandanimal nurseryandreproduction.Incontrast,theUKNationalEcosystem AssessmentFollow-on(Turneretal.,2014)statesthatthenursery functionisalreadyvaluedthroughthefishthatiscaughtandsold onmarkets(i.e.throughitscontributiontofisheries)and,thus,it isnotincludedinthelistoffinalecosystemservices.Instead,itis splitbetweentwointermediateservicesnamed“larvalandgamete supply”and“formationofspecieshabitat”.
Otherauthorsincludethemaintenanceofallvegetalandanimal populationsaswellastheirresilienceamongregulatingorsuppor- tingservices(Beaumontetal.,2007,Rönnbäcketal.,2007)whichis difficulttodetachfrombiodiversityorecologicalintegrity.Inother cases, thedefinition of nurseries as ecosystem service remains ambiguousandcanbeusedwithdifferentconnotations.Forexam- ple,theservicehabitat/refugiaanalyzedbyCostanzaetal.(1997) includednurseryareasforcommercialspeciesaswellasresting areasformigratoryspecies.Itwasvaluedwithfish/shrimpmarket prices,endangeredspeciesconservationvalueandgeneralconser- vationvalue.InSalomidietal.(2012)theservice“reproduction&
nurseryareas”seemstocoverbydefinitionallmarinespecies(i.e.
theviabilityofpopulations),buttheexamplesaremostlylinked tocommercialspecies.Someothernamesreferringtothenursery functionasanecosystemserviceintheliteratureare:breedingand feedingground,nurseryhabitat,habitatprovision,refugeorshelter (seeTableS2inLiqueteetal.,2013).
Giventhisvarietyofopinionsabouthowthenurseryfunction shouldbedefinedandclassifiedinanecosystemservices’context, weproposetofollowa simplifiedrepresentation oftheecosys- temservices’cascadeframework(derivedfromHaines-Young&
Potschin,2010)(Fig.1).Morecompleteschemeshavebeendevel- oped,forinstance,ininternationalinitiativessuchasMülleretal.
(2010),TEEB(2010)orMaesetal.(2013)orotherproposalssuch asVillamagnaetal.(2013).Applyingthiskindofconceptualframe- workclarifieswhichcompartmentofthesocio-ecologicalsystems isbeinganalyzedandwhatismissingtofullycharacterized,for instance,oneecosystemservice.InFig.1,ecosystemfunctionsand processescompriseallthebiophysicalrolesthatsustainthepro- visionofaspecificecosystemservice,thusindicatingthenatural capacitytoprovidethat service.Ecosystemservices(alsonoted asecosystemserviceflows)aretheactualcontributionofecosys- temcomponents(asgoodsorservices)tohumanwell-being.The benefits and values designate the perception or valuation that human-beingsattributetoaspecificservice.Themanagementand socialresponsesreflecthowthepoliticalandpersonaldecisionsact asdriversofchangeoftheenvironment,affectingtheecosystems’
condition.Biodiversityis the variety oflife, including variation amonggenes,species,ecosystemsandhabitats.
Tomovefromthisconceptualframeworktoreal-worldassess- mentsresearchersgenerallyuseindicatorsorproxies.Indicators are variables that provide aggregated information on certain phenomena,actingascommunicationtoolsthatfacilitateasim- plificationofcomplexprocesses(Müller&Burkhard,2012).Proxies arehereassumedtobeapproximationsofecosystemservices’indi- catorswhentheentirephenomenacannotbequantified;aproxyis thusafigurethatcanrepresentthevalueofanecosystemservice indicator.Dependingontheobjectiveofeachcasestudy,theprox- iesorindicatorsmayrefertoecosystemfunctionsandprocesses,
Table1
Summaryofdefinitionsandinterpretationsaimingtoclassifythenurseryfunctionasanecosystemservice.
Ecosystemservice Servicecategory Definition Application Reference
Habitatsforspecies Habitatorsupporting service
Habitatsprovideeverything thatanindividualplantor animalneedstosurvive:food;
water;andshelter.Each ecosystemprovidesdifferent habitatsthatcanbeessential foraspecies’lifecycle.
Migratoryspeciesincluding birds,fish,mammalsand insectsalldependupon differentecosystemsduring theirmovements.
Itseemstocoverallhabitat functionforallspecies
TEEB(2015)
Maintenanceofnursery populationsandhabitats
Regulationand maintenanceservice
Habitatsforplantandanimal nurseryandreproduction
Reproductionandnursery functionsthatsupport provisioningservices
CICES(2015)
Larvalandgamete
supply/Formationofspecies habitat
Supportingintermediate services
Forinstance,thequantityof larvae&gametessuppliedtoa particularlocation/For instance,changeinareaor qualityofhabitat
Thenurseryfunctionisalready valuedthroughthefish provision
Turneretal.(2014), UKNEAFollow-on
Lifecyclemaintenance Regulatingand maintenance services
Biologicalandphysicalsupport to
facilitatethehealthyand diverse
reproductionofspecies
Themaintenanceofkey habitatsthatactasnurseries, spawningareas
ormigratoryroutesforall species
Liqueteetal.(2013)
Reproductionandnursery areas
Theprovisionofthe appropriateenvironmental conditionsforreproduction andgrowingduringtheearly stagesofmarinespecies.
Thedefinitionseemsto coverallmarinespecies,but theexamplesaremostlylinked tocommercialspecies
Salomidietal.(2012)
Maintenanceoflifecyclesof migratoryspecies
Habitatorsupporting service
Habitatsthatsustainmigratory specieswithcommercialvalue
Thefocusisontemporal habitatsandcommercial species
TEEB(2010)
Biologicallymediatedhabitat Supportservices Habitatwhichisprovidedby livingmarineorganisms
Itrefersto“essentialbreeding andnurseryspaceforplants andanimals[...]commercial and/orsubsistencespecies”
Beaumontetal.(2007)
Maintenanceofplant,algaland animalpopulations
Regulatingservices Reproduction Itreferstothemaintenanceof allvegetalandanimal populations
Rönnbäcketal.(2007)
Refugia/habitat Habitatforresidentand
transientpopulations
Nurseryareasforcommercial speciesaswellasrestingareas formigratoryspecies.
Costanzaetal.(1997)
theactualflowofecosystemservices,orthehumanbenefitorvalue.
Thus, selectingadequateindicators tomeasure each ecosystem serviceisacrucialstepofanyecosystemserviceassessment.
2.2. Assessmentsofnurseryhabitats
AftertheoverviewoftheconceptualapproachesinSection2.1, sections2.2 and2.3review thepractical assessmentsaboutthe nurseryfunctionandnurseriesandecosystemservicesfoundin theliterature.
Themajorityofthearticlesthatanalyzethenurseryfunction dealswiththerolethatcoastalenvironmentsplayforthemain- tenance ofprosperousfisheries. Theseassessmentsexplore and quantify therole ofhabitats such assalt marshes (Boesch and Turner,1984),mangroves(Mumbyetal.,2004,Aburto-Oropeza et al., 2008, Zavalloni et al., 2014), macroalgae and seagrasses (Cheminée etal., 2013,Blandon and zuErmgassen, 2014, Tuya etal.,2014),maerl(Kamenosetal.,2004)ortheircombinations (Meyneckeetal.,2008,McMahonetal.,2012)forprotectinglarvae andjuveniles,especiallyoffishandshrimppopulations.Themain reasonsforthelossofthisecologicalfunctionarethedisruptionof
Fig.1.Generaldiagramoftheconceptslinkingnaturalandsocialsystemsthroughecosystemservices.SeethedefinitionsofthefiveboxesinSection2.1.
252 C.Liqueteetal./EcologicalIndicators63(2016)249–257 connectivitybetweenspawning,nurseryandadult-stagehabitats
(McMahonetal.,2012,Leeetal.,2014)andtherapiddestructionof essentialhabitatsduetoanthropogenicdisturbanceslikelanduse changeorintensiveexploitation(Mangialajoetal.,2008,Walters etal.,2008,Zavallonietal.,2014).
Generallywithoutestablishinglinkstospecificspecies,some studies on terrestrial ecosystems highlight the importance of maintaininghabitats’diversity(eitherfortheirnurseryorshelter functions)foragriculturalproduction(Firbanketal.,2008,Cong etal.,2014).Othersfocusontheimportanceofmaintaininghabitats andpopulationsforrecreationalpurposeslikerecreationalfish- eries,divingorotheractivitiesrelatedwithecotourism(Reesetal., 2010).
The problem arises when trying to quantify nursery as an ecosystemservicewiththehelpofappropriateindicatorsorprox- ies.Mostoftheexamplesfoundintheliteraturelinkthenursery functionofcertainhabitatswiththedeliveryoffoodprovisionor recreation(Table2),eitherquantifyingnurseriesindependentlyor asa supportingservice. Incontrast,otherpublications consider thenurseryfunctionasaservicebuttheysuggestusingthesame indicatorsasforbiodiversityorecosystemcondition(seeFig.1).
Forinstance,Maesetal.(2014)compilesaseriesofindicatorsto measureecosystemservicesundertheEUBiodiversityStrategy.
Theypropose toquantify the“maintenance of nurserypopula- tionsandhabitats”withproxiessuchasconservationinvestments,
habitat−landscapeprotection,biodiversityvalue,ecologicalstatus orhabitatsdiversitythatcanbeconsideredasindicatorsofecosys- temcondition(Table2).Thismayhampertheanalysesthattryto assesstherelationshipsbetweenbiodiversity,ecosystemfunctions, andthedeliveryofparticularecosystemservices;asintroduced inSection1.Thesameauthors,though,acknowledgethatthese indicatorscanbesurrogates ofecosystem services(Maes etal., 2016).
Theproxiesofecosystemservicecapacity(i.e.ecosystemfunc- tionsandprocesses)usuallyrelatetotheconditionofthenursery habitats(extent,density,etc.)ortothediversityfoundonthem, withoutnecessarilyfocusingonspecieswithdirecthumaninter- est.The majority ofproxies of ecosystem service flow propose measuringthepresence or increase of juvenileswithcommer- cialorrecreationalinterestwithinnurseryhabitats;whileafew proxiesrequirethecomparisonoffishproductionwithotherchar- acteristicsofthenurseryhabitats(e.g.Aburto-Oropezaetal.,2008, Meyneckeetal.,2008).Mostoftheproxiesofbenefitsandvalue trytoestimatetheproportionofcommercialfisheriesthatdepends ontheexistenceandfunctioningofacertainnurseryhabitat.The inputforrecreationalfishingislessstudiedbutcanbeestimated inasimilarway.Onlyafewproxiesinvolvetheopinionoflocal residentsorusers.Themethodologiesusedtoestimatethebene- fitsandvalueshaveagreatvariety,whichisdealtwithinthenext section.Itmustbenoticedthattheclassificationofindicatorsin
Table2
Examplesofindicatorsandproxiesrelatedtothenurseryfunctionextractedfrompeer-reviewedliterature.Weorganizedandreclassifiedthoseindicatorsandproxies followingtheframeworkproposedinFig.1.Sources:1Aburto-Oropezaetal.,2008,2Barbieretal.,2002,3BlandonandzuErmgassen,2014,4Cheminéeetal.,2013,5Jackson etal.,2015,6Kamenosetal.,2004,7Knowleretal.,2003,8Maesetal.,2014,9Meyneckeetal.,2008,10Mumbyetal.,2004,11Stoneetal.,2008,12Tuyaetal.,2014,13Zavalloni etal.,2014.
Biodiversityandecosystemcondition Ecosystemfunctionsandprocesses Ecosystemserviceflow Benefitsandvalues
•Biodiversityvalue(speciesdiversity orabundance,endemicsorredlist species)8
•Oxygenconcentration(%)8
•Turbidity(%)8
•Ecologicalstatus(hightobad)8
•Hydromorphologicalstatus(high, good,other)8
•Habitatnurseryfunction(spp/habitat)4
•Canopyheight(cm)4
•Canopycover(%)4
•Residencetimeinseagrassateachlife stageofthefisheryspecies(yr)5
•Spawningandnurseryareas(ha)8
•Submergedandintertidalhabitats diversity8
•Speciesdistributionandabundance8
•Extentofmarineprotectedareas(ha)8
•Mangrovesextent(kmofcoast)10
•Sizedistributionofreeffishindifferent habitats(%indiv/sizeclass)10
•Wildshrimpdensityathightide (indiv/m2)13
•Relationshipbetweenfisheries landings(t/yr)andmangroves edgelength(km)1
•Carryingcapacityofmangroves (production)dependingon changesinareaandmarketprices (demand)2
•Enhancementofjuvenilefishby seagrasshabitats(indiv/m2)3
•Annualproductionofeachfish speciesattributabletoseagrass (g/m2)3
•Densityofreeffishjuvenileswith commercialorrecreationalinterest inCystoseiraforests(indiv/m2)4
•Juvenilegadoidsassociatedwith maerlandotherhabitats (indiv/m3)6
•Changeinrecruitmentofadults (%)7
•Catch-per-unit-effort(kg/day) distributionagainstwetland connectivityindex(%)9
•Catch-per-unit-effort(kg/day) distributionagainstwetlandpatch density(ha)9
•Structureofreeffish communities(multidimensional scalingordination)10
•Biomassofreeffishin
mangrove-richsystems(kg/km2)10
•Biomassofcommercialfishin seagrassmeadows(kg/ha)12
•Annualvalueoftheservices providedtothefishery (USD/kmofmangrove)1
•Economicproductionalong theproductivemangrove fringe(USD/ha/yr)1
•Marginalvalueofachangein mangrovearea(USD/ha)2
•Estimatedwelfarelosses associatedwithanannual mangrovedeforestation(USD)2
•Annualeconomic enhancementofcommercial fishbyseagrass(kg/m2, AUD/ha)3
•Commercialfisherylandings linkedtoseagrass-associated species(EUR/yr,%)5
•Expenditureofrecreational fisherspursuing
seagrass-associatedspecies (EUR/yr,%)5
•Benefitofprotectingfish habitattestingchangesin habitatquality(CAD/ha, CAD/km)7
•Increaseoffishbiomassfrom mangrove-scarceto mangrove-richsystems(%)10
•Willingnesstoparticipatein mangrovereforestationproject forthenurserybenefits(%)11
•Willingness-to-payfor mangrovereforestationproject (Rs/yr)11
•Valueofcommercialfishin seagrassmeadows(EUR/ha)12
•Benefitsfromcultivated shrimpoverbenefitsfromwild shrimp(%)13
Table2hasbeendoneforthispaper.Mostofthepublicationspro- poseindividualmeasuresandfiguresofthe‘nurseryfunction’orthe
‘maintenanceofnurserypopulationsandhabitats’servicethatcan beasdifferentinmagnitudeandinterpretationasthoseshownin Table2.
2.3. Economicmethodsandchallenges
Theeconomicbenefitsderivedfromthenurseryfunctioncon- stituteatypicalexampleofindirectusevaluesthatisanexample ofbenefitsderivedfromfunctionalservicesthatsupportcurrent productionandconsumption(Barbier,2007).Asaresult,thebene- fitsfromthenurseryfunctionreflecttheirsupportorprotection forallactivitiesthat havea directmeasurableeffectonhuman well-being.Followingthisview,theeconomicbenefitsofthenurs- eryfunctionofcoastalwetlandsshouldbe,forinstance,estimated byvaluingtheadditionalbenefitsforcommercialandrecreational fisheries.
In the context of ecosystem service valuation, a variety of methods are applied to estimate the economic value of the nursery functionrelated totheenhancement of fisheries. They includesurrogatemarketprice(Curtis,2004),specificintegrated approacheslinkingbiologicwitheconomicmodels(Knowleretal., 2003,Zavallonietal.,2014),productionfunctions(Barbieretal., 2002,Johnstonetal.,2002,McArthurandBoland,2006,Barbier, 2007),contingentorconjointvaluation(Nunesetal.,2004,Stone etal.,2008),valuetransferofwillingnesstopay(Luisettietal., 2014),ordirectmonetaryassessmentofcoastalfisheriesthrough thetransformation of fishabundanceintofinancial valueusing standard market-priceswith quantitative estimates of juvenile fishes(Aburto-Oropezaet al.,2008, BlandonandzuErmgassen, 2014,Tuyaetal.,2014,Jacksonetal.,2015).
Thechoiceoftheappropriatevaluationmethodisverymuch debated in the economic literature. For instance, one limita- tion when combining market values with surface or juvenile countsis thatusuallyneitherpriceeffects(i.e.changes inmar- ketpriceinresponsetofishabundance)norexploitationeffects (i.e.changes in exploitation intensityin response tofishabun- dance)areaccountedfor.Asaresult,Knowleretal.(2003)argue that valuationshould bebased on a bio-economic model link- ing nursery and habitat quality to some welfare measures. In addition, since the nursery function enhances theproductivity ofeconomic activitiesorprotectsthem frompossibledamages, Barbier(2007)suggeststhatanappropriatevaluationmethodis aproductionfunctioninwhichnurseryisconsideredaproduction input.
Movingaway fromfisheries,afew studiesassessedtheeco- nomic contribution of the nursery function to the production ofinsects forcommercialpurposesinland,in dryenvironments (Rodriguezetal.,2006).Whentheavailabilityofthenurseryfunc- tiondependsonthestateofthehabitat,itsvaluecanbeestimated applyingthereplacementcost method(Rodriguezet al.,2006).
Also,inthecaseswherecertainspecieshavearecreationalvalue, someauthorsassessthenurseryfunctionwithconventionalstated preferencemethodssuchaschoiceexperiment(Cerdaetal.,2013) orrevealedpreferencesapproachessuchastravelcost(Gürlük&
Rehber,2008).
3. Differentperspectives-fromecologytoeconomy
In our review of the studies that analyze nursery habitats in ecosystem service assessments, we identified some back- ground arguments or perspectives sharedby different articles.
We observedthat thesebackgroundperspectivesmainlydeter- mine which components of natural and social systems shown
in Fig. 1 are evaluated and which method is used for the assessment.Hence,basedonourinterpretationoftheliterature, we summarize below three main perspectives,not necessarily independent from each other, that we have named ecologi- cal, conservationist and economical perspectives. The naming of these perspectives tries to be illustrative for the readers and by no means tries to define the corresponding scientific disciplines.
1.Theecologicalpointofview:Speciespopulations,community compositionandhabitatsarewithinthemostrelevantbiodi- versityconstituents.Measurementsofspeciespopulations(e.g.
abundanceanddistribution)andecosystemstructure(e.g.habi- tat structure) are considered key biodiversity variables that can beapplied acrosstaxa and acrossterrestrial, freshwater andmarinerealms(Pereiraetal.,2013).Theecologicalpoint of view aims at assessing ecosystem condition using biodi- versity constituentsas indicators (e.g.variety orpresence of certainhabitats,ecologicalstatus).Themainissueistodiffer- entiatebetweenbiodiversity,astheunderpinningcharacteristic supportingmostecosystemservices,andtheoutcomeofaspe- cific service, which has to be measured with other metrics (e.g.residencetimeoffishinseagrass,densityofgadoidjuve- niles).Henceinpracticalassessments,thisperspectivefocuses onthecompartments‘biodiversity andecosystem condition’,
‘ecosystemfunctionsandprocesses’andsometimeson‘ecosys- temserviceflow’of Fig.1.Whenit covers‘managementand social responses’it concentratesontheimpactsthat ecologi- calsystemsreceivefromnaturalorhuman-inducedpressures.
In this context, the “maintenance of nursery populations and habitats”cannotbeassessed asastand-aloneecosystem serviceaslongasitisnotdifferentiatedfrombiodiversityand ecosystem condition. Otherwise theecosystem service to be assedwouldbeforinstancefisheriesunderpinnedbynursery habitats.
2.Theconservationistpointofview:Ecosystemservicescanbe apowerfultooltopreservebiodiversityandnaturalcondition, andtoengagemultipleactorsandsectorsinthisobjective(e.g.
Maes et al., 2013). However, many stakeholders, practition- ersandend-usersofecosystemserviceassessmentsprimarily measureprovisioninggoods(e.g.fish)orhumanexperiencesin nature(e.g.recreation)andtherebydismisstheindirectcontri- butionofhabitatsandspeciestohumanwell-being(e.g.nursery) (Villamagnaetal.,2013).Theconservationistpointofviewhas theobjectiveofhaltingbiodiversitylossandpreservingnature, infrontofnaturalresourcesexploitation,usingthearguments ofecosystemservicesacrosssectorsanddisciplines.Theriskof thisperspectiveistoassessthenurseryfunctionusingbiodi- versityconstituentsasindicators,especiallywhenspecificdata abouttheecologicalprocesses(ecosystemservicecapacity)are not available.Theconservationistpoint ofviewmayaddress allthecomponentsofFig.1butitgivesaspecialemphasisto
‘biodiversityand ecosystemcondition’and‘management and social responses’.Fromthis perspective,the“maintenanceof nurserypopulationsandhabitats”shouldbeincludedinthelist of ecosystemservicesto makeits contributiontowell-being explicit,evenifsomeofitsindicatorsmayrefertoecosystem condition.
3.Theeconomicpointofview:Theconceptofecosystemservices representstheflowsofvaluefromnaturalcapitaltohumansoci- eties(TEEB,2010).Wemustgivetheseflowsadequateattention andweightinthedecision-makingprocess,otherwisehuman welfarewilldeteriorate(Costanzaetal.,1997).Theeconomic point ofviewpursuesassigningvalues toecosystemservices throughthebenefitsthathaveadirecteffectonhumanwell- beingratherthan throughtheservicesthemselves.Themain
254 C.Liqueteetal./EcologicalIndicators63(2016)249–257 issueisthatonlyprovisioningandafewculturalserviceshave
explicitpricesoraretradedinmarkets,whileotherecosystem benefits,especially regulatingservices, remainlargely invisi- blebecausetheycannotbeverypreciselyestimatedwiththe availablemonetarymethods.Intermsofassessments,theeco- nomicperspectivefocusesonthe‘benefitandvalue’component ofFig.1andsometimeson‘ecosystemserviceflow’.“Mainte- nanceofnurserypopulationsandhabitats”isacombinationof ecologicalphenomenasupportingthedeliveryofotherprovi- sioningorculturalservices(e.g.foodorrecreation),fromwhich humansobtainbenefits.Still,insomeeconomicassessments, thenurseryfunctionisconsideredasanecosystemservicethatis linkedtothevaluehumansgivetothepresenceofwildlife,either fordirectuse(e.g.diving)ornon-use(e.g.bequestorexistence value).Undertheeconomicpointofview,includingnurseries amongotherecosystemservicestobevaluedcouldleadtodou- blecountingwiththeassessmentofotherecosystemservices orwiththeassessmentofbiodiversityitself.Therefore,“main- tenanceofnurserypopulationsandhabitats”shouldpreferably notbeconsideredasaservice.
4. Optionsandrecommendationstoassessthenursery function
Inthissection,wedescribetheoptionsthatecosystemservice practitionersmayface toassessthenursery function,wehigh- lightthemainriskofeachoption,andweproposeourpreferred choice.Finally,wediscusssomelessonslearntfromthispaperthat gobeyondthenurseryfunction.
1.Thefirstoptionisexcludingthenurseryfunctionfromthelist of ecosystem services assuming that it is already quantified throughfoodprovision,recreationor otherservices.Therea- sonbehind this choiceis because assessing“maintenance of nurserypopulationsandhabitats”mayleadtodouble-counting or may overlap with general analyses of biodiversity. How- ever,theriskofthisoptionistoignorethenaturalcapacityto deliverfoodprovisionorrecreation,wherethenurseryfunction mayplayakeyroleand,thus,promoteunsustainablemanage- mentifananalysisofecosystemconditionisnotperformedin parallel.For instance,when theestimationof fisheriesMaxi- mumSustainableYieldignorestheeffectofnurserygrounds, it mayleadto fisheriescollapse. Evenin relatively complete assessments(e.g. fish stocksassessments), it is difficult that an analysis of fisheries captures the relevance and value of thenurseryfunctionifthis isnotanexplicitobjectiveofthe study.
2.Thesecondoptionistoinclude“maintenanceofnurserypopu- lations and habitats” among the ecosystem services but in practiceuseasurrogateassessment,i.e.a substitutemeasure for the service that usually comesfrom general biodiversity orecologicalintegrityanalyses.Thischoiceisunderstandable undercertaincircumstanceslikethelackofadequateresources, dataortimeforconductingfull integratedassessments.Typ- icalexamplesarelocalassessmentsbasedonremote sensing indevelopingcountries(Liqueteetal.,2016).Themainriskof thisoptionistocreateconfusionbetweenthecomponents‘bio- diversityand ecosystemcondition’, ‘ecosystem functionsand processes’and ‘ecosystem serviceflow’ in Fig.1. Thisconfu- sionwillhidetheeffectsofbiodiversityonecosystemservices delivery. In this situation, it is advised to differentiate the biodiversity-relatedinformation fromthe ecosystemservices quantification, and to avoid aggregating these two kinds of results.
3.Thethirdoptionalsoincludesthenurseryfunctionasanecosys- temservice,butthistimesupportedbyanintegratedecosystem assessment that comprises at least ‘biodiversity and ecosys- temcondition’andsomeoralltheothercomponentsofFig.1, makingacleardifferentiationbetweencomponentsandmak- ingreferencetospeciesofdirectuseforhumans.Inthiskind of assessments, therelevance of the nursery habitats for all organismscanbeanalyzedasabiodiversityconstituent,butthis cannotbeconsideredanassessmentofecosystemservices.The mainriskofthisoptionistodoublecountthenurseryfunction togetherwithotherprovisioningorculturalservices,particu- larlywhen onlythe ecosystem goods (e.g.fish) and not the processesarevalued.
Takingintoaccountalltheargumentspresented,ourpreferred choiceisthethirdoption.Weconcludethatthenurseryfunction shouldbeconsideredanecosystemserviceonitsownrightwhen it islinked toa concrete humanbenefit(e.g.enhanced fishing, increasedrecreationalactivities)andnotwhenitisrepresentedasa generalbiodiversityconstituent.Inouropinion,theriskofdouble- countingcanbeavoidedbyagoodplanningandclearobjectiveof thestudy.Nurseryhabitatsarecrucialforthemaintenanceoffish- eries(e.g.Jacksonetal.,2015),butwehavenotreadasinglestudy addingthemonetaryvaluefrom“maintenanceofnurserypopu- lationsandhabitats”andthatof“foodprovisioning”,i.e.counting twicethesamebenefit.Instead,theindicatorsusedtocharacter- izethedeliveryandbenefitfromthenurseryfunctionaredifferent fromthoseoffisheries(e.g.Table2).Whenitcomestoeconomic valuation,theresultsfrom“maintenanceofnurserypopulations andhabitats”shouldbeonlyusedtoestimatewhatshareofthe totalfishingvalueultimatelydependsonspecificnurseryhabitats.
Evenifthosemonetaryvaluescannotbeadded,theyareextremely importanttomakethecasefortheprotectionofessentialhabi- tats,tojustifyconservationinvestmentsortoregulateconflicting humanactivities.
Thus,weadvocateforthedistinctionbetweentheanalysisof biodiversityandecologicalintegrityandecosystemserviceassess- ments(quantificationofcertainbiologically-mediatedprocesses thatbenefithumanbeings),andfortheirintegrationwhenecosys- temservicesactasapolicytoolforprotectingbiodiversity(e.g.MA, 2005,IPBESinDíazetal.,2015).Onlywiththisdistinctionscience maybeabletoquantifythelinkbetweenbiodiversityandecosys- temservices(e.g.Reyersetal.,2012,Maesetal.,2012)andpolicy maybeeffectiveinhaltingbiodiversityloss.
The analysis of the nursery function in ecosystem service assessments presented in this papersuggests that similar con- siderations and conclusions could apply for other biodiversity constituentsthatmaybetreated asecosystem servicessuchas
“biodiversity” or “habitat quality” (InVEST, 2015, Nelson et al., 2011),“nutrient cycling”(MA,2005),“waterconditions”(CICES, 2015),or“habitats forspecies”(TEEB,2015).Again,inallthese cases, we should clarify whether (1) these services can be measuredindependently from theoverall ecosystem condition, (2) there is a direct human benefit from these services, and (3) their benefit is overlapping with other services or can be differentiated.
Acknowledgments
Thispaperistheresultofongoingdiscussionswithinamulti- disciplinaryteam,wheresharingandrefiningourpointsofview enrichedourunderstandingandourwork.Thisisfosteredbythe research activitiesdeveloped under the EUFP7 projects MARS (grantagreementno.603378)andOpenNESS(grantagreementno.
308428)and,consequently,byallthepartnersandcolleagueswe havethepleasuretocollaboratewith.
AppendixA.
CommonInternationalClassificationofEcosystemServicesv4.3(CICES,2015):
Section Division Group Class
Provisioning Nutrition Biomass Cultivatedcrops
Rearedanimalsandtheiroutputs Wildplants,algaeandtheiroutputs Wildanimalsandtheiroutputs Plantsandalgaefromin-situaquaculture Animalsfromin-situaquaculture
Water Surfacewaterfordrinking
Groundwaterfordrinking
Materials Biomass Fibresandothermaterialsfromplants,algae
andanimalsfordirectuseorprocessing Materialsfromplants,algaeandanimalsfor agriculturaluse
Geneticmaterialsfromallbiota
Water Surfacewaterfornon-drinkingpurposes
Groundwaterfornon-drinkingpurposes
Energy Biomass-basedenergysources Plant-basedresources
Animal-basedresources
Mechanicalenergy Animal-basedenergy
Regulation&Maintenance Mediationofwaste,toxics andothernuisances
Mediationbybiota Bio-remediationbymicro-organisms,algae, plants,andanimals
Filtration/sequestration/storage/accumulation bymicro-organisms,algae,plants,andanimals Mediationbyecosystems Filtration/sequestration/storage/accumulation
byecosystems
Dilutionbyatmosphere,freshwaterand marineecosystems
Mediationofsmell/noise/visualimpacts
Mediationofflows Massflows Massstabilisationandcontroloferosionrates
Bufferingandattenuationofmassflows
Liquidflows Hydrologicalcycleandwaterflow
maintenance Floodprotection
Gaseous/airflows Stormprotection
Ventilationandtranspiration Maintenanceofphysical,
chemical,biological conditions
Lifecyclemaintenance,habitatand genepoolprotection
Pollinationandseeddispersal
Maintenanceofnurserypopulationsand habitats
Pestanddiseasecontrol Pestcontrol Diseasecontrol Soilformationandcomposition Weatheringprocesses
Decompositionandfixingprocesses Waterconditions Chemicalconditionoffreshwaters
Chemicalconditionofsaltwaters Atmosphericcompositionand
climateregulation
Globalclimateregulationbyreductionof greenhousegasconcentrations Microandregionalclimateregulation
Cultural Physicalandintellectual
interactionswithbiota, ecosystems,and land-/seascapes
Physicalandexperiential interactions
Experientialuseofplants,animalsand land-/seascapesindifferentenvironmental settings
Physicaluseofland-/seascapesindifferent environmentalsettings
Intellectualandrepresentative interactions
Scientific Educational Heritage,cultural Entertainment Aesthetic Spiritual,symbolicand
otherinteractionswith biota,ecosystems,and land-/seascapes
Spiritualand/oremblematic Symbolic
Sacredand/orreligious
Otherculturaloutputs Existence
Bequest
