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Fish and Fisheries. 2018;1–15. wileyonlinelibrary.com/journal/faf | 1 Received: 29 June 2017 | Accepted: 18 January 2018 DOI: 10.1111/faf.12273 ORIGINAL ARTICLE Translating the terrestrial mitigation hierarchy to marine megafauna by-catch E J Milner-Gulland 1 | Serge Garcia 2 | William Arlidge 1 | Joseph Bull 3,4 | Anthony Charles 5 | Laurent Dagorn 6 | Sonya Fordham 7 | Joshua Graff Zivin 8 | Martin Hall 9 | Jeffrey Shrader 10 | Niels Vestergaard 11 | Chris Wilcox 12 | Dale Squires 13 1 Department of Zoology, University of Oxford, Oxford, UK 2 IUCN Commission on Ecosystem Management Fisheries Expert Group, Gland, Switzerland 3 Department of Food and Resource Economics, Center for Macroecology, Evolution and Climate, University of Copenhagen, Copenhagen, Denmark 4 Durrell Institute of Conservation and Ecology, University of Kent, Canterbury, UK 5 School of Environment and School of Business, Saint Mary’s University, Halifax, NS, Canada 6 French National Research Institute for Sustainable Development (IRD), UMR MARBEC (IRD, Ifremer, Univ. Montpellier, CNRS), Sète, France 7 Shark Advocates International, Washington, DC, USA 8 School of Global Policy and Strategy, University of California San Diego, San Diego, CA, USA 9 Inter-American Tropical Tuna Commission, San Diego, CA, USA 10 School of International and Public Affairs, Columbia University, New York, NY, USA 11 Department of Sociology, Environmental and Business Economics, University of Southern Denmark, Esbjerg, Denmark 12 CSIRO Marine and Atmospheric Research, Hobart, Tas., Australia 13 Southwest Fisheries Science Centre, National Oceanic and Atmospheric Administration, San Diego, CA, USA Correspondence E J Milner-Gulland, Department of Zoology, University of Oxford, Oxford, UK. Email: [email protected] Funding information Pew Charitable Trusts Abstract In terrestrial and coastal systems, the mitigation hierarchy is widely and increasingly used to guide actions to ensure that no net loss of biodiversity ensues from develop- ment. We develop a conceptual model which applies this approach to the mitigation of marine megafauna by-catch in fisheries, going from defining an overarching goal with an associated quantitative target, through avoidance, minimization, remediation to offsetting. We demonstrate the framework’s utility as a tool for structuring think- ing and exposing uncertainties. We draw comparisons between debates ongoing in terrestrial situations and in by-catch mitigation, to show how insights from each could inform the other; these are the hierarchical nature of mitigation, out-of-kind offsets, research as an offset, incentivizing implementation of mitigation measures, societal limits and uncertainty. We explore how economic incentives could be used throughout the hierarchy to improve the achievement of by-catch goals. We con- clude by highlighting the importance of clear agreed goals, of thinking beyond single species and individual jurisdictions to account for complex interactions and policy leakage, of taking uncertainty explicitly into account and of thinking creatively about approaches to by-catch mitigation in order to improve outcomes for conservation and fishers. We suggest that the framework set out here could be helpful in support- ing efforts to improve by-catch mitigation efforts and highlight the need for a full empirical application to substantiate this. KEYWORDS albatrosses, biodiversity offsetting, economic incentives, no net loss, sharks and rays, turtles This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2018 The Authors. Fish and Fisheries Published by John Wiley & Sons Ltd.

Translating the terrestrial mitigation hierarchy to marine ......of marine megafauna by-catch in fisheries, going from defining an overarching goal with an associated quantitative

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Page 1: Translating the terrestrial mitigation hierarchy to marine ......of marine megafauna by-catch in fisheries, going from defining an overarching goal with an associated quantitative

Fish and Fisheries 20181ndash15 wileyonlinelibrarycomjournalfafemsp|emsp1

Received29June2017emsp |emsp Accepted18January2018DOI 101111faf12273

O R I G I N A L A R T I C L E

Translating the terrestrial mitigation hierarchy to marine megafauna by- catch

E J Milner-Gulland1 emsp|emspSerge Garcia2emsp|emspWilliam Arlidge1emsp|emspJoseph Bull34emsp|emsp Anthony Charles5emsp|emspLaurent Dagorn6emsp|emspSonya Fordham7emsp|emspJoshua Graff Zivin8emsp|emsp Martin Hall9emsp|emspJeffrey Shrader10emsp|emspNiels Vestergaard11emsp|emspChris Wilcox12emsp|emspDale Squires13

1DepartmentofZoologyUniversityofOxfordOxfordUK2IUCNCommissiononEcosystemManagementFisheriesExpertGroupGlandSwitzerland3DepartmentofFoodandResourceEconomicsCenterforMacroecologyEvolutionandClimateUniversityofCopenhagenCopenhagenDenmark4DurrellInstituteofConservationandEcologyUniversityofKentCanterburyUK5SchoolofEnvironmentandSchoolofBusinessSaintMaryrsquosUniversityHalifaxNSCanada6FrenchNationalResearchInstituteforSustainableDevelopment(IRD)UMRMARBEC(IRDIfremerUnivMontpellierCNRS)SegraveteFrance7SharkAdvocatesInternationalWashingtonDCUSA8SchoolofGlobalPolicyandStrategy UniversityofCaliforniaSanDiegoSanDiegoCAUSA9Inter-AmericanTropicalTunaCommissionSanDiegoCAUSA10SchoolofInternationalandPublicAffairsColumbiaUniversityNewYorkNYUSA11DepartmentofSociologyEnvironmentalandBusinessEconomicsUniversityofSouthernDenmarkEsbjergDenmark12CSIROMarineandAtmosphericResearchHobartTasAustralia13SouthwestFisheriesScienceCentre NationalOceanicandAtmosphericAdministrationSanDiegoCAUSA

CorrespondenceEJMilner-GullandDepartmentofZoologyUniversityofOxfordOxfordUKEmailejmilner-gullandzoooxacuk

Funding informationPewCharitableTrusts

AbstractInterrestrialandcoastalsystemsthemitigationhierarchyiswidelyandincreasinglyusedtoguideactionstoensurethatnonetlossofbiodiversityensuesfromdevelop-mentWedevelopaconceptualmodelwhichappliesthisapproachtothemitigationofmarinemegafaunaby-catchinfisheriesgoingfromdefininganoverarchinggoalwithanassociatedquantitativetargetthroughavoidanceminimizationremediationtooffsettingWedemonstratetheframeworkrsquosutilityasatoolforstructuringthink-ingandexposinguncertaintiesWedrawcomparisonsbetweendebatesongoinginterrestrial situations and in by-catch mitigation to show how insights from eachcould informtheotherthesearethehierarchicalnatureofmitigationout-of-kindoffsetsresearchasanoffsetincentivizingimplementationofmitigationmeasuressocietallimitsanduncertaintyWeexplorehoweconomicincentivescouldbeusedthroughout thehierarchy to improve theachievementofby-catchgoalsWecon-cludebyhighlightingtheimportanceofclearagreedgoalsofthinkingbeyondsinglespeciesand individual jurisdictions toaccount forcomplex interactionsandpolicyleakageoftakinguncertaintyexplicitlyintoaccountandofthinkingcreativelyaboutapproaches toby-catchmitigation inorder to improveoutcomes forconservationandfishersWesuggestthattheframeworksetoutherecouldbehelpfulinsupport-ingeffortsto improveby-catchmitigationeffortsandhighlighttheneedforafullempiricalapplicationtosubstantiatethis

K E Y W O R D S

albatrossesbiodiversityoffsettingeconomicincentivesnonetlosssharksandraysturtles

ThisisanopenaccessarticleunderthetermsoftheCreativeCommonsAttributionLicensewhichpermitsusedistributionandreproductioninanymediumprovidedtheoriginalworkisproperlycitedcopy2018TheAuthorsFish and FisheriesPublishedbyJohnWileyampSonsLtd

2emsp |emsp emspensp MILNER- GULLAND Et AL

1emsp |emspINTRODUC TION

Thegoal of nonet loss (NNL)of biodiversity fromeconomicde-velopment is becomingwidely adopted by national governmentsand international lenders potentially offering a method to limitthe impacts of environmental damage in terrestrial and coastalsystems(BBOP2012IFC2012)Severallargemultinationalcom-panieshavesigneduptoNNLoreventoproducinganetgainofbiodiversity as a result of their activities (BullampBrownlie 2017Raineyetal2015)GenerallyNNLisassuredbytheuseofamit-igation hierarchy often applied as part of an Environmental andSocialImpactAssessment(ESIA)Themitigationhierarchyrequiresthatprojectproponentsfirstavoiddoingharmtobiodiversityforexample by sitting the development away from particularly sen-sitive areas Subsequentlywhile carryingout their developmenttheyshouldminimize theharmdone forexampleby limiting thefootprint of heavymachinery to specific areas and not pollutingwatercoursesTheythenremediatethebiodiversitylosswithinthedevelopment footprint for example by replanting cleared areaspost-developmentThefinalstepistooffsetanyresidualadditionaldamage caused by their development through improvement ofbiodiversityelsewhere(Gardneretal2013)usingarangeofap-proachesforexamplediggingnewpondsorclearinginvasiveveg-etationinanadjacentsite(BullHardyMoilanenampGordon2015)Offsetting isaparticularlycontroversialelementofthehierarchybecauseitrequiresacceptanceofadevelopmentthatharmsbiodi-versity inagivenlocationandassumesthat it ispossibletocom-pensateforthisharmbybiodiversityenhancementelsewhere(egMaron etal 2016)More generally there ismuch debate aboutwhetherNNL isattainableandhow it shouldbe implemented inpractice(mostrecentlyexploredbyBullLloydampStrange2017)

Despiteitsgrowinguseinterrestrialandcoastalenvironmentsthemitigationhierarchyhasnotbeensowidelyapplied innear-shoreandhighseasmarinesettingsandmanyquestionsaboutitsapplicationintheoceanremain(SquiresampGarciainpressUNEP-WCMC2016)Marine experience to date hasmostly concernedcoastaldevelopmentforexamplerelatingtowindfarmsurbande-velopmentaquacultureandportsratherthaninthecapturefish-eriesarena(egKyriaziLejanoMaesampDegraer2015VaissiegravereLevrel Pioch amp Carlier 2014) The four steps of themitigationhierarchyarediscussedinfisherieshoweverandasintheterres-trialliteraturetheoptionofoffsettingisparticularlycontroversial(egthedebatearoundWilcoxampDonlan2007analysisofthepo-tentialforoffsettingseabirdby-catchbyinvasivespecieseradica-tiononnestingislandsFinkelsteinetal2008WilcoxampDonlan2009ŽydelisWallaceGilmanampWerner2009)Theuseofeco-nomicincentivestoreducetheamountorimpactofby-catchhasreceivedattentionbuthasalsonotyetbeenfullyexplored(DuttonampSquires2008GjertsenSquiresDuttonampEguchi2014InnesPascoe Wilcox Jennings amp Paredes 2015) The current FAOInternationalGuidelinesonBycatchManagementandReductionofDiscardsmentioneconomicincentivesonlybriefly(astheonlyeconomic instrument) and refer only to incentives to promote

innovationingeartechnology(FAO2011)Manyquestionsremainas towhether it is possible to apply themitigation hierarchy tomarineby-catchandwhatmeasurescouldbeusedtoincentivizeactionateachstageinthehierarchyInparticularthereisaneedforaconceptualframeworkthatintegratestherangeofby-catchmitigationmeasuresandtheapproachesusedtoincentivizetheminanholisticway

This article explores application of themitigation hierarchy toaddress a specific fishery concern that ofmarinemegafauna by-catchWetakeldquomarinemegafaunardquotoencompasslong-livedspecieswithlowreproductiverateswhicharethereforepotentiallysensitivetoby-catchforexamplemarinemammalsturtlesseabirdsandlargefishwhilewedefineby-catchascatchwhichisnotdirectlytargeted(bearing inmind thecomplexities indefinitionhighlightedbyFAO2011)We limit our discussion tomarinemegafauna by-catch formanageabilityofscopeandbecausethisissueisofparticularcon-cernwithin both the conservation and fisheries realmsHowevermanyofthepointsweraiseareapplicabletoby-catchmorebroadlyIt isalsotheissueforwhichdiscussionoftheapplicabilityofNNLandthemitigationhierarchytomarinesystemshasbeenparticularlyactive(egfollowingthepaperbyWilcoxampDonlan2007)

First we outline a conceptual framework for by-catchmitiga-tionbasedon theapplicationofa sequentialmitigationhierarchytoachieveNNLWethendiscusssomekeyissuesthatariseintheapplicationofamitigationhierarchytomarinemegafaunaby-catchandrelatethemtotheequivalentdebate intheterrestrialsettingWemoveontoconsiderhowincentivestomitigatetheamountorimpact of by-catch can be used to support the application of theframeworkFinallywesumup thepotentialofour framework forimprovingby-catchmitigationoutcomes

2emsp |emspCONCEPTUAL FR AME WORK FOR BY- C ATCH REDUC TION

ToclarifyhowachievingNNLthroughamitigationhierarchywouldwork for marine megafauna by-catch we present a conceptualframeworkrelatingtothetargetlevelofby-catchimpactinafisheryTheapproachcanoperateatarangeoflevelsfromtheglobaltothestock to the individualanimalThemostusual andmost intuitivescaleatwhichNNLcouldapplytoby-catchisatthescaleofafish-erytargetingagivenstockorsetofstockssothisisthescaleweuseinthisexplorationTable1explainsthetermsweusetodescribetheconceptualframework

The approach starts by defining the goal in terms of a desiredchangeinbiodiversitythisiscommonlytakentobeNNLofbiodiver-sitybutthatisnotnecessarilytheonlygoalForexampleintheter-restrialrealmnetgainisawidelyusedgoal(Raineyetal2015)whilein themarine realmby-catchminimization isoften thepolicygoal(exceptfortotallyprotectedspecies)whichmayimplyanetlossorgaininbiodiversitydependingonthecurrentby-catchlevelAnotherpotentialgoalcouldbepopulationrecovery (cf theUSEndangeredSpeciesActWolfHartlCarrollNeelampGreenwald2015)

emspensp emsp | emsp3MILNER- GULLAND Et AL

ThenextstepistodefineaquantitativetargetandassociatedmetricbywhichthegoalwillbemeasuredInthecaseofby-catchofmarinemegafauna one relatively intuitive approach is to de-fine the target as zero net change in population growth rate ofthe focal species caused as a result of by-catch and associatedmitigationmeasures inthecontextofalltheotherfactors influ-encingthatpopulation(aswasdoneeginthestudiesreviewedbyLewisonCrowderReadampFreeman2004)Thedownsideofthis metric is its requirement for monitoring data that can pro-vide trends in population size over time decomposed into vitalrates(survivalfecundity)sothatthecontributionofby-catchandmitigationmeasures tochange inpopulationgrowth ratecanbediscerned Thismay be challenging formanymarinemegafauna(CaswellBraultReadampSmith1998)Othermore readilymon-itored targets couldbebasedonnumbersof animals for exam-plenotexceedingaPotentialBiologicalRemoval(PBR)threshold(RichardampAbraham2013)Thedownsideofnumbers-basedmet-ricsistheirmoreindirectrelationshipwiththeconservationstatusofthespeciesconcerned

Using themetric of net change in population growth rate thebaselinefromwhichgainsandlossesfromdifferentmeasurestakentomitigateby-catchareassessedcouldbeazeropopulationgrowthratesuchthatthepopulationremainsstableatthecurrentlevel(astatic baseline) the projected population growth rate of the spe-ciesintheabsenceofby-catchwhichcouldbepositiveornegativedependingontherelativeimportanceofby-catchinthecontextofotherthreats(adynamicbaseline)oranaspirationalbaselinesuchaspopulationgrowthatXperyeartothepointatwhichitreachessomedesiredsteady-stateabundance(whichwouldneedtobedy-namicgiventhatpopulationshavedensity-dependentgrowth)Suchabaseline is therefore a typeofcounterfactual againstwhichanyimprovement or deterioration in the population of the by-caughtspeciesasaresultoftheimplementationofthemitigationhierarchy

iscompared(iewhatwouldhavehappenedintheabsenceoftheby-catchmitigationmeasures)

Next the different approaches which can be used to attainNNL(orwhatevergoal isset)areassessed intermsoftheireffectonthechosenmetricforexamplethereductioninseabirdmortal-ityfromfittingtorilinesinafisherycanbeassessedintermsofitseffectonthegrowthrateofawanderingalbatross(Diomedea exu-lansDiomedeidae)populationThefourcategoriesoftheterrestrialmitigationhierarchyareavoidanceminimizationremediation(alsoknown as restoration or rebuilding) and offsetting In the case ofmarinemegafaunaby-catchwetakeldquoavoidancerdquotorepresentmea-surestakeninordertoreducetheprobabilityofencounterbetweenpotentially harmful gear and a potentially by-caught individualby separating fishing activity from individuals or stocks of poten-tialmegafaunaby-catch species (seeTable2 for example actions)We take ldquominimizationrdquo asmeasureswhich reduce theprobabilityofcapturebythegeargiventhattheencountercannotberealisti-callyldquoavoidedrdquoThesemeasuresoccuroncethereisspatio-temporaloverlapbetweena fishingvesselandamarinemegafauna individ-ualldquoRemediationrdquoalsooccursatseabutpost-captureandaimstoreduce theprobabilityofmortality givencapture ldquoOffsettingrdquo re-ferstomeasurestocompensateforby-catchmortalitythatoperateseparatelyfromthefocalfishingactivitybutwhichtargetthesamestockoftheby-caughtspecies

Inrealitytherearegreyareasbetweeneachofthesestagesandarangeofwaysinwhichby-catchmitigationmeasurescanbecat-egorizedForexample herewe include restorationand rebuildingactivitiesat thestock level inldquooffsettingrdquobecauseourframeworkis structuredaround individual-levelcaptureprobabilityHoweveranotherapproachmightbetocombineremediationatthe individ-uallevelinacategorywithrestorationrebuildingmeasuresthatim-provepopulationviabilityatthestocklevelsuchasrestockingandhabitatimprovementleavingoffsettingasmeasureswhichbenefit

Term Explanation

Goal Thedesiredchangeinbiodiversityforexamplenonetloss(NNL)ofbiodiversityasaresultofthecombinedeffectofthedamagingaction(egby-catch)andassociatedmitigationmeasures

Target Inourframeworkwedistinguishbetweentheoverallgoalatthepolicylevel(egNNL)andthequantitativetargetwhichoperationalizesthegoalforwhichametriccanbedefined

Metric TheunitsusedtomeasuregainsandlossesinbiodiversityinordertoevaluatewhetherthegoalhasbeenachievedInourcasethisisnetchangeinpopulationgrowthrateofthefocalspeciesasaresultofby-catch+mitigationmeasures

Baseline ThereferencepointagainstwhichNNLisassessedThiscouldbestatic(egcurrentpopulationgrowthrate)dynamic(projectedpopulationgrowthrateintheabsenceofby-catchbutcontinuationofotherprocessesaffectingvitalrates)oraspirational(desiredchangeinpopulationgrowthrate)

Counterfactual Theprojectedchangeinpopulationgrowthrateinthepresenceofby-catchbutabsenceofmitigationmeasuresagainstwhichNNLisassessed(egbusinessasusual)IfthebaselineisdynamicthecounterfactualisthesameasthebaselineotherwisebotharerequiredtofullydefinethescenarioagainstwhichNNLisevaluated

TABLE 1emspExplanationoftermsusedinthemitigationhierarchy

4emsp |emsp emspensp MILNER- GULLAND Et AL

thestockmoreindirectlyoractatthebroaderspecieslevel(suchasrestoration in other locations ormeasures to improve complianceand reduce uncertainty) Howeverwe feel that the clarity of theprobabilisticapproachinourframeworkwhichextendstheclassi-ficationbyHall(1996)isparticularlyhelpful

Ourdivisionofmitigationapproachesintothesecategoriescanberepresentedinthefollowingconceptualmodelrelatingtoapar-ticularby-catchspeciesinwhichtheunitisrateofchangeinpopu-lationsizeasaresultofby-catchanditsmitigation

HereΔλT is the target levelofoverallnetdamage inflictedbyby-catchonthespeciesconcernedmeasuredintermsofchangeinpopulationgrowthratewithrespecttotheagreedbaselineAzeroΔλTimpliesthatthereductioninpopulationgrowthratecausedbyby-catch after avoidance andmitigationmeasures have been im-plementedisbalancedbythegainengenderedbyoffsetmeasuresThereisalsothepossibilityforΔλTtobenegative(thereisstilladdi-tionalpopulationdeclineasaresultofby-catchevenaftermeasurestoreduceit)orpositive(equivalenttonet gainmeaningthatspeciespopulationgrowthishigherthanitwouldotherwisehavebeenasaresultofthecombinationofmeasurestakenunderthemitigationhierarchy)

f(EBtimesBPUE)istheeffectonpopulationgrowthrateoftheby-catch-relevantcomponentoffishingeffortbrokendownintotheby-catch-relevanteffortitselfEBandtheby-catchtakenperunitof that effort BPUEwhere f() is the effect of this effort on theby-caught speciesrsquo population dynamics Thiswould generally becalculatedastheoutputofapopulationmodelAreduction inEB isequivalenttoafisheryavoidingby-catchpartiallyorcompletelyIt could include restricting the fishery to particular areas or sea-sons modification of fishing practices and operations (eg set-tingthegeardeepertoavoiddepthswhereby-caughtspeciesare

prevalent)AreductioninBPUEistheresultoftheat-seameasuresencompassed intheldquominimizerdquoandldquoremediaterdquostepsofthemiti-gationhierarchy

By-catch-relevanteffortEBisasubsetoftheoverallfishingef-fort thatoccurs in thearea inwhichthere is riskofby-catch (E)Given thecomplexitiesof estimatingEB inmanycases itwill benecessarytoapproximateitbyE(egTuckPolacheckampBulman2003) Thismay be problematic for example Baacuteez etal (2007)show that loggerhead turtle (Caretta caretta Cheloniidae) by-catchintheMediterraneanwasnotcorrelatedwithfishingeffort(measuredasnumberofhooks)by-catchwasinsteadstronglyre-lated todistance from thecoastThey suggest that thiswasnotbecauseturtleabundance isa functionofdistance (whichwouldhave impliedagradient inEB) butbecause fisherbehaviourvar-iedalthoughtheyleftinvestigationofthemechanismsforfurtherresearchBPUEisafunctionofcatchabilityoftheby-caughtspe-ciesaswellasEB forexampleWardLawrenceDarbyshireandHindmarsh(2008)carriedoutamultispeciesanalysisoftheeffectsof nylon leaders on catch rates and showed that catch reducedwithnylonforsharksbluemarlin(Makaira nigricansIstiophoridae)and snake mackerel (Gempylus serpens Gempylidae) and in-creased for bigeye tuna (Thunnus obesus Scombridae) and blackmarlin(Istiompax indicaIstiophoridae)TherelationshipsbetweenEEB andBPUEare likely tobe complex and confoundedTherehavebeen limitedexplorationsof these relationships inby-catchdatasetswhich typically suffer from low sample sizes and zero-inflationrequiringspecializedmodellingtechniques (eg thespa-tiallyexplicitBayesianhierarchicalmodelsofSimsCoxampLewison2008)By-catchmitigationmayuseasuiteofinteractingmeasuresfrom several levels of the mitigation hierarchy (Table2) whichchangeovertimeaddingfurthertothecomplexityofseparatingE EBandBPUE(asdiscussedfortargetfisherydatabyBishop2006)Wedonothereattemptfurthertoclarifytheserelationshipsbutakeyresearchneedistodisentanglethesevariablesinanempiricalsetting

(1)ΔλT= f(

EBtimesBPUE)

minusOT

Step of the hierarchy Example measures

Avoidance Excludingfishingfromtheareas(no-fishingzones)seasons(closedseasons)ortimesofdaywherethesespeciesaremostvulnerable

Minimization Usingon-vesseltechnologieswhichaimtoreducethenumberofencounteredindividualsthatarecapturedduringfishingoperationssuchastorilinesforscaringseabirdsawayfromlonglinesorsonicdevicestosignalnetstomarinemammals

Remediation Deviceswhichenableindividualstoreleasethemselvesfromthegear(selectivitygridsturtleexcluderdevices)ortobereleased(egMedinapanelsoperatedintunapurse-seinefisheriestoletdolphinsescapebeforegettingonthedeck)orreleasingthemondeckandprovidingforasafereturntothesea(egalargemeshsoftwebbingcargonetcanbeusedtoldquosieverdquoarayfromthecatchandliftitoverthesideofthevesselFrancis2014)

Offsetting Eradicatinginvasivepredatorsonislandswhereseabirdsnestrestoringhabitatrestockingwithhatchery-raisedindividualsimprovingby-catchperformanceofothergeartypesinthearea

TABLE 2emspExamplesofmeasureswhichcanbetakenundereachstepofthemitigationhierarchy

emspensp emsp | emsp5MILNER- GULLAND Et AL

OT is the net effect on population growth rate of policiesaimingtoimprovetheoverallviabilityoftheby-caughtspeciesrsquopopulation representing ldquooffsettingrdquo of the damage caused Itrepresents the expected effects of measures to improve con-ditions for individuals which would not have been at risk ofby-catch at that particular stage in their lives or location Forexample supplementation in nesting areas (for turtles) resto-rationofnestinghabitat(forseabirds)orimplementationofpro-tectedareasaimedatdemographicgroupsnotdirectlyimpactedby fishing (calving areas for cetaceans juvenile concentrationsforfish)

3emsp |emspOPER ATIONALIZING THE FR AMEWORK

In Table3we illustrate the application of the by-catchmitigationframework using four examples from different fisheries and by-catchtaxaSpecificsolutionstoEquation1couldcomefromtakingintoaccount the regulatory cultural andeconomicconditions inaparticularfisheryForinstanceoncethefocalby-catchpopulationhasbeendefinedthenitispossibletosolvetheequationbyassign-ingfactorsaffectingdecision-makingincludingcostIfaleast-costapproachtoby-catchgoalsisappropriateEBBPUEandOT could be expressedasfunctionsofcosttosolvetheequationforagivenΔλT Another approachwould be tomaximizeΔλT subject to a budgetconstraint

Table3highlightsthatthereisnotalwayspotentialforeffec-tive action at each level of the hierarchy for some species (egoceanicwhitetipslonglines)theremaybelimitedpotentialatalllevelsTheframeworkisawayoforganizingandstructuringthink-ingaboutby-catchmitigationandenablingmitigationeffective-nesstobeassessedagainstaconcretelydefinedandmeasurabletargetItsfunctionisnottoproposenewwaysofdoingby-catchmitigationforcasesliketheseIfonusingtheframeworktoanal-yse the effectiveness of the measures available for a given by-caughtstockitisfoundthatitisnotpossibletoreachthechosentarget(egNNL)thendifficultdecisionsmustbemadeForexam-plethetargetmayneedtochangewhichcouldimplyanaccep-tanceofcontinuingdeclineoftheby-caughtstockOrthefisherymustbe restructured in away that reducesby-catcheffectively(maybeevencloseddown)Orinvestmentmustbemadeintotech-nological innovation todevelopnewways to reduceby-catch Ifitisfoundthatthedataareinadequatefortheanalysisrequiredthenthedecisionmustbemadeeithertoinvestinimprovingtheevidencebaseor to recognize that it is not possible to evaluatewhether by-catch mitigation has been effective in reaching theagreed goal The frameworkrsquosmain utility therefore is tomakethesechoicesexplicit

Equation1couldbeextendedtohandlemultiplespeciesvary-inggeartypesorheterogeneousby-catchreductionmethodsForinstanceBPUEcanbedecomposedintoseveralcomponentsrepre-sentingthedifferentstagesoftheprocessIfBPUErepresentsthesumofindividualsdeadonarrivalindividualscapturedanddyingon

thevessel and individualsdyingafter live releasewecan rewriteBPUEasaseriesoffactors

whereBDOAistheby-catchperuniteffortthatarrivestotheboatdeadBOBistheby-catchperuniteffortthatarrivestothevesselalivePDVistheproportiondyingonthevesselandPDRisthepro-portiondying after release For instance a higherproportionofby-catchofseaturtlesandotherspeciesarrivestotheboatdeadwhenusinglonglinesthataresetdeepsuchasthoseusedforbig-eyetunathatcanbesetmorethan300mdeepwhencomparedto a shallow set longline such as those used inmany nearshoreartisanal fisheries (Andrakaetal2013HallSwimmerampParga2012Swimmeretal2006)ThisdifferencewouldappearintheBDOA termSuchadecomposition illustratestheflexibilityofthisframeworkinhandlingfishery-andspecies-specificfeaturesandalsoservestohighlightareaswheredifferentmitigationmethodswouldhavethegreatestinfluence(egShiodeHuShigaYokotaampTokai2005)Anotherextensiontothebasicframeworkwouldbetoconsiderexplicitlytheuncertaintysurroundingdifferentel-ements of the conceptual model and the impact of this uncer-taintyonwhichelementofby-catchmitigationshouldbeafocus(Table3)

It is important tonote that this equation isnot a truebioeco-nomicequationtobesolvedRatheritisaconceptualframeworkinwhichwemakethecomponentsofthemitigationhierarchyexplicitinordertoguidethinkingtowardsamoreholisticapproachtoad-dressingby-catchItalsodoesnotrepresentahierarchysuchasisrequiredinterrestrialsystemsTomakethisequationintoahierar-chyratherthanamodelforleast-costmitigationofby-catchitcouldbesetupasagoalprogrammingfunctionwithsequentialsolutionstoeachelementsummedtoproducethefinalmitigationoutcomeInoperationaltermsthistranslatesintoapresumptionthatinvestmentandeffortshouldbefocusseddifferentiallyonsequentialelementsofthemodelstartingwithEBthenBPUEthenOTsothatoffsettingrelatesonly to theunavoidable residualharmonceall other stepshavebeentakenThismaybereflected intheemphasisplacedontheincentivesgiventofisherstochangebehaviourpertainingtose-quentialelementsofthehierarchyinthetimingoftheoffsetorinthedispositionofthefundingforresearchandconservationactionallocatedbygovernment

ResearchiscurrentlyongoingtooperationalizeEquation1tore-duceturtleby-catchofasmall-scalegillnetfisheryoperatingoutofSanJoseportPeru(Alfaro-Shiguetoetal2010)Currentlyasmall-scalecertificationschemeisundertrialbytheNGOProDelphinuswhich aims to give premium prices for fish caught by skippersabiding by best-practice by-catch reduction guidelines (J Alfaro-Shigueto and J Mangel personal communication) The researchentailscollectingdetailedeconomicdatafromallgillnetvesselstounderstand the economic costs involved in fishing operations tocalculatethepotentialadditionalcostsofmeasuresateachstagein

(2)BPUE=BDOA+PDVtimesBOB+(

1minusPDV)

timesBOBtimesPDR

6emsp |emsp emspensp MILNER- GULLAND Et AL

TABLE 3emspSummaryofoptionsforby-catchmitigationstructuredaccordingtothemitigationhierarchyforfourcase-studies

Fram

ewor

k st

ep

Cas

e- st

udy

Alb

atro

sses

lon

glin

esTu

rtle

slo

nglin

esRa

ysp

urse

sei

nes

Oce

anic

whi

tetip

slo

nglin

es

Definingtheproblem

Fisheryandspatial

extent

Braziliandomesticindustrialcoastallongline

fleet

EasternPacific(coastalandpelagic)

small-scalecommerciallonglinefishery

Tunapurse-seinefisheryof

theeasternPacific

AsianandEUlonglinetunafisheriesinthe

Indi

an o

cean

Targetspecies

Variousspeciesofsharkandswordfish

Mahi-mahi(

Cory

phae

na h

ippu

rus

Coryphaenidaeseasonal)tunasharks

(mostlysilkyC

arch

arhi

nus f

alci

form

is

Carcharinidae)billfish

Variousspeciesoftuna

Variousspeciesoftuna

By-catchspeciesof

conc

ern

Albatrossamppetrelspeciesparticularconcern

forcriticallyendangeredTristanalbatross

(Dio

med

ea d

aben

nenaDiomedeidae)

Oliveridley(L

epid

oche

lys o

livac

ea

Cheloniidae)greenblack(C

helo

nia

myd

asCheloniidae)hawksbill

(Ere

tmoc

hely

s im

bric

ataCheloniidae)

loggerhead(PeruandMexico)and

leatherback(D

erm

oche

lys c

oria

cea

Cheloniidae)

Sevenmobulidspecies

includingCITES-listedM

anta

bi

rost

ris(Mobulidae)and

M a

lfred

i(Mobulidae)

caughtmostlyalivein

dolphin-associatedor

free-schoolsets

OceanicwhitetipsharkVulnerableonIUCN

redlistretentionbannedbytunaRFMOs

listedonCITESAppendixII

By-catchtarget

(Δλ T)

BraziliangovernmentMinimizeby-catch

Rulesfocusontargetsforuseofminimizing

measuresratherthanonby-catchnumbers

NotwelldefinedRFMOssuggest

minimizingby-catchCouldconsiderPBR

foroliveridleyszerocatchforleather-

backs(reflectingtheirrespective

populationstatus)

IATTC(2015)zeroretention

storingorsellingandlive

releaseofby-caughtrays

whenpossibleImplies

by-catchminimization

Targetby-catchlevelnotdefineddueto

uncertaintyRFMOsbanretentionlanding

andtrans-shipment

Mitigationhierarchyelement

Avoid

[timeareaclosuresnight-timesetting]

[timeareaclosuresdeeperlines]

[timeareaclosures]

[deepsetting]

Minimize

[torilineslineweights]

[monofilamentlinecirclehooks(not

leatherbacks)]

ndash [hardtoavoidcatching]

[monofilamentlinecirclehooksbanon

steelleaders]

Remediate

ndash [hardtoreleasealive]

[improvedhandling]

[improvedhandling]

[shortsets]

Offset

[invasiveeradication]

[beachprotection]

[illegaltrade]

[informationgatheringillegaltrade]

Factorsaffectingoperationalization

Scopefor

incentives

Participatoryresearchonbarrierstouptakeof

minimizationmeasuresPositiveincentives

forthoseusingnewmeasurespaidforby

forexamplefisheries-widelevy

Certificationsustainabilitystandardsin

exportmarkets

Transitionalpaymentsto

promotebetterhandlingon

deckhenceimproving

survival

Ifinformationgatheringseenasavalidoffset

duetohighuncertaintyfundingatagging

schemecouldincentivizefisherstocollect

dataonsharkcatchratesurvivalof

releasedsharksby-catchhotspotsto

supportimprovementsacrossthewhole

mitigationframework

(Continues)

emspensp emsp | emsp7MILNER- GULLAND Et AL

themitigationhierarchy In theabsenceofhighqualitypopulationdatawithwhichtoparameterizeamodelaPBR-basedapproachisbeingusedtosetatargetby-catchlevel intermsofnumberof in-dividualsofeachoftheturtlespeciescaughtinthefisheryExpertopinionfromfishersandProdelphinusstaffsupplementedbydatafromalong-runningby-catchobserverprogrammeoperatingoutoftheport(Alfaro-Shiguetoetal2011)givesthepotentialreductioninturtleby-catchnumbersasaresultofagivenmitigationapproachInterviews and focus groups with fishers provide understandingof their preferences for different by-catchmitigation approachesbarriers and constraints to implementation and potential partici-pationindifferentincentiveschemesthiscanbesupplementedbyDiscreteChoiceExperimentsprovidingempiricalestimatesforpref-erencesforcombinationsofby-catchreductionmeasures(cfRogers2013)Thisfieldresearchproducesashort-listoffeasiblemitigationmeasuresateachstageinthemitigationhierarchyforcostingandtesting(egspecificareasortimesforfisheryclosureunderavoid-ancecombinationsofhooktypesandnetmodificationundermini-mizationtraininginturtlehandlingandreleaseforremediationandimprovingby-catchperformanceofothergeartypesintheareaforoffsetting)Thisenablestheanalysisoftheeffectivenessandcostof various combinations of by-catch reduction strategies framedwithinthefourstepsofthemitigationhierarchy(avoidminimizere-mediateoffset)withacleartargetby-catchreductiongoalinmind

4emsp |emspCOMPARING KE Y DEBATES BET WEEN TERRESTRIAL NNL AND BY- C ATCH MITIGATION

41emsp|emspThe hierarchical nature of mitigation

Terrestrial situationsareusuallyviewedas requiringastricthierar-chywithavoidanceminimizationandremediationtakingprecedenceoveroffsetsPartofthereasonforthishierarchymaybesocietalval-uesandexpectationsbut also it is a reflectionof reversibility anduncertaintyTheterrestrialmitigationhierarchywassetuptoaddresshabitatdestructioncausedbydevelopmentwhich iseffectively ir-reversiblehenceavoidanceisstrictlypreferredfromaconservationperspective Inpractice avoidancehasbeenaneglected step andmuchofthedisquietaboutbiodiversityoffsettinghasbeenbecauseofthetendencytopaylipservicetoavoidanceandfocusinsteadonoffsetswhich thenmay be implemented on paper only (HoughampRobertson2009Phalanetal2017)EvenwithperfectenforcementandcompliancewithmeasuresfurtherdownthemitigationhierarchythestrictavoidanceofhabitatlossismorecertaintolimitimpactthanreducinglossesinthecourseofapotentiallydamagingactionwhichismorecertainthanrestoringdamageafterthefactorcompensatingforitwithactionselsewhereOfteninterrestrialsystemsmultipliersareusedattheoffsetstagetoreflectthisuncertaintyrequiringthatanadditionalamountofequivalentlandisprotectedinanoffsetoverandabovetheamountthatislostduringthedevelopment(withtheratiooflandoffsettolanddestroyedinthe10sto100sdependingonthecircumstancesMoilanenVanTeeffelenBen-HaimampFerrierFr

amew

ork

step

Cas

e- st

udy

Alb

atro

sses

lon

glin

esTu

rtle

slo

nglin

esRa

ysp

urse

sei

nes

Oce

anic

whi

tetip

slo

nglin

es

Major

uncertainties

Lackofspecies-levelidentificationof

by-catchlackofunderstandingof

compliance

Lackofecologicalknowledgeofturtle

populationtrendsampdistribution

Potentialforsignificantadditional

by-catchfromcoastalgillnetfishery

Impactofcatchonmobulid

survivalPredictorsof

mobuliddistributions

Lackofobserversorreportingsoverylimited

understandingofby-catchlevelsspatio-

temporalencounterhotspotspost-release

survivalcompliance

Keyobstacle

Compliancewithexistingrulesmustbe

improved

Fundingforalternativestofishingata

largeenoughscaleLongtimelagand

uncertaintyinoffseteffectiveness

Limitedknowledgeofmobulid

distributionsmakes

avoidancedifficult

Lackofmonitoringlimitsoptions

Overallassessment

Existingmeasuresforimprovingimplementa-

tionofminimizationstepalreadyexistbut

needincentivizingoffsettingcouldprovide

short-termgainstocomplementthese

Targetedfundingcouldfacilitateimprove-

mentsthroughoutthehierarchyBest

approachmaydifferbyspecies(particu-

larlyleatherbacksvsothers)

Focusonremediationstepis

currentlythemainoption

avai

labl

e

Somepotentialforminimizationthrough

deepsettingbutchallengingtochange

behaviourinthisfisheryelectronic

monitoringsystemswouldhelp

Keyreferences

BugoniManciniMonteiroNascimentoamp

Neves(2008)Wanlessetal(2009)

Alfaro-ShiguetoDuttonampMangel(2007)

Halletal(2012)Andrakaetal(2013)

JonesampFrancis(2012)Hallamp

Roman(2013)Crolletal

(2016)Fowler(2016)

Tolottietal(2015)

Ticksindicatethepotentialforactionatdifferentstepsofthehierarchybasedonfeasibilitycurrentknowledgeandimpactonmortality(

=highpotential

=somepotential

=limitedpotential

ndash=nopotential)TextinbracketsgivessuggestedmeasuresateachlevelofthehierarchytheseareillustrativeratherthandefinitiveTheinformationforthecase-studiesisbasedontheexpertknowledge

oftheauthorsthroughtheirinvolvementinmanagementoftheby-catchissueinthesefisheriesRFMOregionalfisheriesmanagementorganizationPBRpotentialbiologicalremoval

TABLE 3emsp(Continued)

8emsp |emsp emspensp MILNER- GULLAND Et AL

2009)Bycontrastinfisheriessettingstherehavebeensuggestionsthatdependingonthelegalenvironmentitmaybemoreappropriateforoffsetstobeusedaspartofaleast-costconservationapproachalongsidemoretraditionalmitigationmethodsratherthanasthelaststep inamitigationhierarchy (DuttonJosephSquiresampWilliams2011DuttonampSquires2008WilcoxampDonlan2007)

42emsp|emspOut- of- kind offsets

Out-of-kind offsets are those which do not act to increase theimpact-affectedbiodiversityIntermsofourconceptualframeworktheyareoffsetswhichdonotacttoincreasethepopulationgrowthrateoftheby-catch-affectedfocalpopulation(Equation1)Forex-ampleonesuggestedbenefitof raising funds foroffsetting fromaby-catchtaxonfishersisthattheproceedsfromsuchataxcanfinanceoffsetselsewherewithintherangeoftheby-catch-affectedpopulation (Dutton amp Squires 2008) Although not a true offsetunderamitigationhierarchyfundsfromtheCaliforniadriftgillnetindustry in 2002 financed sea turtle nesting site conservation inBajaCaliforniaforcompensatorymitigationofseaturtleby-catch(Jannise Squires Seminoff amp Dutton 2010) In terrestrial (andmarine)systems itcanbemorechallengingtodefinethe impact-affected biodiversity because impact is rarely as clearly linkedtoagivenspeciesandstockas it is forby-catchBecauseofthisthelocationandbiodiversitytargetofconservationactionsfallingundertheldquooffsetrdquoheadinghassometimesbeenlooselyrelatedtotheactual impactBest-practicestandardsstatethatoffsetsmustbeimplementedasclosetothedamagingactivitiesaspossibleandfocusonbiodiversityassimilaraspossibletothatwhichhasbeenimpacted (BBOP 2012) However there have also been calls forldquoout-of-kindrdquooffsetsthatgivemoreconservationbang-for-buckbyfocussingonthreatenedspeciesorrarehabitatsorareasinneedofconservation rather than the impactedareasor specieswhichmay be considered less ldquovaluablerdquo for conservation (Bull Hardyetal2015)Thishasledtosubstantialdebateastotheappropri-atelimitsonthegeographicscaleandbiodiversityfocusforoffset-ting(egApostolopoulouampAdams2017)Italsodrawsattentiontothesubjectiveanduser-definednatureof theword ldquobiodiversityrdquo(Morar ToadvineampBohannan 2015) As it is impossible fully tooperationalizetheconceptimplementersofthemitigationhierar-chyhavelatitudetointerpretbiodiversityaccordingtoforexampleeaseofmeasurement perceived societal valueormitigation cost(Maron etal 2016) In our casewe take a narrow focus on theby-caughtspecies itself this is in linewithmuchof the literatureon by-catch but notwith the broader discourses on ecosystem-basedapproachestomarinemanagementandecosystemservices(RosenbergampMcLeod2005)Thesediscoursessuggest theneedforamorefunctionalecosystem-basedapproachtononetlossofbiodiversitythishasyettotranspireeitherinthemarineorintheterrestrialliteraturepossiblybecausesubstantialchallengesinde-finingimpact-affectedbiodiversitytheninevitablyensue

Asmarinemegafauna stocks are often transboundary andmi-gratorydefiningtheappropriatespatialunit foroffsettingmaybe

achallengebecause themosteffective location foranoffsetmayormaynotbewithintheareaofinfluenceofagivenfisheryClearlyandpreciselydefining the spatial unitwithinwhich themitigationhierarchywill be implemented during theprocess of defining theoverallgoal(suchasNNL)isvitalThisunitshouldreflectthescaleoverwhichanactionwillaffectλToffsetswhicharewithinthedis-tributionofthefocalstockoftheby-caughtspecies(asdefinedforEquation1)arenotout-of-kindHoweverchallengesemergewhenthe appropriate spatial unit for offsetting activities is different totheappropriatespatialunitforotherelementsofthemitigationhi-erarchywhicharelikelytobedefinedinsteadbyjurisdictionalareaor target fish stock distribution Inmany fisheries the species af-fectedbyby-catchmaynotbewellenoughknownandoffsetsmayaccordinglyneedtobebroadlytargetedtobenefitanypotentiallyaffectedspeciesTrueout-of-kindoffsetswouldincludefundingtheconservationofunaffectedspeciesorstocksofhabitatsnotusedbythefocalstockorcontributionstoaconservationfundwithoutaclearcommitmentthatthefundsaretobespentonincreasingλT for thefocalby-caughtstockTheseareunlikelytoformpartofbest-practiceguidanceforby-catchoffsets

43emsp|emspResearch as an offset

Arelatedareaofactivecontroversyformarineby-catchiswhetherresearchor informationgatheringshouldbeseenasavalidoffsetmechanism The rationale is that this research could be used toreduceuncertaintypromote innovationand thereby improveout-comes for by-caught species albeit indirectly An offset could beusedto incentivizebetterdatacollectionfor instanceusingaby-catchlevytopayfortaggingortoputby-catchobserversorelec-tronicmonitoringsystemsonboatsThismightbeapreludetolatermitigation or avoidance activities once more is known about thebiological settingWhether research activities could appropriatelybeconsideredaspartofanldquooffsetrdquoiscontroversialmdashinsomecasesan indirectbenefit to theby-caught stockmightbe clearly appar-ent(egtheoceanicwhitetip(Carcharinus longimanusCarcharinidae)case-studyinTable3)whileinothercasesusinginvestmentinre-searchasanoffsetcouldbeseenasacaseofmoralhazardpoten-tially compromising scientistsrsquo independence and having at best ahighlyindirectrelationshiptoNNLoftheby-caughtspeciesAnotherviewisthatreducinguncertaintyisacoreresponsibilityofoperatingafisherywhichthereforeshouldbebornebythemanagementau-thorityorfishingbusinessesInterrestrialsystemsthesedilemmasalsoexistbutthesentimentismuchmoreclearlyexpressedthatre-searchactivitiesarenotappropriateoffsets(BullGordonWatsonampMaron2016)

44emsp|emspIncentivizing implementation of mitigation measures

Thefactorsthatdrivedecision-makingaboutmegafaunaby-catchreduction (by skippers companies fishery managers policymak-ers and other stakeholders) include legal obligations tominimize

emspensp emsp | emsp9MILNER- GULLAND Et AL

by-catch at the national or international levels (eg FAO 2011Rice 2014) the availability and quality of technical fixes associ-atedcosts tofishers limitsonaccesstoseafoodmarketsaswellassocietalpressuresHowevermuchresearchonby-catchreduc-tion focuses on identifying and implementing technicalmeasuresto reduceBPUE rather thanon the social andeconomicbarriersto implementation (Campbell amp Cornwell 2008) Technologicalinnovation to improve BPUE needs to be appropriately incentiv-izedwitheffortsmadetoensurethatsuchmeasuresareascost-effective as possible for fishers (Gjertsen Hall amp Squires 2010Lent amp Squires 2017) However it often happens that even ap-parently suitable by-catchmeasures are notwidely implemented(eg Damalas amp Vassilopoulou 2013 Orphanides amp Palka 2013RadzioSmolinskyampRoosenburg2013)Inthesecasesthedegreeofnon-implementationandthereasonsbehinditneedstobeun-derstoodsoitcanbeaddressed(Coxetal2007)Thesetypesofconsiderationarealsonotwellresearchedintheterrestrialoffset-tingliteraturebecausecomplianceispoorlymonitored(BullSuttleGordonSinghampMilner-Gulland2013)andthereislittlesupportfor researchon thebarriers to implementationofamitigationhi-erarchyandhowtosupportdeveloperstoaddressthesebarriers(BullBryantBakerampMilner-Gulland2015)Thesocialimpactsofimplementingabiodiversitymitigationhierarchyonresourceusersarementioned inguidance (egBBOP2012)buthowtomeasureandaccountforthemisverypoorlyunderstoodThefewstudiesin-vestigatingdeliveryofpromisedoffsetmeasuresinterrestrialsys-temssuggestaverypoorrecord(QueacutetierRegneryampLevrel2014)Therefore the social side of implementing the mitigation hierar-chyand incentivizingcompliance isanarea thatneedsmore andmoreactiveresearchwithinboththeterrestrialandmarinerealms(FultonSmithSmithampvanPutten2011)Thisisparticularlytruewhentheburdenof implementingmitigationapproaches isbornebyrelativelysmall-scaleproducersratherthangovernmentsormul-tinationals(egthepelagiclonglinefisheriesinTable3)

45emsp|emspSocietal limits

Foraspeciesathighriskofextinctioncompleteavoidanceofby-catchmightbethemostdesirablepolicyfrombothamanagementagency and societal perspective In addition with emblematic orhighlythreatenedmarinemegafaunaitmaybeviewedbymembersof the public asmorallywrong to kill any individuals even ifmiti-gationisinplace(egMauirsquosdolphinHamneretal2014) leadingtopressureongovernmentstoreflectthisethicalconcerninregu-lationsThesedilemmasecho the issueof thresholds in terrestrialoffsetswhichrecognizesthattherearesomecriticalareasinwhichdevelopmentisnotsocietallyappropriateregardlessofthepoten-tialformitigationandotherareasinwhichthemitigationhierarchycan be appropriately applied (Bull etal 2013) Examples of loca-tionswhereathresholdapproach isseenasappropriate interres-trial systems include the habitat of highly endangered species orecosystemswhich are limited in extent and irreplaceable (such asoldgrowthforest) In terrestrialsystems therefore themitigation

hierarchyisseenasmostappropriateforapplicationinmorecom-monanddegradedhabitatssuchasfarmlandSimilarlyinfisheriestheremaybesomesituationsinwhichthestockssubjecttoby-catchare so precious or threatened that no level of threat from fishingcanbecontemplatedandotherswherefishingsubjecttoNNLandthemitigationhierarchyisasociallyacceptableapproachInsitua-tions inwhich trade-offs between conservation and developmentareseenasnecessaryoracceptablebywidersocietyasociallicencetooperatemaybegainedthroughadoptingoffsetsintheabsenceofregulationForexampleinsub-SaharanAfricaseverallargedevel-opmentprojectsareattemptingtooffsettheirimpactsongreatapesandtheirhabitats(Kormosetal2014)Aby-catchequivalentmightbe fishing companies voluntarily donating funds for turtle nestingbeachrestorationintheirareaofoperationinadditiontocomply-ingwithregulatoryby-catchmitigationmeasuresThesemeasuresmayimprovetheimageofthecompanywiththegeneralpublicbuttoavoidaccusationsofldquogreenwashingrdquotheireffectivenessneedstobeproperlyscrutinized(Bulletal2016)Transparentlyembeddingthesetypesofactionswithinamitigationhierarchysuchasweareproposing and critically evaluating their contribution to increasingthepopulationgrowthrate(asperEquation1)wouldbeonewaytopromptsuchscrutiny

46emsp|emspUncertainty

The nature of the uncertainties surrounding biology and enforce-ment in themarine setting raisesquestions about theorderingofsteps in themitigationhierarchy inaway that isdissimilar to ter-restrialsystemswherethehierarchyofuncertaintiesmaybecleareranduncertaintyisgenerallylowerForexampleitmaybethattheimpactonoverallpopulationgrowthrateofanoffsetmeasurelikeeradicating invasivespecies fromaseabirdnestinghabitat isbothless uncertain and more cost-effective than avoidance measuressuchasclosingareaswhichmayormaynotbefrequentedbyadultseabirds in a given time-periodGenerally though itmightbe as-sumedthatmeasureswhichtargetlifestagessubjecttohighlevelsofnaturalmortalityorwithinwhichindividualcontributiontoover-allpopulationgrowthrateislow(egheadstartingjuvenileturtles)maybelesseffectiveinachievingNNLthanmeasureswhichtargetreproductivelymatureadultfemales(suchaslivereleasesHeppellCrowderampCrouse1996)Howeverbeforeimplementinganoffsetthataimstoimprovethesurvivalofonelifestageinordertocom-pensatefortheby-catchmortalityofanotherarobustassessmentoftheconsequences(withassociateduncertainties)shouldbecar-ried out through detailed population modelling based on strongempiricalstudies(cfWallaceHeppellLewisonKelezampCrowder2008)Interrestrialsystemstherequirementsequentiallytoapplythemitigationhierarchyisbroadlyunchallengedbutactuallysimilararguments apply For example habitat restoration sits above off-settinginthehierarchyandyetitisalong-termuncertainprocesswhichmayinsomecircumstancesbemuchlesspreferabletoanoff-setusingawell-establishedapproachwhichishighlylikelytoleadtoconservationgains

10emsp |emsp emspensp MILNER- GULLAND Et AL

47emsp|emspTemporal considerations

Thetimingofoffsetsinrelationtootherelementsofthemitigationhierarchyhasbeenthesubjectofdebatewithintheterrestriallitera-tureThemainsuggestionforaddressingthetemporarylossofbio-diversitywhileoffsetscometofruitionhasbeenadoptingmitigationbankingwherebyoffsetsareimplementedinadvanceofpotentiallydamagingactivitiesprovidingbiodiversitycreditswhichcanbeusedtocompensateforlaterlossesThisbothremovesanelementofun-certaintyfromtheoffsetimplementationandreducesthetimelagbetweenlossandgain(Mann2015)Withrespecttomarinemega-faunaby-catchflexibilityintimingprovidesadditionalscopeforcostreduction and benefit enhancementwhichmay not be present intraditionalhabitat-basedterrestrialoffsetsForexampletemporarymeasuressuchasashort-termby-catchtaxtofundanoffsetmaybeusedifmitigationoravoidancemethodstaketimetocomeonlineorifatemporarynudgeisenoughtocausebehaviouralchangeThismightbethecaseifapolicywasneededtoinducefisherstotakeupnewgeartoavoidthecostofanoffsetorifconcernsaboutsafetyoryieldreductionsduringthetransitiontonewgearcouldbeallayedbyatemporarysubsidyforearlyadoptersorapaidparticipatorymoni-toringprogrammeto informwider implementation(egthemobu-lidandsharkcase-studiesinTable3)Justasforhabitatrestoration(ZedlerampCallaway 1999) by-catchoffset strategieswhich targetjuvenilestagesof long-livedspecies (eg turtleheadstartingor in-vasive removal fromseabirdnesting islands)may takemanyyearsfor their effects to become apparent in an increase in populationgrowthratesAdditionaluncertaintyisintroducedbythedifficultyinmonitoringpopulationsofmanyby-catch species (eg seabirdsHatch2003)leadingtouncertainestimatesoftheimpactofoffsetactivitiesonpopulationgrowth(seecase-studiesinTable3)Theseproblemsarenot insuperablehoweverpositivetrendshavebeenreportedinturtlepopulationsoverdecadesasaresultofnestpro-tection(egDuttonDuttonChaloupkaampBoulon2005)

5emsp |emspUSING INCENTIVES TO REDUCE BY- C ATCH

Manyoftheexamplesandprinciplesdiscussedaboveeitherimplic-itlyorexplicitlyrelatetotheeconomicsocialinstitutionalormoralincentivesoperatingondifferentactorsinsideandoutsidethefish-erywhichcanbepositiveornegativeWenowturntoadiscussionofhowincentivescanbeusedtoreduceby-catchwithinourframe-workIncentivescanbeputinplacetochangefisherbehaviourwithrespecttoanyoftheelementsoftheframework (avoidminimizeremediateandoffsetTable3)Althoughdiscussedintheliteraturemostof these incentive approaches are yet tobe implemented inthe realworldparticularly forby-catchThereforeuntil empiricalevidenceoftheireffectivenessisavailablethesesuggestionscomewithacaveat

Financial costsofby-catchmitigationactions canarise for in-stancefromlostcatchcapitalinvestmentsinnewgearormitigation

equipmentor the lossofaccesstoafisheryCostsmayalsoarisefromthedeploymentofby-catchobserversortrainingintheuseofnewgearThesecostscanbepaidbyfishingcompaniesorindivid-ualsorbygovernmentsNGOsorseafoodconsumersWhetherornotcompensationforcostsincurredbyfishersisseenasappropri-atedependsonwhetherby-catchreductionisseenasasocialgoodthatfishersareproviding(inwhichcasetheyshouldbecompensatedforit)orasputtingrighttheharmthattheyaredoingtobiodiver-sitywhilegeneratingtheirownprivategain(ineconomiclanguagewhetherby-catchisviewedasanunpricedexternalityinwhichcasetheyshouldpay)Italsodependsonwhethereconomichardshipwillensueacaseforcompensationofby-catchreductioncostsincurredbypeopledependenton fishing for their livelihoodsmaybemoresympatheticallyreceivedbyotheractorsthanacasemadebyalargemultinationalfishingcompany

Ifby-catchisseenasanunpricedexternalityitmightbesociallyoptimaltotaxfishersfortheirby-catchsothatthisexternalityisin-ternalizedThisplacesanexplicitpriceuponby-catch(Boyce1996Pascoeetal2010SquiresampGarcia2014)Theby-catchprice islikely to be incorporated into the price of the target species andtherebybecomespartofthetargetspeciescostThispricecouldbeset differently for different demographic classesof theby-caughtspecies depending on the impact the loss of an individualwouldhaveonthepopulationAllelsebeingequalputtingapriceonby-catchmeans that theseafoodproduct that is the targetcatchbe-comesmoreexpensiveandconsumershave topaymore for theirseafoodreducingdemandTheninprincipleeveryfirminthesup-plychaineveryvesselandeveryconsumerhaveanincentivetore-duceby-catchuntileacheconomicactorrsquosmarginalcostofby-catchreductionequals thecommonpriceofby-catch that theyall faceOffsetsareonewaytopriceandinternalizetheby-catchexternalitycostIfanoffsettingactioniscostlytoimplementandmustbepaidforwith each unit of by-catch it implicitly prices the residual by-catch In this circumstance the effect from a financial standpointisthesameasaby-catchtaxwiththe levelsetbasedonthecostoftheoffsetVariousinstitutionalstructurestosupportthischargeperunitofby-catcharepossiblewithdifferentimplicationsintermsofthedistributionofcostsandbenefitsForexampleaninsuranceschemecouldbepaidintobyfishersthatpaysoutintheeventofaby-catcheventtherebyspreadingthecostofunavoidablerareby-catcheventsOratradablepermitschemecouldoperatesuchthatfisherswhoexperienceaby-catcheventcanbuyapermitwiththecostvaryingdependingondemandforpermits (henceprovidingavessel-levelincentivetoinnovatetoreduceby-catch)

If there isdemandforconservation inan internationalmarketthen price premiums and market access (through eco-labellingsupply chain certification other food sustainability campaignsWardampPhillips2010)orboycottsactingasstrategicthreatsfromconsumers (Kotchen 2013 Segerson 2010) could act as positiveornegativeeconomic leversonthe fisheryprovidingan incentivefor fishers to reduce their by-catch voluntarily (as has been sug-gested for the Brazilianmahi-mahi fishery Table3) For exampletheMarine StewardshipCouncil now includesby-catchmitigation

emspensp emsp | emsp11MILNER- GULLAND Et AL

intheircertificationprocess(MSC2014)Demand-ledleversmaybemoreorlessapplicableatdifferentlevelsinthehierarchyforexam-pleavoidancemayberelativelyhardtoevidencewhileoffsettingmaybelesseasytoselltoaconsumerthanminimizationorreme-diationConcerns about the unintended consequences of positiveincentives (particularlyfordirectsubsidiesratherthanconditionalincentives)maydeterminewhethertheyareanappropriateinstru-mentinagivencaseForexampletheymaybeinappropriateifthereisariskthattheadditionalmoneyisreinvestedinincreasedfishingcapacityor iftheremaybeconsumptionproductionorconserva-tionleakages(transferoftheproblemsomewhereelse)whetheratthe vessel fishery or trans-national levelHigh transactions costsmayalsolimitthebenefitsofincentivesschemes

Otherchangeswhichmayneedtobeincentivizedforsuccessfulimplementationofby-catchreductionpoliciesmaybelessamenabletofinancialmeasuresatleastpartlybecauseitislessclearhowtoassign financial value to theactionsor to thebenefits and losseswhichtheyproduceForexampleperceivedreductionsinsafetyforfishingcrews(fromweightedlonglinesfor instance)arecoststhatmaybehardtovaluefinanciallyOtherprerequisitesfor long-termsustainable behaviour change such as changes in social norms sothatfishingcommunitiesseeby-catchreductionasappropriatebe-haviourortechnicalskillacquisitionsothattheycanusenewmeth-odsmaybeincentivizedbycarefullydesignedinterventionsworkingwithfishers(Halletal2007)Conservationpoliciesbasedoneco-nomic incentives (extrinsicmotivation) are not always superior tothosebasedupon intrinsicmotivation Infact incentive-basedby-catch reduction policy instruments could even be counterproduc-tivebyreducingtheeffectivenessofintrinsicmotivationdependingupon the situation (although the empirical evidence on this topicisweak RodeGoacutemez-BaggethunampKrause 2015) If the changerequiredforby-catchreductiontoworkmeetscultural resistancethenparticipatory researchmightbeespeciallyeffective inbreak-ingdownbarriersbetweenthosewhowantby-catchreductiontotakeplaceandthosewhoactuallyhavetoimplementit(thefishers)ForexampleinAustraliathegovernment-fundedbodyOceanwatchfacilitatesengagementbetweencommunities thefishing industryseafood suppliers and government to improve knowledge sharing(wwwoceanwatchorgau)Innovationiscrucialinfisheriesandfish-ersareaccustomedtoadoptingnewtechnologyorprocessespo-tentiallymakingan incentivizedparticipatory researchprogrammeespeciallyfruitful

Sometimes the most efficient way to solve problems is a so-cial instrumentoran institutionalchange inplaceoforaswellasan economic instrument For example supporting developmentof fisherorganizations rather than instituting a vessel-level taxorsubsidy might provide the impetus needed to change behaviourInstitutingcatchshares(individualtransferablequotas)mayprovideanenablingenvironmentforby-catchreductionforexamplebypro-motingmoreeffectivemonitoring(Grimmetal2012)Experiencein terrestrial system produces similar insights incentive-basedschemeswhichalsobuildcommunitycohesionandsupportthede-velopment or strengthening of localmanagement institutions are

more effective in the longer run than direct economic incentives(Clementsetal2010)

6emsp |emspCONCLUSIONS

The framework we present here is novel It draws upon and ex-tends the frameworks for conceptualizing by-catch developed byHall (1996) and Hall Alverson andMetuzals (2000) It amalgam-atesHallrsquos frameworkwith themitigationhierarchyasused in theEnvironmental Impact Assessment literature (BBOP 2012) Thesuggestions about goals metric andmitigation actions are drawnfromtheempiricalby-catchliteratureandtheissueswediscussin-tegratetheconcernsoftheextensiveterrestrialandnascentmarineoffsetting literature with the by-catch literature The frameworkmakesclear thatanearlycrucial step is toclarify thegoalofanyby-catch reduction policyOverarching goals like those issued bytheConventiononBiologicalDiversity(egAichiTarget11that10ofmarinehabitatshouldbeunderprotectionby2020)needtobetranslatedintooperationaltermswithineachfisheryCurrentlyleg-islatedoragreedby-catch reductiongoals tend tobe less specificthantheycouldbeandthisleadstoproblemsininterpretingthesegoals inordertoplanaby-catchmitigationstrategy(seethecase-studies inTable3 for examples) This ambiguity is tobe expectedwithinnegotiatedtargetsbutitisachallengenonetheless(Maxwelletal2015)Usingacommonunitofby-catch impactsuchastheΔλTwhichweuseherewouldbehelpfulbothinclarifyingexpecta-tionsandevaluatingtheeffectivenessofelementsofthemitigationhierarchy

Once the by-catch goal is known options for implementingavoidanceminimizationremediationandoffsetscanbeclarified(asinTable2)Howeveroutsideof the interconnectedbiologyof theecosystemby-catch isembeddedwithinsocialandeconomicsys-temsDifferentunitsofanalysismaybeneededatdifferent levelsofthehierarchytocopewiththechallengesofincompleteoverlapbetween jurisdictional units fisheries target stocks and by-catchstocksJurisdictionalissuesareimportantandcomplexpotentiallyimpeding implementationFleets interact raisingtheriskofpolicyleakageforexampleifpeopleshifttootherfisheriesgearorliveli-hoodsThereforethescaleatwhicheachelementofthemitigationhierarchyisimplementedislikelytovarywithincentivestomitigateoftenbeingbest appliedat thevessel level focussedon reducingindividualmortalitywhileoffsettingisimplementedatthescaleoftheby-catchspeciesrsquostockWithtransboundaryspeciesunilateralconservationinonejurisdictioncreatesthepotentialforproductiontrade and conservation leakages For example a conserving Statecouldimplementtheavoidancestepandshutdownordramaticallycurtailitsownproductionofswordfishtoreduceseaturtleby-catchbuttheknock-oneffectmaybemoreimportationofswordfishfromfleetswithhigherseaturtleby-catch(RausserHamiltonKovachampStifter2009)

Translatingtheframeworkfromaspeciestoanecosystemlevelwill require consideration of the potential interactions between

12emsp |emsp emspensp MILNER- GULLAND Et AL

by-catchmitigationapproachestargetedatdifferentspecies(Serafyetal 2012) Actions to mitigate by-catch for one group of spe-cies can increase or decrease it for others and so a system-wideapproach isneededForexample changing fromJ-hooks tocirclehookstoreducemortalityofturtlesmaydecreaseorincreasesharkmortality(Andrakaetal2013GodinCarlsonampBurgener2012)In terrestrial systems similar interactions arise and value judge-mentsaremade(whetherexplicitlyorimplicitly)astowhatlossandgain of ldquobiodiversityrdquo translates to in operational terms andwhatelementsofbiodiversitymattermosttoimplementers

Uncertainty is high in ocean ecosystems creating both chal-lengesandopportunitiesinapplyingtheconceptofNNLthroughamitigationhierarchythatincludesoffsettingInparticularformarinemegafaunathereishighuncertaintyintheprocesseslinkinganyel-ementofthemitigationhierarchythroughtochangesinpopulationgrowthrateFurthermore impactscanbelong-termhardtomea-sureandspatiallydiffuseanduncertaintyisnotpredictablyspreadthroughthehierarchyThiscreatesadifferentsetofchallengestothosefacedinterrestrialsystemswhereatleastforsometypesofenvironmentalimpactthelinksbetweenactionandimpactarerel-ativelydirectandmeasurableanduncertaintygenerally increasesthroughthemitigationhierarchy (fromavoidthroughminimizere-mediatetooffset)

By-catch reduction measures have had significant successesoverthelastdecadesasaresultofsubstantialinvestmentoftimeand funding by researchers management authorities conserva-tionorganizationsandfishers(Coxetal2007)Howeverthissuc-cessisnotuniversalJustasforanyfisheriesmanagementissueapoorregulatoryregimelimitedcomplianceandlackofinforma-tionhampereffortstoreduceby-catchInsomeplaceshighlevelsofby-catch limitedoptions formitigationandweakgovernance(leadingtopoorenforcement)cancombinetomaketheby-catchproblemintractableOurframeworkwillnotsolvetheseproblemsHowever itbrings together the full rangeofapproaches forby-catchmitigationinastructuredandsystematicwaywhichrequiresatargettobeexpressedagainstwhichoutcomescanbeevaluatedByexposingareasofuncertaintyanddatadeficiencyitcouldchal-lengescientistsandmanagerstoobtainthedatarequiredproperlytoevaluate theeffectivenessofmitigationmeasuresThis couldthensupportandencourageclearerdecision-makingandprioriti-zationofactionsOurframeworkdemonstratesthattheprincipleof implementing thegoalofnonet loss throughamitigationhi-erarchy isasapplicable tomarinemegafaunaby-catchas to ter-restrial systems where it is already widely used in challengingdata-poorcircumstances

There isuntappedpotential forcost-effectiveby-catchmitiga-tionwhichcouldberealizedwiththeadoptionofthisframeworkandwithconsiderationofnewapproachestoincentivizingby-catchmitigationwithinthestepsofthehierarchyApplyingittoafewcase-studiesinpracticewilldemonstrateempiricallywhereandhowthepotentialforimprovedeffectivenesscouldbestberealizedExistinglegalframeworksoftenprecludeapproacheswhichimplicitlyorex-plicitly permit by-catch including the use of economic incentives

ornewapproachessuchasoffsetsHoweverinthiscontextofdy-namicuncertaintythedividendsofthinkingmorecreativelyaboutby-catchmitigationcouldbehigh

ACKNOWLEDG EMENTS

EJMG acknowledges the Pew Charitable Foundation for its sup-port of thiswork This article originated at a 2013workshop co-organized by NOAA-Fisheries and IUCN-CEEM-FEG entitledldquoMultidisciplinaryWorkshoptoAddressEcosystem-LevelImpactsofFisheriesBycatchonMarineMegafaunaBiodiversityConservationthrough Mitigation Policy Economic Instruments and TechnicalChangerdquo We thank the reviewers for their insightful commentswhichmuchimprovedthemanuscript

ORCID

E J Milner-Gulland httporcidorg0000-0003-0324-2710

R E FE R E N C E S

Alfaro-Shigueto J Dutton P H amp Mangel J (2007) Interactionsbetween leatherback turtles and Peruvian artisanal fisher-ies Chelonian Conservation and Biology 6 129ndash134 httpsdoiorg1027441071-8443(2007)6[129ibltap]20co2

Alfaro-Shigueto JMangel JCBernedoFDuttonPHSeminoffJAampGodleyB J (2011) Small-scale fisheriesofPeruAmajorsinkformarineturtles inthePacificJournal of Applied Ecology481432ndash1440httpsdoiorg101111j1365-2664201102040x

Alfaro-ShiguetoJMangelJCPajueloMDuttonPHSeminoffJ A amp Godley B J (2010) Where small can have a large im-pact Structure and characterization of small-scale fisheries inPeru Fisheries Research 106 8ndash17 httpsdoiorg101016jfishres201006004

Andraka SMugM HallM PonsM Pacheco L ParralesM hellipOrtega D (2013) Circle hooks Developing better fishing prac-ticesintheartisanallonglinefisheriesoftheEasternPacificOceanBiological Conservation 160 214ndash224 httpsdoiorg101016jbiocon201301019

ApostolopoulouEampAdamsWM(2017)BiodiversityoffsettingandconservationReframingnaturetosaveitOryx5123ndash31httpsdoiorg101017S0030605315000782

BaacuteezJCRealRGarciacutea-SotoCJoseacuteMMaciacuteasDampCamintildeasJA(2007)Loggerheadturtleby-catchdependsondistancetothecoastindependentoffishingeffortImplicationsforconservationandfish-eries management Marine Ecology Progress Series 338 249ndash256httpsdoiorg101017S0030605315000782

BBOP (2012) Standard on biodiversity offsets Business and biodiversity offsets programmeWashingtonDCForestTrends

Bishop J (2006) Standardizing fishery-dependent catch and ef-fort data in complex fisheries with technology change Reviews in Fish Biology and Fisheries 16 21ndash38 httpsdoiorg101007s11160-006-0004-9

BoyceJ(1996)AneconomicanalysisofthefisheriesbycatchproblemJournal of Environmental Economics and Management31 314ndash336httpsdoiorg101006jeem19960047

BugoniLManciniPLMonteiroDSNascimentoLampNevesTS(2008)SeabirdbycatchintheBrazilianpelagiclonglinefisheryandareviewofcaptureratesinthesouthwesternAtlanticOceanEndangered Species Research5137ndash147httpsdoiorg103354esr00115

emspensp emsp | emsp13MILNER- GULLAND Et AL

BullJWampBrownlieS(2017)Thetransitionfromnonetlosstoanetgainof biodiversity is far from trivialOryx51 53ndash59 httpsdoiorg101017S0030605315000861

BullJWBryantCBakerJampMilner-GullandEJ(2015December28)Developing measuring and communicating the outcomes of cor-porate biodiversity strategies [pdfdocument]RetrievedfromhttpwwwwildbusinessorgBull_etal_2015_WBLpdf

BullJWGordonAWatsonJEampMaronM(2016)Seekingcon-vergenceonthekeyconceptsinlsquononetlossrsquopolicyJournal of Applied Ecology531686ndash1693httpsdoiorg1011111365-266412726

BullJWHardyMJMoilanenAampGordonA (2015)Categoriesof flexibility in biodiversity offsetting and their implications forconservation Biological Conservation 192 522ndash532 httpsdoiorg101016jbiocon201508003

Bull JW Lloyd S P amp StrangeN (2017) Implementation gap be-tween the theory and practice of biodiversity offset multipliersConservation Lettershttpsdoiorg101111conl12335

Bull JW SuttleKBGordonA SinghN JampMilner-Gulland EJ(2013)BiodiversityoffsetsintheoryandpracticeOryx47369ndash380httpsdoiorg101017S003060531200172X

CampbellLMampCornwellML(2008)Humandimensionsofbycatchreduction technology Current assumptions and directions for fu-tureresearchEndangered Species Research5325ndash334httpsdoiorg103354esr00172

Caswell H Brault S Read A J amp Smith T D (1998) Harborporpoise and fisheries An uncertainty analysis of inciden-tal mortality Ecological Applications 8 1226ndash1238 httpsdoiorg1018901051-0761(1998)008[1226hpafau]20co2

ClementsTJohnANielsenKAnDTanSampMilner-GullandEJ (2010)Payments forbiodiversityconservation in thecontextofweak institutions Comparison of three programs from CambodiaEcological Economics 69 1283ndash1291 httpsdoiorg101016jecolecon200911010

CoxTLewisonRŽydelisRCrowderLSafinaCampReadA(2007)ComparingeffectivenessofexperimentalandimplementedbycatchreductionmeasuresTheidealandtherealConservation Biology211155ndash1164httpsdoiorg101111j1523-1739200700772x

CrollDADewarHDulvyNKFernandoDFrancisMPGalvaacuten-Magantildea F hellip Newton K M (2016) Vulnerabilities and fisher-ies impactsTheuncertain futureofmanta anddevil raysAquatic Conservation Marine and Freshwater Ecosystems 26 562ndash575httpsdoiorg101002aqc2591

Damalas D amp Vassilopoulou V (2013) Slack regulation com-pliance in the Mediterranean fisheries A paradigm from theGreek Aegean Sea demersal trawl fishery modelling discardogives Fisheries Management and Ecology 20 21ndash33 httpsdoiorg101111j1365-2400201200860x

DuttonDLDuttonPHChaloupkaMampBoulonRH(2005)IncreaseofaCaribbeanleatherbackturtleDermochelys coriaceanestingpop-ulation linked to long-termnestprotectionBiological Conservation126186ndash194httpsdoiorg101016jbiocon200505013

DuttonPJosephJSquiresDampWilliamsM(2011)Bellagioblue-print foractiononseaturtlesChapter2 InPDuttonDSquiresampM Ahmed (Eds) Conservation of pacific sea turtles (pp 15ndash36)HonoluluHIUniversityofHawaiiPress

DuttonPampSquiresD (2008)AholisticstrategyforPacificseatur-tlerecoveryOcean Development and International Law39200ndash222httpsdoiorg10108000908320802013685

FAO (2011 January 5) International guidelines on bycatch manage-ment and reduction of discards Rome Italy Food and AgricultureOrganisation [pdf document] Retrieved from httpwwwfaoorgdocrephelliptba0022t00pdf

Finkelstein M Bakker V Doak D F Sullivan B Lewison RSatterthwaite W H hellip Henry R W (2008) Evaluating the po-tential effectiveness of compensatory mitigation strategies for

marinebycatchPLoS ONE3 e2480httpsdoiorg101371jour-nalpone0002480

FowlerSJ(2016January5)Draft best practice mitigation guidelines for sharks and rays taken in purse- seine and long-line fisheries Convention on Migratory Species[pdfdocument]RetrievedfromhttpwwwcmsintsitesdefaultfilesdocumentCMS_Sharks_CWG1_Doc_3_2pdf

FrancisMP(2014)Survival and depth distribution of spinetail devilrays (Mobula japanica) released from purse-seine catches NIWA ClientReportNoWLG2014-2WellingtonNewZealandDepartmentofConservation

Fulton E A Smith A D Smith D C amp van Putten I E (2011)Human behaviour The key source of uncertainty in fish-eries management Fish and Fisheries 12 2ndash17 httpsdoiorg101111j1467-2979201000371x

GardnerTAHaseABrownlieSEkstromJMPilgrimJDSavyCEhellipTenKateK(2013)BiodiversityoffsetsandthechallengeofachievingnonetlossConservation Biology271254ndash1264httpsdoiorg101111cobi12118

GjertsenHHallMampSquiresD(2010)IncentivestoaddressbycatchInRAllenJJosephampDSquires(Eds)Conservation and manage-ment of transnational tuna fisheries (pp225ndash250)Ames IAWiley-Blackwellhttpsdoiorg1010029780813820262ch14

Gjertsen H Squires D Dutton P amp Eguchi T (2014) Cost-effectivenessofalternativeconservationstrategieswithapplicationtothePacificLeatherbackTurtleConservation Biology28140ndash149httpsdoiorg101111cobi12239

GodinACCarlson JKampBurgenerV (2012)Theeffectofcirclehooks on shark catchability and at-vessel mortality rates in long-lines fisheriesBulletin of Marine Science88 469ndash483 httpsdoiorg105343bms20111054

GrimmDBarkhornIFestaDBonzonKBoomhowerJHovlandV amp Blau J (2012) Assessing catch sharesrsquo effects evidencefrom Federal United States and associated British Columbianfisheries Marine Policy 36 644ndash657 httpsdoiorg101016jmarpol201110014

HallMA(1996)OnbycatchesReviews in Fish Biology and Fisheries6319ndash352httpsdoiorg101007BF00122585

HallMAAlversonDLampMetuzalsKI(2000)By-catchProblemsand solutions Marine Pollution Bulletin 41 204ndash219 httpsdoiorg101016S0025-326X(00)00111-9

HallMANakanoHClarke S Thomas SMolloy J PeckhamSHhellipHallSJ (2007)Workingwithfisherstoreduceby-catchesIn S J Kenelly (Ed)By-catch reduction in the worldrsquos fisheries (pp235ndash288) Dordrecht The Netherlands Springer httpsdoiorg101007978-1-4020-6078-6_8

HallM amp RomanM (2013)Bycatch and non-tuna catch in the tropi-cal tuna purse seine fisheries of the worldFisheriesandAquacultureTechnicalPaper568RomeItalyFAO

HallMASwimmerYampPargaM(2012)NoldquosilverbulletsrdquobutplentyofoptionsWorkingwiththeeasternpacificartisanalfisherstore-duceseaturtlemortalityinfisheriesInJASeminoffampBWallace(Eds)Sea turtles of the eastern pacific Advances in research and con-servation(pp136ndash153)TucsonAZUniversityofArizonaPress

HamnerRMWadePOremusMStanleyMBrownPConstantineR amp Baker C S (2014) Critically low abundance and limits tohuman-relatedmortalityfortheMauirsquosdolphinEndangered Species Research2687ndash92httpsdoiorg103354esr00621

HatchSA(2003)Statisticalpowerfordetectingtrendswithapplica-tions to seabird monitoringBiological Conservation 111 317ndash329httpsdoiorg101016S0006-3207(02)00301-4

HeppellSSCrowderLBampCrouseDT(1996)Modelstoevaluateheadstartingasamanagementtoolforlong-livedturtlesEcological Applications6556ndash565httpsdoiorg1023072269391

HoughPampRobertsonM(2009)MitigationunderSection404oftheCleanWater ActWhere it comes from what it meansWetlands

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Ecology and Management 17 15ndash33 httpsdoiorg101007s11273-008-9093-7

IATTC(2015)Resolution on the conservation of mobulid rays caught in as-sociation with fisheries in the IATTC convention area Inter-AmericanTropical TunaCommission89thAnnualMeetingResolutionC-15-04LaJollaCAInter-AmericanTropicalTunaCommission

IFC(2012)Performance standard 6 Biodiversity conservation and sustain-able management of natural resources January 1 2012WashingtonDCInternationalFinanceCorporation

Innes J Pascoe S Wilcox C Jennings S amp Paredes S (2015)MitigatingundesirableimpactsinthemarineenvironmentAreviewofmarket-basedmanagementmeasuresFrontiers in Marine Science276httpsdoiorg103389fmars201500076

JanniseCSquiresDSeminoffJampDuttonP (2010)Conservationinvestments andmitigationTheCaliforniadrift gillnet fishery andpacificseaturtles InRQGraftonRHilbornDSquiresMTaitampMJWilliams(Eds)Handbook of marine fisheries conservation and management(pp231ndash240)OxfordUKOxfordUniversityPress

Jones E amp FrancisM (2012)Protected rays ndash Occurrence and devel-opment of mitigation methods in the New Zealand tuna purse seine fishery Auckland New Zealand National Institute of Water andAtmosphericResearch

KormosRKormosCFHumleTLanjouwARainerHVicturineR hellipWilliamson E A (2014) Great apes and biodiversity offsetprojectsinAfricaThecasefornationaloffsetstrategiesPLoS ONE9(11)e111671httpsdoiorg101371journalpone0111671

KotchenMJ (2013)Voluntaryand information-basedapproachestoenvironmentalmanagementApubliceconomicsperspectiveReview of Environmental Economics and Policy 7(2) 276ndash295 httpsdoiorg101093reepret012

Kyriazi Z LejanoRMaes FampDegraer S (2015)Bargaining a netgaincompensationagreementbetweenamarinerenewableenergydeveloperandamarineprotectedareamanagerMarine Policy6040ndash48httpsdoiorg101016jmarpol201506005

LentRampSquiresD(2017)ReducingmarinemammalbycatchinglobalfisheriesAneconomicsapproachDeep Sea Research Part II Topical Studies in Oceanography 140 268ndash277 httpsdoiorg101016jdsr2201703005

Lewison R L Crowder L B Read A J amp Freeman S A (2004)Understanding impactsof fisheriesbycatchonmarinemegafaunaTrends in Ecology amp Evolution19598ndash604httpsdoiorg101016jtree200409004

MannC (2015)StrategiesforsustainablepolicydesignConstructiveassessmentofbiodiversityoffsetsandbankingEcosystem Services16266ndash274httpsdoiorg101016jecoser201507001

Marine Stewardship Council (2014 June 21) MSC fisheries certifica-tion requirements v20 [pdf doc] httpswwwmscorgdocumentsscheme-documentsfisheries-certification-scheme-documentsfisheries-certification-requirements-version-20

MaronM IvesCDKujalaHBullJWMaseykFJBekessyShellip Possingham H P (2016) Taming a wicked problem Resolvingcontroversies inbiodiversityoffsettingBioScience66(6)489ndash498httpsdoiorg101093bioscibiw038

MaxwellSLMilner-GullandEJJonesJPKnightATBunnefeldNNunoAhellipRhodesJR(2015)BeingsmartaboutSMARTenvi-ronmentaltargetsScience3471075ndash1076httpsdoiorg101126scienceaaa1451

Moilanen A Van Teeffelen A J Ben-Haim Y amp Ferrier S (2009)Howmuch compensation is enoughA framework for incorporat-inguncertaintyandtimediscountingwhencalculatingoffsetratiosfor impactedhabitatRestoration Ecology17 470ndash478 httpsdoiorg101111j1526-100X200800382x

MorarNToadvineTampBohannanBJ(2015)Biodiversityattwenty-fiveyearsRevolutionorredherringEthics Policy amp Environment1816ndash29httpsdoiorg1010802155008520151018380

OrphanidesCDampPalkaDL(2013)Analysisofharborporpoisegill-netbycatchcomplianceandenforcement trends in theUSnorth-western Atlantic January 1999 to May 2010 Endangered Species Research20251ndash269httpsdoiorg103354esr00499

Pascoe S Innes J Holland D Finas M Theacutebaud O TownsendR hellip Hutton T (2010) Use of incentive-based managementsystems to limit bycatch and discarding International Review of Environmental and Resource Economics 4 123ndash161 httpsdoiorg10156110100000032

PhalanBHayesG Brooks SMarshDHoward PCostelloeBhellip Whitaker S (2017) Avoiding impacts on biodiversity throughstrengthening the first stage of the mitigation hierarchy Oryxhttpsdoiorg101017S0030605316001034

Queacutetier F Regnery B amp Levrel H (2014) No net loss of biodiver-sity or paper offsets A critical review of the French no net losspolicy Environmental Science amp Policy 38 120ndash131 httpsdoiorg101016jenvsci201311009

RadzioTASmolinskyJAampRoosenburgWM(2013)Lowuseofre-quiredterrapinbycatchreductiondevicesinarecreationalcrabpotfisheryHerpetological Conservation and Biology8222ndash227

RaineyHJPollardEHBDutsonGEkstromJMLivingstoneSRTempleHJampPilgrimJD(2015)AreviewofcorporategoalsofnonetlossandnetpositiveimpactonbiodiversityOryx49232ndash238httpsdoiorg101017S0030605313001476

Rausser G C Hamilton S F Kovach M amp Stifter R (2009)UnintendedconsequencesThe spillovereffectsof commonprop-ertyregulationsMarine Policy3324ndash39httpsdoiorg101016jmarpol200803020

Rice J (2014) Evolution of international commitments for fisheriessustainability ICES Journal of Marine Science Journal du Conseil71157ndash165httpsdoiorg101093icesjmsfst078

RichardYampAbrahamER(2013)ApplicationofPotentialBiologicalRemoval methods to seabird populations New Zealand AquaticEnvironmentandBiodiversityReport108

RodeJGoacutemez-BaggethunEampKrauseT(2015)Motivationcrowd-ingbyeconomic incentives inconservationpolicyAreviewoftheempiricalevidenceEcological Economics117270ndash282httpsdoiorg101016jecolecon201411019

RogersAA(2013)SocialwelfareandmarinereservesIswillingnesstopayforconservationdependentonmanagementprocessAdiscretechoiceexperimentoftheNingalooMarineParkinAustraliaCanadian Journal of Agricultural EconomicsRevue Canadienne Drsquoagroeconomie61217ndash238httpsdoiorg101111cjag12008

Rosenberg A A amp McLeod K L (2005) Implementing ecosystem-basedapproachestomanagementfortheconservationofecosystemservicesMarine Ecology Progress Series300 270ndash274 httpsdoiorg103354meps300270

Segerson K (2010) Can voluntary programs reduce sea turtle by-catch Insights from the literature in environmental economics InRQGraftonRHilbornDSquiresMTaitampMJWilliams(Eds)Handbook of marine fisheries conservation and management(pp618ndash629)OxfordUKOxfordUniversityPress

Serafy JECookeS JDiazGAGraves JEHallMShivjiMampSwimmerY(2012)CirclehooksincommercialrecreationalandartisanalfisheriesResearchstatusandneedsforimprovedconser-vation and management Bulletin of Marine Science 88 371ndash391httpsdoiorg105343bms20121038

ShiodeDHu F ShigaM Yokota K amp Tokai T (2005)Midwaterfloatsystemforstandardizinghookdepthsontunalonglinestore-duce sea turtleby-catchFisheries Science71 1182ndash1184httpsdoiorg101111j1444-2906200501080x

Sims M Cox T amp Lewison R (2008) Modeling spatial patternsin fisheries bycatch Improving bycatch maps to aid fisheriesmanagement Ecological Applications 18 649ndash661 httpsdoiorg10189007-06851

emspensp emsp | emsp15MILNER- GULLAND Et AL

Squires D amp Garcia SM (2014) Ecosystem-level impacts of fisheries bycatch on marine megafauna Biodiversity conservation through miti-gation policy economic instruments and technical changeReportofthe IUCN-CEM-FEGScientificworkshopGland Switzerland 7ndash10October2013GlandSwitzerlandIUCN

SquiresDampGarciaSM(inpress)Fisheries bycatch in marine ecosys-tems Policy economic instruments and technical change ChichesterUKJWileyampSons

SwimmerYArauzRMcCrackenMMcNaughtonLBallesteroJMusylMhellipBrillR(2006)DivingbehavioranddelayedmortalityofoliveridleyseaturtlesLepidochelys olivaceaaftertheirreleasefromlongline fishing gearMarine Ecology Progress Series323 253ndash261httpsdoiorg103354meps323253

TolottiMTFilmalterJDBachPTravassosPSeretBampDagornL(2015)BanningisnotenoughThecomplexitiesofoceanicsharkmanagementbytunaregional fisheriesmanagementorganizationsGlobal Ecology and Conservation 4 1ndash7 httpsdoiorg101016jgecco201505003

Tuck G N Polacheck T amp Bulman C M (2003) Spatio-temporaltrendsoflonglinefishingeffortintheSouthernOceanandimplica-tionsforseabirdbycatchBiological Conservation1141ndash27httpsdoiorg101016S0006-3207(02)00378-6

UNEP-WCMC(2016)Marine no net loss A feasibility assessment of imple-menting no net loss of biodiversity in the seaCambridgeUKUnitedNationsEnvironmentProgramme

Vaissiegravere A-C Levrel H Pioch S amp Carlier A (2014) Biodiversityoffsets for offshore wind farm projects The current situation inEurope Marine Policy 48 172ndash183 httpsdoiorg101016jmarpol201403023

Wallace B P Heppell S S Lewison R L Kelez S amp CrowderL B (2008) Impacts of fisheries bycatch on loggerhead tur-tles worldwide inferred from reproductive value analy-ses Journal of Applied Ecology 45 1076ndash1085 httpsdoiorg101111j1365-2664200801507x

Wanless R M Ryan P G Altwegg R Angel A Cooper JCuthbert R amp Hilton G M (2009) From both sides Dire de-mographic consequences of carnivorous mice and longlining for

the critically endangered Tristan albatrosses on Gough IslandBiological Conservation 142 1710ndash1718 httpsdoiorg101016jbiocon200903008

WardP LawrenceEDarbyshireRampHindmarshS (2008) Large-scale experiment shows that nylon leaders reduce shark bycatchandbenefitpelagiclonglinefishersFisheries Research90100ndash108httpsdoiorg101016jfishres200709034

WardTampPhillipsB(2010)SeafoodecolabelingInRQGraftonRHilbornDSquiresMTaitampMJWilliams(Eds)Handbook of ma-rine fisheries conservation and management (pp 608ndash617) OxfordUKOxfordUniversityPress

WilcoxCampDonlanCJ (2007)Compensatorymitigationasasolu-tion to fisheries bycatch-biodiversity conservation conflictsFrontiers in Ecology and the Environment 5 325ndash331 httpsdoiorg1018901540-9295(2007)5[325cmaast]20co2

WilcoxCampDonlanCJ (2009)NeedforaclearandfairevaluationofbiodiversityoffsetsforfisheriesbycatchConservation Biology23770ndash772httpsdoiorg101111j1523-1739200901173x

Wolf SHartlBCarrollCNeelMCampGreenwaldDN (2015)Beyond PVAWhy recovery under the Endangered Species Act ismorethanpopulationviabilityBioScience65200ndash207httpsdoiorg101093bioscibiu218

ZedlerJBampCallawayJC (1999)TrackingwetlandrestorationDomitigation sites follow desired trajectories Restoration Ecology 769ndash73httpsdoiorg101046j1526-100X199907108x

Žydelis R Wallace B P Gilman E L amp Werner T B (2009)Conservation of marine megafauna through minimization of fish-eries bycatch Conservation Biology 23 608ndash616 httpsdoiorg101111j1523-1739200901172x

How to cite this articleMilner-GullandEJGarciaSArlidgeW etalTranslatingtheterrestrialmitigationhierarchytomarinemegafaunaby-catchFish Fish 2018001ndash15 httpsdoiorg101111faf12273

Page 2: Translating the terrestrial mitigation hierarchy to marine ......of marine megafauna by-catch in fisheries, going from defining an overarching goal with an associated quantitative

2emsp |emsp emspensp MILNER- GULLAND Et AL

1emsp |emspINTRODUC TION

Thegoal of nonet loss (NNL)of biodiversity fromeconomicde-velopment is becomingwidely adopted by national governmentsand international lenders potentially offering a method to limitthe impacts of environmental damage in terrestrial and coastalsystems(BBOP2012IFC2012)Severallargemultinationalcom-panieshavesigneduptoNNLoreventoproducinganetgainofbiodiversity as a result of their activities (BullampBrownlie 2017Raineyetal2015)GenerallyNNLisassuredbytheuseofamit-igation hierarchy often applied as part of an Environmental andSocialImpactAssessment(ESIA)Themitigationhierarchyrequiresthatprojectproponentsfirstavoiddoingharmtobiodiversityforexample by sitting the development away from particularly sen-sitive areas Subsequentlywhile carryingout their developmenttheyshouldminimize theharmdone forexampleby limiting thefootprint of heavymachinery to specific areas and not pollutingwatercoursesTheythenremediatethebiodiversitylosswithinthedevelopment footprint for example by replanting cleared areaspost-developmentThefinalstepistooffsetanyresidualadditionaldamage caused by their development through improvement ofbiodiversityelsewhere(Gardneretal2013)usingarangeofap-proachesforexamplediggingnewpondsorclearinginvasiveveg-etationinanadjacentsite(BullHardyMoilanenampGordon2015)Offsetting isaparticularlycontroversialelementofthehierarchybecauseitrequiresacceptanceofadevelopmentthatharmsbiodi-versity inagivenlocationandassumesthat it ispossibletocom-pensateforthisharmbybiodiversityenhancementelsewhere(egMaron etal 2016)More generally there ismuch debate aboutwhetherNNL isattainableandhow it shouldbe implemented inpractice(mostrecentlyexploredbyBullLloydampStrange2017)

Despiteitsgrowinguseinterrestrialandcoastalenvironmentsthemitigationhierarchyhasnotbeensowidelyapplied innear-shoreandhighseasmarinesettingsandmanyquestionsaboutitsapplicationintheoceanremain(SquiresampGarciainpressUNEP-WCMC2016)Marine experience to date hasmostly concernedcoastaldevelopmentforexamplerelatingtowindfarmsurbande-velopmentaquacultureandportsratherthaninthecapturefish-eriesarena(egKyriaziLejanoMaesampDegraer2015VaissiegravereLevrel Pioch amp Carlier 2014) The four steps of themitigationhierarchyarediscussedinfisherieshoweverandasintheterres-trialliteraturetheoptionofoffsettingisparticularlycontroversial(egthedebatearoundWilcoxampDonlan2007analysisofthepo-tentialforoffsettingseabirdby-catchbyinvasivespecieseradica-tiononnestingislandsFinkelsteinetal2008WilcoxampDonlan2009ŽydelisWallaceGilmanampWerner2009)Theuseofeco-nomicincentivestoreducetheamountorimpactofby-catchhasreceivedattentionbuthasalsonotyetbeenfullyexplored(DuttonampSquires2008GjertsenSquiresDuttonampEguchi2014InnesPascoe Wilcox Jennings amp Paredes 2015) The current FAOInternationalGuidelinesonBycatchManagementandReductionofDiscardsmentioneconomicincentivesonlybriefly(astheonlyeconomic instrument) and refer only to incentives to promote

innovationingeartechnology(FAO2011)Manyquestionsremainas towhether it is possible to apply themitigation hierarchy tomarineby-catchandwhatmeasurescouldbeusedtoincentivizeactionateachstageinthehierarchyInparticularthereisaneedforaconceptualframeworkthatintegratestherangeofby-catchmitigationmeasuresandtheapproachesusedtoincentivizetheminanholisticway

This article explores application of themitigation hierarchy toaddress a specific fishery concern that ofmarinemegafauna by-catchWetakeldquomarinemegafaunardquotoencompasslong-livedspecieswithlowreproductiverateswhicharethereforepotentiallysensitivetoby-catchforexamplemarinemammalsturtlesseabirdsandlargefishwhilewedefineby-catchascatchwhichisnotdirectlytargeted(bearing inmind thecomplexities indefinitionhighlightedbyFAO2011)We limit our discussion tomarinemegafauna by-catch formanageabilityofscopeandbecausethisissueisofparticularcon-cernwithin both the conservation and fisheries realmsHowevermanyofthepointsweraiseareapplicabletoby-catchmorebroadlyIt isalsotheissueforwhichdiscussionoftheapplicabilityofNNLandthemitigationhierarchytomarinesystemshasbeenparticularlyactive(egfollowingthepaperbyWilcoxampDonlan2007)

First we outline a conceptual framework for by-catchmitiga-tionbasedon theapplicationofa sequentialmitigationhierarchytoachieveNNLWethendiscusssomekeyissuesthatariseintheapplicationofamitigationhierarchytomarinemegafaunaby-catchandrelatethemtotheequivalentdebate intheterrestrialsettingWemoveontoconsiderhowincentivestomitigatetheamountorimpact of by-catch can be used to support the application of theframeworkFinallywesumup thepotentialofour framework forimprovingby-catchmitigationoutcomes

2emsp |emspCONCEPTUAL FR AME WORK FOR BY- C ATCH REDUC TION

ToclarifyhowachievingNNLthroughamitigationhierarchywouldwork for marine megafauna by-catch we present a conceptualframeworkrelatingtothetargetlevelofby-catchimpactinafisheryTheapproachcanoperateatarangeoflevelsfromtheglobaltothestock to the individualanimalThemostusual andmost intuitivescaleatwhichNNLcouldapplytoby-catchisatthescaleofafish-erytargetingagivenstockorsetofstockssothisisthescaleweuseinthisexplorationTable1explainsthetermsweusetodescribetheconceptualframework

The approach starts by defining the goal in terms of a desiredchangeinbiodiversitythisiscommonlytakentobeNNLofbiodiver-sitybutthatisnotnecessarilytheonlygoalForexampleintheter-restrialrealmnetgainisawidelyusedgoal(Raineyetal2015)whilein themarine realmby-catchminimization isoften thepolicygoal(exceptfortotallyprotectedspecies)whichmayimplyanetlossorgaininbiodiversitydependingonthecurrentby-catchlevelAnotherpotentialgoalcouldbepopulationrecovery (cf theUSEndangeredSpeciesActWolfHartlCarrollNeelampGreenwald2015)

emspensp emsp | emsp3MILNER- GULLAND Et AL

ThenextstepistodefineaquantitativetargetandassociatedmetricbywhichthegoalwillbemeasuredInthecaseofby-catchofmarinemegafauna one relatively intuitive approach is to de-fine the target as zero net change in population growth rate ofthe focal species caused as a result of by-catch and associatedmitigationmeasures inthecontextofalltheotherfactors influ-encingthatpopulation(aswasdoneeginthestudiesreviewedbyLewisonCrowderReadampFreeman2004)Thedownsideofthis metric is its requirement for monitoring data that can pro-vide trends in population size over time decomposed into vitalrates(survivalfecundity)sothatthecontributionofby-catchandmitigationmeasures tochange inpopulationgrowth ratecanbediscerned Thismay be challenging formanymarinemegafauna(CaswellBraultReadampSmith1998)Othermore readilymon-itored targets couldbebasedonnumbersof animals for exam-plenotexceedingaPotentialBiologicalRemoval(PBR)threshold(RichardampAbraham2013)Thedownsideofnumbers-basedmet-ricsistheirmoreindirectrelationshipwiththeconservationstatusofthespeciesconcerned

Using themetric of net change in population growth rate thebaselinefromwhichgainsandlossesfromdifferentmeasurestakentomitigateby-catchareassessedcouldbeazeropopulationgrowthratesuchthatthepopulationremainsstableatthecurrentlevel(astatic baseline) the projected population growth rate of the spe-ciesintheabsenceofby-catchwhichcouldbepositiveornegativedependingontherelativeimportanceofby-catchinthecontextofotherthreats(adynamicbaseline)oranaspirationalbaselinesuchaspopulationgrowthatXperyeartothepointatwhichitreachessomedesiredsteady-stateabundance(whichwouldneedtobedy-namicgiventhatpopulationshavedensity-dependentgrowth)Suchabaseline is therefore a typeofcounterfactual againstwhichanyimprovement or deterioration in the population of the by-caughtspeciesasaresultoftheimplementationofthemitigationhierarchy

iscompared(iewhatwouldhavehappenedintheabsenceoftheby-catchmitigationmeasures)

Next the different approaches which can be used to attainNNL(orwhatevergoal isset)areassessed intermsoftheireffectonthechosenmetricforexamplethereductioninseabirdmortal-ityfromfittingtorilinesinafisherycanbeassessedintermsofitseffectonthegrowthrateofawanderingalbatross(Diomedea exu-lansDiomedeidae)populationThefourcategoriesoftheterrestrialmitigationhierarchyareavoidanceminimizationremediation(alsoknown as restoration or rebuilding) and offsetting In the case ofmarinemegafaunaby-catchwetakeldquoavoidancerdquotorepresentmea-surestakeninordertoreducetheprobabilityofencounterbetweenpotentially harmful gear and a potentially by-caught individualby separating fishing activity from individuals or stocks of poten-tialmegafaunaby-catch species (seeTable2 for example actions)We take ldquominimizationrdquo asmeasureswhich reduce theprobabilityofcapturebythegeargiventhattheencountercannotberealisti-callyldquoavoidedrdquoThesemeasuresoccuroncethereisspatio-temporaloverlapbetweena fishingvesselandamarinemegafauna individ-ualldquoRemediationrdquoalsooccursatseabutpost-captureandaimstoreduce theprobabilityofmortality givencapture ldquoOffsettingrdquo re-ferstomeasurestocompensateforby-catchmortalitythatoperateseparatelyfromthefocalfishingactivitybutwhichtargetthesamestockoftheby-caughtspecies

Inrealitytherearegreyareasbetweeneachofthesestagesandarangeofwaysinwhichby-catchmitigationmeasurescanbecat-egorizedForexample herewe include restorationand rebuildingactivitiesat thestock level inldquooffsettingrdquobecauseourframeworkis structuredaround individual-levelcaptureprobabilityHoweveranotherapproachmightbetocombineremediationatthe individ-uallevelinacategorywithrestorationrebuildingmeasuresthatim-provepopulationviabilityatthestocklevelsuchasrestockingandhabitatimprovementleavingoffsettingasmeasureswhichbenefit

Term Explanation

Goal Thedesiredchangeinbiodiversityforexamplenonetloss(NNL)ofbiodiversityasaresultofthecombinedeffectofthedamagingaction(egby-catch)andassociatedmitigationmeasures

Target Inourframeworkwedistinguishbetweentheoverallgoalatthepolicylevel(egNNL)andthequantitativetargetwhichoperationalizesthegoalforwhichametriccanbedefined

Metric TheunitsusedtomeasuregainsandlossesinbiodiversityinordertoevaluatewhetherthegoalhasbeenachievedInourcasethisisnetchangeinpopulationgrowthrateofthefocalspeciesasaresultofby-catch+mitigationmeasures

Baseline ThereferencepointagainstwhichNNLisassessedThiscouldbestatic(egcurrentpopulationgrowthrate)dynamic(projectedpopulationgrowthrateintheabsenceofby-catchbutcontinuationofotherprocessesaffectingvitalrates)oraspirational(desiredchangeinpopulationgrowthrate)

Counterfactual Theprojectedchangeinpopulationgrowthrateinthepresenceofby-catchbutabsenceofmitigationmeasuresagainstwhichNNLisassessed(egbusinessasusual)IfthebaselineisdynamicthecounterfactualisthesameasthebaselineotherwisebotharerequiredtofullydefinethescenarioagainstwhichNNLisevaluated

TABLE 1emspExplanationoftermsusedinthemitigationhierarchy

4emsp |emsp emspensp MILNER- GULLAND Et AL

thestockmoreindirectlyoractatthebroaderspecieslevel(suchasrestoration in other locations ormeasures to improve complianceand reduce uncertainty) Howeverwe feel that the clarity of theprobabilisticapproachinourframeworkwhichextendstheclassi-ficationbyHall(1996)isparticularlyhelpful

Ourdivisionofmitigationapproachesintothesecategoriescanberepresentedinthefollowingconceptualmodelrelatingtoapar-ticularby-catchspeciesinwhichtheunitisrateofchangeinpopu-lationsizeasaresultofby-catchanditsmitigation

HereΔλT is the target levelofoverallnetdamage inflictedbyby-catchonthespeciesconcernedmeasuredintermsofchangeinpopulationgrowthratewithrespecttotheagreedbaselineAzeroΔλTimpliesthatthereductioninpopulationgrowthratecausedbyby-catch after avoidance andmitigationmeasures have been im-plementedisbalancedbythegainengenderedbyoffsetmeasuresThereisalsothepossibilityforΔλTtobenegative(thereisstilladdi-tionalpopulationdeclineasaresultofby-catchevenaftermeasurestoreduceit)orpositive(equivalenttonet gainmeaningthatspeciespopulationgrowthishigherthanitwouldotherwisehavebeenasaresultofthecombinationofmeasurestakenunderthemitigationhierarchy)

f(EBtimesBPUE)istheeffectonpopulationgrowthrateoftheby-catch-relevantcomponentoffishingeffortbrokendownintotheby-catch-relevanteffortitselfEBandtheby-catchtakenperunitof that effort BPUEwhere f() is the effect of this effort on theby-caught speciesrsquo population dynamics Thiswould generally becalculatedastheoutputofapopulationmodelAreduction inEB isequivalenttoafisheryavoidingby-catchpartiallyorcompletelyIt could include restricting the fishery to particular areas or sea-sons modification of fishing practices and operations (eg set-tingthegeardeepertoavoiddepthswhereby-caughtspeciesare

prevalent)AreductioninBPUEistheresultoftheat-seameasuresencompassed intheldquominimizerdquoandldquoremediaterdquostepsofthemiti-gationhierarchy

By-catch-relevanteffortEBisasubsetoftheoverallfishingef-fort thatoccurs in thearea inwhichthere is riskofby-catch (E)Given thecomplexitiesof estimatingEB inmanycases itwill benecessarytoapproximateitbyE(egTuckPolacheckampBulman2003) Thismay be problematic for example Baacuteez etal (2007)show that loggerhead turtle (Caretta caretta Cheloniidae) by-catchintheMediterraneanwasnotcorrelatedwithfishingeffort(measuredasnumberofhooks)by-catchwasinsteadstronglyre-lated todistance from thecoastThey suggest that thiswasnotbecauseturtleabundance isa functionofdistance (whichwouldhave impliedagradient inEB) butbecause fisherbehaviourvar-iedalthoughtheyleftinvestigationofthemechanismsforfurtherresearchBPUEisafunctionofcatchabilityoftheby-caughtspe-ciesaswellasEB forexampleWardLawrenceDarbyshireandHindmarsh(2008)carriedoutamultispeciesanalysisoftheeffectsof nylon leaders on catch rates and showed that catch reducedwithnylonforsharksbluemarlin(Makaira nigricansIstiophoridae)and snake mackerel (Gempylus serpens Gempylidae) and in-creased for bigeye tuna (Thunnus obesus Scombridae) and blackmarlin(Istiompax indicaIstiophoridae)TherelationshipsbetweenEEB andBPUEare likely tobe complex and confoundedTherehavebeen limitedexplorationsof these relationships inby-catchdatasetswhich typically suffer from low sample sizes and zero-inflationrequiringspecializedmodellingtechniques (eg thespa-tiallyexplicitBayesianhierarchicalmodelsofSimsCoxampLewison2008)By-catchmitigationmayuseasuiteofinteractingmeasuresfrom several levels of the mitigation hierarchy (Table2) whichchangeovertimeaddingfurthertothecomplexityofseparatingE EBandBPUE(asdiscussedfortargetfisherydatabyBishop2006)Wedonothereattemptfurthertoclarifytheserelationshipsbutakeyresearchneedistodisentanglethesevariablesinanempiricalsetting

(1)ΔλT= f(

EBtimesBPUE)

minusOT

Step of the hierarchy Example measures

Avoidance Excludingfishingfromtheareas(no-fishingzones)seasons(closedseasons)ortimesofdaywherethesespeciesaremostvulnerable

Minimization Usingon-vesseltechnologieswhichaimtoreducethenumberofencounteredindividualsthatarecapturedduringfishingoperationssuchastorilinesforscaringseabirdsawayfromlonglinesorsonicdevicestosignalnetstomarinemammals

Remediation Deviceswhichenableindividualstoreleasethemselvesfromthegear(selectivitygridsturtleexcluderdevices)ortobereleased(egMedinapanelsoperatedintunapurse-seinefisheriestoletdolphinsescapebeforegettingonthedeck)orreleasingthemondeckandprovidingforasafereturntothesea(egalargemeshsoftwebbingcargonetcanbeusedtoldquosieverdquoarayfromthecatchandliftitoverthesideofthevesselFrancis2014)

Offsetting Eradicatinginvasivepredatorsonislandswhereseabirdsnestrestoringhabitatrestockingwithhatchery-raisedindividualsimprovingby-catchperformanceofothergeartypesinthearea

TABLE 2emspExamplesofmeasureswhichcanbetakenundereachstepofthemitigationhierarchy

emspensp emsp | emsp5MILNER- GULLAND Et AL

OT is the net effect on population growth rate of policiesaimingtoimprovetheoverallviabilityoftheby-caughtspeciesrsquopopulation representing ldquooffsettingrdquo of the damage caused Itrepresents the expected effects of measures to improve con-ditions for individuals which would not have been at risk ofby-catch at that particular stage in their lives or location Forexample supplementation in nesting areas (for turtles) resto-rationofnestinghabitat(forseabirds)orimplementationofpro-tectedareasaimedatdemographicgroupsnotdirectlyimpactedby fishing (calving areas for cetaceans juvenile concentrationsforfish)

3emsp |emspOPER ATIONALIZING THE FR AMEWORK

In Table3we illustrate the application of the by-catchmitigationframework using four examples from different fisheries and by-catchtaxaSpecificsolutionstoEquation1couldcomefromtakingintoaccount the regulatory cultural andeconomicconditions inaparticularfisheryForinstanceoncethefocalby-catchpopulationhasbeendefinedthenitispossibletosolvetheequationbyassign-ingfactorsaffectingdecision-makingincludingcostIfaleast-costapproachtoby-catchgoalsisappropriateEBBPUEandOT could be expressedasfunctionsofcosttosolvetheequationforagivenΔλT Another approachwould be tomaximizeΔλT subject to a budgetconstraint

Table3highlightsthatthereisnotalwayspotentialforeffec-tive action at each level of the hierarchy for some species (egoceanicwhitetipslonglines)theremaybelimitedpotentialatalllevelsTheframeworkisawayoforganizingandstructuringthink-ingaboutby-catchmitigationandenablingmitigationeffective-nesstobeassessedagainstaconcretelydefinedandmeasurabletargetItsfunctionisnottoproposenewwaysofdoingby-catchmitigationforcasesliketheseIfonusingtheframeworktoanal-yse the effectiveness of the measures available for a given by-caughtstockitisfoundthatitisnotpossibletoreachthechosentarget(egNNL)thendifficultdecisionsmustbemadeForexam-plethetargetmayneedtochangewhichcouldimplyanaccep-tanceofcontinuingdeclineoftheby-caughtstockOrthefisherymustbe restructured in away that reducesby-catcheffectively(maybeevencloseddown)Orinvestmentmustbemadeintotech-nological innovation todevelopnewways to reduceby-catch Ifitisfoundthatthedataareinadequatefortheanalysisrequiredthenthedecisionmustbemadeeithertoinvestinimprovingtheevidencebaseor to recognize that it is not possible to evaluatewhether by-catch mitigation has been effective in reaching theagreed goal The frameworkrsquosmain utility therefore is tomakethesechoicesexplicit

Equation1couldbeextendedtohandlemultiplespeciesvary-inggeartypesorheterogeneousby-catchreductionmethodsForinstanceBPUEcanbedecomposedintoseveralcomponentsrepre-sentingthedifferentstagesoftheprocessIfBPUErepresentsthesumofindividualsdeadonarrivalindividualscapturedanddyingon

thevessel and individualsdyingafter live releasewecan rewriteBPUEasaseriesoffactors

whereBDOAistheby-catchperuniteffortthatarrivestotheboatdeadBOBistheby-catchperuniteffortthatarrivestothevesselalivePDVistheproportiondyingonthevesselandPDRisthepro-portiondying after release For instance a higherproportionofby-catchofseaturtlesandotherspeciesarrivestotheboatdeadwhenusinglonglinesthataresetdeepsuchasthoseusedforbig-eyetunathatcanbesetmorethan300mdeepwhencomparedto a shallow set longline such as those used inmany nearshoreartisanal fisheries (Andrakaetal2013HallSwimmerampParga2012Swimmeretal2006)ThisdifferencewouldappearintheBDOA termSuchadecomposition illustratestheflexibilityofthisframeworkinhandlingfishery-andspecies-specificfeaturesandalsoservestohighlightareaswheredifferentmitigationmethodswouldhavethegreatestinfluence(egShiodeHuShigaYokotaampTokai2005)Anotherextensiontothebasicframeworkwouldbetoconsiderexplicitlytheuncertaintysurroundingdifferentel-ements of the conceptual model and the impact of this uncer-taintyonwhichelementofby-catchmitigationshouldbeafocus(Table3)

It is important tonote that this equation isnot a truebioeco-nomicequationtobesolvedRatheritisaconceptualframeworkinwhichwemakethecomponentsofthemitigationhierarchyexplicitinordertoguidethinkingtowardsamoreholisticapproachtoad-dressingby-catchItalsodoesnotrepresentahierarchysuchasisrequiredinterrestrialsystemsTomakethisequationintoahierar-chyratherthanamodelforleast-costmitigationofby-catchitcouldbesetupasagoalprogrammingfunctionwithsequentialsolutionstoeachelementsummedtoproducethefinalmitigationoutcomeInoperationaltermsthistranslatesintoapresumptionthatinvestmentandeffortshouldbefocusseddifferentiallyonsequentialelementsofthemodelstartingwithEBthenBPUEthenOTsothatoffsettingrelatesonly to theunavoidable residualharmonceall other stepshavebeentakenThismaybereflected intheemphasisplacedontheincentivesgiventofisherstochangebehaviourpertainingtose-quentialelementsofthehierarchyinthetimingoftheoffsetorinthedispositionofthefundingforresearchandconservationactionallocatedbygovernment

ResearchiscurrentlyongoingtooperationalizeEquation1tore-duceturtleby-catchofasmall-scalegillnetfisheryoperatingoutofSanJoseportPeru(Alfaro-Shiguetoetal2010)Currentlyasmall-scalecertificationschemeisundertrialbytheNGOProDelphinuswhich aims to give premium prices for fish caught by skippersabiding by best-practice by-catch reduction guidelines (J Alfaro-Shigueto and J Mangel personal communication) The researchentailscollectingdetailedeconomicdatafromallgillnetvesselstounderstand the economic costs involved in fishing operations tocalculatethepotentialadditionalcostsofmeasuresateachstagein

(2)BPUE=BDOA+PDVtimesBOB+(

1minusPDV)

timesBOBtimesPDR

6emsp |emsp emspensp MILNER- GULLAND Et AL

TABLE 3emspSummaryofoptionsforby-catchmitigationstructuredaccordingtothemitigationhierarchyforfourcase-studies

Fram

ewor

k st

ep

Cas

e- st

udy

Alb

atro

sses

lon

glin

esTu

rtle

slo

nglin

esRa

ysp

urse

sei

nes

Oce

anic

whi

tetip

slo

nglin

es

Definingtheproblem

Fisheryandspatial

extent

Braziliandomesticindustrialcoastallongline

fleet

EasternPacific(coastalandpelagic)

small-scalecommerciallonglinefishery

Tunapurse-seinefisheryof

theeasternPacific

AsianandEUlonglinetunafisheriesinthe

Indi

an o

cean

Targetspecies

Variousspeciesofsharkandswordfish

Mahi-mahi(

Cory

phae

na h

ippu

rus

Coryphaenidaeseasonal)tunasharks

(mostlysilkyC

arch

arhi

nus f

alci

form

is

Carcharinidae)billfish

Variousspeciesoftuna

Variousspeciesoftuna

By-catchspeciesof

conc

ern

Albatrossamppetrelspeciesparticularconcern

forcriticallyendangeredTristanalbatross

(Dio

med

ea d

aben

nenaDiomedeidae)

Oliveridley(L

epid

oche

lys o

livac

ea

Cheloniidae)greenblack(C

helo

nia

myd

asCheloniidae)hawksbill

(Ere

tmoc

hely

s im

bric

ataCheloniidae)

loggerhead(PeruandMexico)and

leatherback(D

erm

oche

lys c

oria

cea

Cheloniidae)

Sevenmobulidspecies

includingCITES-listedM

anta

bi

rost

ris(Mobulidae)and

M a

lfred

i(Mobulidae)

caughtmostlyalivein

dolphin-associatedor

free-schoolsets

OceanicwhitetipsharkVulnerableonIUCN

redlistretentionbannedbytunaRFMOs

listedonCITESAppendixII

By-catchtarget

(Δλ T)

BraziliangovernmentMinimizeby-catch

Rulesfocusontargetsforuseofminimizing

measuresratherthanonby-catchnumbers

NotwelldefinedRFMOssuggest

minimizingby-catchCouldconsiderPBR

foroliveridleyszerocatchforleather-

backs(reflectingtheirrespective

populationstatus)

IATTC(2015)zeroretention

storingorsellingandlive

releaseofby-caughtrays

whenpossibleImplies

by-catchminimization

Targetby-catchlevelnotdefineddueto

uncertaintyRFMOsbanretentionlanding

andtrans-shipment

Mitigationhierarchyelement

Avoid

[timeareaclosuresnight-timesetting]

[timeareaclosuresdeeperlines]

[timeareaclosures]

[deepsetting]

Minimize

[torilineslineweights]

[monofilamentlinecirclehooks(not

leatherbacks)]

ndash [hardtoavoidcatching]

[monofilamentlinecirclehooksbanon

steelleaders]

Remediate

ndash [hardtoreleasealive]

[improvedhandling]

[improvedhandling]

[shortsets]

Offset

[invasiveeradication]

[beachprotection]

[illegaltrade]

[informationgatheringillegaltrade]

Factorsaffectingoperationalization

Scopefor

incentives

Participatoryresearchonbarrierstouptakeof

minimizationmeasuresPositiveincentives

forthoseusingnewmeasurespaidforby

forexamplefisheries-widelevy

Certificationsustainabilitystandardsin

exportmarkets

Transitionalpaymentsto

promotebetterhandlingon

deckhenceimproving

survival

Ifinformationgatheringseenasavalidoffset

duetohighuncertaintyfundingatagging

schemecouldincentivizefisherstocollect

dataonsharkcatchratesurvivalof

releasedsharksby-catchhotspotsto

supportimprovementsacrossthewhole

mitigationframework

(Continues)

emspensp emsp | emsp7MILNER- GULLAND Et AL

themitigationhierarchy In theabsenceofhighqualitypopulationdatawithwhichtoparameterizeamodelaPBR-basedapproachisbeingusedtosetatargetby-catchlevel intermsofnumberof in-dividualsofeachoftheturtlespeciescaughtinthefisheryExpertopinionfromfishersandProdelphinusstaffsupplementedbydatafromalong-runningby-catchobserverprogrammeoperatingoutoftheport(Alfaro-Shiguetoetal2011)givesthepotentialreductioninturtleby-catchnumbersasaresultofagivenmitigationapproachInterviews and focus groups with fishers provide understandingof their preferences for different by-catchmitigation approachesbarriers and constraints to implementation and potential partici-pationindifferentincentiveschemesthiscanbesupplementedbyDiscreteChoiceExperimentsprovidingempiricalestimatesforpref-erencesforcombinationsofby-catchreductionmeasures(cfRogers2013)Thisfieldresearchproducesashort-listoffeasiblemitigationmeasuresateachstageinthemitigationhierarchyforcostingandtesting(egspecificareasortimesforfisheryclosureunderavoid-ancecombinationsofhooktypesandnetmodificationundermini-mizationtraininginturtlehandlingandreleaseforremediationandimprovingby-catchperformanceofothergeartypesintheareaforoffsetting)Thisenablestheanalysisoftheeffectivenessandcostof various combinations of by-catch reduction strategies framedwithinthefourstepsofthemitigationhierarchy(avoidminimizere-mediateoffset)withacleartargetby-catchreductiongoalinmind

4emsp |emspCOMPARING KE Y DEBATES BET WEEN TERRESTRIAL NNL AND BY- C ATCH MITIGATION

41emsp|emspThe hierarchical nature of mitigation

Terrestrial situationsareusuallyviewedas requiringastricthierar-chywithavoidanceminimizationandremediationtakingprecedenceoveroffsetsPartofthereasonforthishierarchymaybesocietalval-uesandexpectationsbut also it is a reflectionof reversibility anduncertaintyTheterrestrialmitigationhierarchywassetuptoaddresshabitatdestructioncausedbydevelopmentwhich iseffectively ir-reversiblehenceavoidanceisstrictlypreferredfromaconservationperspective Inpractice avoidancehasbeenaneglected step andmuchofthedisquietaboutbiodiversityoffsettinghasbeenbecauseofthetendencytopaylipservicetoavoidanceandfocusinsteadonoffsetswhich thenmay be implemented on paper only (HoughampRobertson2009Phalanetal2017)EvenwithperfectenforcementandcompliancewithmeasuresfurtherdownthemitigationhierarchythestrictavoidanceofhabitatlossismorecertaintolimitimpactthanreducinglossesinthecourseofapotentiallydamagingactionwhichismorecertainthanrestoringdamageafterthefactorcompensatingforitwithactionselsewhereOfteninterrestrialsystemsmultipliersareusedattheoffsetstagetoreflectthisuncertaintyrequiringthatanadditionalamountofequivalentlandisprotectedinanoffsetoverandabovetheamountthatislostduringthedevelopment(withtheratiooflandoffsettolanddestroyedinthe10sto100sdependingonthecircumstancesMoilanenVanTeeffelenBen-HaimampFerrierFr

amew

ork

step

Cas

e- st

udy

Alb

atro

sses

lon

glin

esTu

rtle

slo

nglin

esRa

ysp

urse

sei

nes

Oce

anic

whi

tetip

slo

nglin

es

Major

uncertainties

Lackofspecies-levelidentificationof

by-catchlackofunderstandingof

compliance

Lackofecologicalknowledgeofturtle

populationtrendsampdistribution

Potentialforsignificantadditional

by-catchfromcoastalgillnetfishery

Impactofcatchonmobulid

survivalPredictorsof

mobuliddistributions

Lackofobserversorreportingsoverylimited

understandingofby-catchlevelsspatio-

temporalencounterhotspotspost-release

survivalcompliance

Keyobstacle

Compliancewithexistingrulesmustbe

improved

Fundingforalternativestofishingata

largeenoughscaleLongtimelagand

uncertaintyinoffseteffectiveness

Limitedknowledgeofmobulid

distributionsmakes

avoidancedifficult

Lackofmonitoringlimitsoptions

Overallassessment

Existingmeasuresforimprovingimplementa-

tionofminimizationstepalreadyexistbut

needincentivizingoffsettingcouldprovide

short-termgainstocomplementthese

Targetedfundingcouldfacilitateimprove-

mentsthroughoutthehierarchyBest

approachmaydifferbyspecies(particu-

larlyleatherbacksvsothers)

Focusonremediationstepis

currentlythemainoption

avai

labl

e

Somepotentialforminimizationthrough

deepsettingbutchallengingtochange

behaviourinthisfisheryelectronic

monitoringsystemswouldhelp

Keyreferences

BugoniManciniMonteiroNascimentoamp

Neves(2008)Wanlessetal(2009)

Alfaro-ShiguetoDuttonampMangel(2007)

Halletal(2012)Andrakaetal(2013)

JonesampFrancis(2012)Hallamp

Roman(2013)Crolletal

(2016)Fowler(2016)

Tolottietal(2015)

Ticksindicatethepotentialforactionatdifferentstepsofthehierarchybasedonfeasibilitycurrentknowledgeandimpactonmortality(

=highpotential

=somepotential

=limitedpotential

ndash=nopotential)TextinbracketsgivessuggestedmeasuresateachlevelofthehierarchytheseareillustrativeratherthandefinitiveTheinformationforthecase-studiesisbasedontheexpertknowledge

oftheauthorsthroughtheirinvolvementinmanagementoftheby-catchissueinthesefisheriesRFMOregionalfisheriesmanagementorganizationPBRpotentialbiologicalremoval

TABLE 3emsp(Continued)

8emsp |emsp emspensp MILNER- GULLAND Et AL

2009)Bycontrastinfisheriessettingstherehavebeensuggestionsthatdependingonthelegalenvironmentitmaybemoreappropriateforoffsetstobeusedaspartofaleast-costconservationapproachalongsidemoretraditionalmitigationmethodsratherthanasthelaststep inamitigationhierarchy (DuttonJosephSquiresampWilliams2011DuttonampSquires2008WilcoxampDonlan2007)

42emsp|emspOut- of- kind offsets

Out-of-kind offsets are those which do not act to increase theimpact-affectedbiodiversityIntermsofourconceptualframeworktheyareoffsetswhichdonotacttoincreasethepopulationgrowthrateoftheby-catch-affectedfocalpopulation(Equation1)Forex-ampleonesuggestedbenefitof raising funds foroffsetting fromaby-catchtaxonfishersisthattheproceedsfromsuchataxcanfinanceoffsetselsewherewithintherangeoftheby-catch-affectedpopulation (Dutton amp Squires 2008) Although not a true offsetunderamitigationhierarchyfundsfromtheCaliforniadriftgillnetindustry in 2002 financed sea turtle nesting site conservation inBajaCaliforniaforcompensatorymitigationofseaturtleby-catch(Jannise Squires Seminoff amp Dutton 2010) In terrestrial (andmarine)systems itcanbemorechallengingtodefinethe impact-affected biodiversity because impact is rarely as clearly linkedtoagivenspeciesandstockas it is forby-catchBecauseofthisthelocationandbiodiversitytargetofconservationactionsfallingundertheldquooffsetrdquoheadinghassometimesbeenlooselyrelatedtotheactual impactBest-practicestandardsstatethatoffsetsmustbeimplementedasclosetothedamagingactivitiesaspossibleandfocusonbiodiversityassimilaraspossibletothatwhichhasbeenimpacted (BBOP 2012) However there have also been calls forldquoout-of-kindrdquooffsetsthatgivemoreconservationbang-for-buckbyfocussingonthreatenedspeciesorrarehabitatsorareasinneedofconservation rather than the impactedareasor specieswhichmay be considered less ldquovaluablerdquo for conservation (Bull Hardyetal2015)Thishasledtosubstantialdebateastotheappropri-atelimitsonthegeographicscaleandbiodiversityfocusforoffset-ting(egApostolopoulouampAdams2017)Italsodrawsattentiontothesubjectiveanduser-definednatureof theword ldquobiodiversityrdquo(Morar ToadvineampBohannan 2015) As it is impossible fully tooperationalizetheconceptimplementersofthemitigationhierar-chyhavelatitudetointerpretbiodiversityaccordingtoforexampleeaseofmeasurement perceived societal valueormitigation cost(Maron etal 2016) In our casewe take a narrow focus on theby-caughtspecies itself this is in linewithmuchof the literatureon by-catch but notwith the broader discourses on ecosystem-basedapproachestomarinemanagementandecosystemservices(RosenbergampMcLeod2005)Thesediscoursessuggest theneedforamorefunctionalecosystem-basedapproachtononetlossofbiodiversitythishasyettotranspireeitherinthemarineorintheterrestrialliteraturepossiblybecausesubstantialchallengesinde-finingimpact-affectedbiodiversitytheninevitablyensue

Asmarinemegafauna stocks are often transboundary andmi-gratorydefiningtheappropriatespatialunit foroffsettingmaybe

achallengebecause themosteffective location foranoffsetmayormaynotbewithintheareaofinfluenceofagivenfisheryClearlyandpreciselydefining the spatial unitwithinwhich themitigationhierarchywill be implemented during theprocess of defining theoverallgoal(suchasNNL)isvitalThisunitshouldreflectthescaleoverwhichanactionwillaffectλToffsetswhicharewithinthedis-tributionofthefocalstockoftheby-caughtspecies(asdefinedforEquation1)arenotout-of-kindHoweverchallengesemergewhenthe appropriate spatial unit for offsetting activities is different totheappropriatespatialunitforotherelementsofthemitigationhi-erarchywhicharelikelytobedefinedinsteadbyjurisdictionalareaor target fish stock distribution Inmany fisheries the species af-fectedbyby-catchmaynotbewellenoughknownandoffsetsmayaccordinglyneedtobebroadlytargetedtobenefitanypotentiallyaffectedspeciesTrueout-of-kindoffsetswouldincludefundingtheconservationofunaffectedspeciesorstocksofhabitatsnotusedbythefocalstockorcontributionstoaconservationfundwithoutaclearcommitmentthatthefundsaretobespentonincreasingλT for thefocalby-caughtstockTheseareunlikelytoformpartofbest-practiceguidanceforby-catchoffsets

43emsp|emspResearch as an offset

Arelatedareaofactivecontroversyformarineby-catchiswhetherresearchor informationgatheringshouldbeseenasavalidoffsetmechanism The rationale is that this research could be used toreduceuncertaintypromote innovationand thereby improveout-comes for by-caught species albeit indirectly An offset could beusedto incentivizebetterdatacollectionfor instanceusingaby-catchlevytopayfortaggingortoputby-catchobserversorelec-tronicmonitoringsystemsonboatsThismightbeapreludetolatermitigation or avoidance activities once more is known about thebiological settingWhether research activities could appropriatelybeconsideredaspartofanldquooffsetrdquoiscontroversialmdashinsomecasesan indirectbenefit to theby-caught stockmightbe clearly appar-ent(egtheoceanicwhitetip(Carcharinus longimanusCarcharinidae)case-studyinTable3)whileinothercasesusinginvestmentinre-searchasanoffsetcouldbeseenasacaseofmoralhazardpoten-tially compromising scientistsrsquo independence and having at best ahighlyindirectrelationshiptoNNLoftheby-caughtspeciesAnotherviewisthatreducinguncertaintyisacoreresponsibilityofoperatingafisherywhichthereforeshouldbebornebythemanagementau-thorityorfishingbusinessesInterrestrialsystemsthesedilemmasalsoexistbutthesentimentismuchmoreclearlyexpressedthatre-searchactivitiesarenotappropriateoffsets(BullGordonWatsonampMaron2016)

44emsp|emspIncentivizing implementation of mitigation measures

Thefactorsthatdrivedecision-makingaboutmegafaunaby-catchreduction (by skippers companies fishery managers policymak-ers and other stakeholders) include legal obligations tominimize

emspensp emsp | emsp9MILNER- GULLAND Et AL

by-catch at the national or international levels (eg FAO 2011Rice 2014) the availability and quality of technical fixes associ-atedcosts tofishers limitsonaccesstoseafoodmarketsaswellassocietalpressuresHowevermuchresearchonby-catchreduc-tion focuses on identifying and implementing technicalmeasuresto reduceBPUE rather thanon the social andeconomicbarriersto implementation (Campbell amp Cornwell 2008) Technologicalinnovation to improve BPUE needs to be appropriately incentiv-izedwitheffortsmadetoensurethatsuchmeasuresareascost-effective as possible for fishers (Gjertsen Hall amp Squires 2010Lent amp Squires 2017) However it often happens that even ap-parently suitable by-catchmeasures are notwidely implemented(eg Damalas amp Vassilopoulou 2013 Orphanides amp Palka 2013RadzioSmolinskyampRoosenburg2013)Inthesecasesthedegreeofnon-implementationandthereasonsbehinditneedstobeun-derstoodsoitcanbeaddressed(Coxetal2007)Thesetypesofconsiderationarealsonotwellresearchedintheterrestrialoffset-tingliteraturebecausecomplianceispoorlymonitored(BullSuttleGordonSinghampMilner-Gulland2013)andthereislittlesupportfor researchon thebarriers to implementationofamitigationhi-erarchyandhowtosupportdeveloperstoaddressthesebarriers(BullBryantBakerampMilner-Gulland2015)Thesocialimpactsofimplementingabiodiversitymitigationhierarchyonresourceusersarementioned inguidance (egBBOP2012)buthowtomeasureandaccountforthemisverypoorlyunderstoodThefewstudiesin-vestigatingdeliveryofpromisedoffsetmeasuresinterrestrialsys-temssuggestaverypoorrecord(QueacutetierRegneryampLevrel2014)Therefore the social side of implementing the mitigation hierar-chyand incentivizingcompliance isanarea thatneedsmore andmoreactiveresearchwithinboththeterrestrialandmarinerealms(FultonSmithSmithampvanPutten2011)Thisisparticularlytruewhentheburdenof implementingmitigationapproaches isbornebyrelativelysmall-scaleproducersratherthangovernmentsormul-tinationals(egthepelagiclonglinefisheriesinTable3)

45emsp|emspSocietal limits

Foraspeciesathighriskofextinctioncompleteavoidanceofby-catchmightbethemostdesirablepolicyfrombothamanagementagency and societal perspective In addition with emblematic orhighlythreatenedmarinemegafaunaitmaybeviewedbymembersof the public asmorallywrong to kill any individuals even ifmiti-gationisinplace(egMauirsquosdolphinHamneretal2014) leadingtopressureongovernmentstoreflectthisethicalconcerninregu-lationsThesedilemmasecho the issueof thresholds in terrestrialoffsetswhichrecognizesthattherearesomecriticalareasinwhichdevelopmentisnotsocietallyappropriateregardlessofthepoten-tialformitigationandotherareasinwhichthemitigationhierarchycan be appropriately applied (Bull etal 2013) Examples of loca-tionswhereathresholdapproach isseenasappropriate interres-trial systems include the habitat of highly endangered species orecosystemswhich are limited in extent and irreplaceable (such asoldgrowthforest) In terrestrialsystems therefore themitigation

hierarchyisseenasmostappropriateforapplicationinmorecom-monanddegradedhabitatssuchasfarmlandSimilarlyinfisheriestheremaybesomesituationsinwhichthestockssubjecttoby-catchare so precious or threatened that no level of threat from fishingcanbecontemplatedandotherswherefishingsubjecttoNNLandthemitigationhierarchyisasociallyacceptableapproachInsitua-tions inwhich trade-offs between conservation and developmentareseenasnecessaryoracceptablebywidersocietyasociallicencetooperatemaybegainedthroughadoptingoffsetsintheabsenceofregulationForexampleinsub-SaharanAfricaseverallargedevel-opmentprojectsareattemptingtooffsettheirimpactsongreatapesandtheirhabitats(Kormosetal2014)Aby-catchequivalentmightbe fishing companies voluntarily donating funds for turtle nestingbeachrestorationintheirareaofoperationinadditiontocomply-ingwithregulatoryby-catchmitigationmeasuresThesemeasuresmayimprovetheimageofthecompanywiththegeneralpublicbuttoavoidaccusationsofldquogreenwashingrdquotheireffectivenessneedstobeproperlyscrutinized(Bulletal2016)Transparentlyembeddingthesetypesofactionswithinamitigationhierarchysuchasweareproposing and critically evaluating their contribution to increasingthepopulationgrowthrate(asperEquation1)wouldbeonewaytopromptsuchscrutiny

46emsp|emspUncertainty

The nature of the uncertainties surrounding biology and enforce-ment in themarine setting raisesquestions about theorderingofsteps in themitigationhierarchy inaway that isdissimilar to ter-restrialsystemswherethehierarchyofuncertaintiesmaybecleareranduncertaintyisgenerallylowerForexampleitmaybethattheimpactonoverallpopulationgrowthrateofanoffsetmeasurelikeeradicating invasivespecies fromaseabirdnestinghabitat isbothless uncertain and more cost-effective than avoidance measuressuchasclosingareaswhichmayormaynotbefrequentedbyadultseabirds in a given time-periodGenerally though itmightbe as-sumedthatmeasureswhichtargetlifestagessubjecttohighlevelsofnaturalmortalityorwithinwhichindividualcontributiontoover-allpopulationgrowthrateislow(egheadstartingjuvenileturtles)maybelesseffectiveinachievingNNLthanmeasureswhichtargetreproductivelymatureadultfemales(suchaslivereleasesHeppellCrowderampCrouse1996)Howeverbeforeimplementinganoffsetthataimstoimprovethesurvivalofonelifestageinordertocom-pensatefortheby-catchmortalityofanotherarobustassessmentoftheconsequences(withassociateduncertainties)shouldbecar-ried out through detailed population modelling based on strongempiricalstudies(cfWallaceHeppellLewisonKelezampCrowder2008)Interrestrialsystemstherequirementsequentiallytoapplythemitigationhierarchyisbroadlyunchallengedbutactuallysimilararguments apply For example habitat restoration sits above off-settinginthehierarchyandyetitisalong-termuncertainprocesswhichmayinsomecircumstancesbemuchlesspreferabletoanoff-setusingawell-establishedapproachwhichishighlylikelytoleadtoconservationgains

10emsp |emsp emspensp MILNER- GULLAND Et AL

47emsp|emspTemporal considerations

Thetimingofoffsetsinrelationtootherelementsofthemitigationhierarchyhasbeenthesubjectofdebatewithintheterrestriallitera-tureThemainsuggestionforaddressingthetemporarylossofbio-diversitywhileoffsetscometofruitionhasbeenadoptingmitigationbankingwherebyoffsetsareimplementedinadvanceofpotentiallydamagingactivitiesprovidingbiodiversitycreditswhichcanbeusedtocompensateforlaterlossesThisbothremovesanelementofun-certaintyfromtheoffsetimplementationandreducesthetimelagbetweenlossandgain(Mann2015)Withrespecttomarinemega-faunaby-catchflexibilityintimingprovidesadditionalscopeforcostreduction and benefit enhancementwhichmay not be present intraditionalhabitat-basedterrestrialoffsetsForexampletemporarymeasuressuchasashort-termby-catchtaxtofundanoffsetmaybeusedifmitigationoravoidancemethodstaketimetocomeonlineorifatemporarynudgeisenoughtocausebehaviouralchangeThismightbethecaseifapolicywasneededtoinducefisherstotakeupnewgeartoavoidthecostofanoffsetorifconcernsaboutsafetyoryieldreductionsduringthetransitiontonewgearcouldbeallayedbyatemporarysubsidyforearlyadoptersorapaidparticipatorymoni-toringprogrammeto informwider implementation(egthemobu-lidandsharkcase-studiesinTable3)Justasforhabitatrestoration(ZedlerampCallaway 1999) by-catchoffset strategieswhich targetjuvenilestagesof long-livedspecies (eg turtleheadstartingor in-vasive removal fromseabirdnesting islands)may takemanyyearsfor their effects to become apparent in an increase in populationgrowthratesAdditionaluncertaintyisintroducedbythedifficultyinmonitoringpopulationsofmanyby-catch species (eg seabirdsHatch2003)leadingtouncertainestimatesoftheimpactofoffsetactivitiesonpopulationgrowth(seecase-studiesinTable3)Theseproblemsarenot insuperablehoweverpositivetrendshavebeenreportedinturtlepopulationsoverdecadesasaresultofnestpro-tection(egDuttonDuttonChaloupkaampBoulon2005)

5emsp |emspUSING INCENTIVES TO REDUCE BY- C ATCH

Manyoftheexamplesandprinciplesdiscussedaboveeitherimplic-itlyorexplicitlyrelatetotheeconomicsocialinstitutionalormoralincentivesoperatingondifferentactorsinsideandoutsidethefish-erywhichcanbepositiveornegativeWenowturntoadiscussionofhowincentivescanbeusedtoreduceby-catchwithinourframe-workIncentivescanbeputinplacetochangefisherbehaviourwithrespecttoanyoftheelementsoftheframework (avoidminimizeremediateandoffsetTable3)Althoughdiscussedintheliteraturemostof these incentive approaches are yet tobe implemented inthe realworldparticularly forby-catchThereforeuntil empiricalevidenceoftheireffectivenessisavailablethesesuggestionscomewithacaveat

Financial costsofby-catchmitigationactions canarise for in-stancefromlostcatchcapitalinvestmentsinnewgearormitigation

equipmentor the lossofaccesstoafisheryCostsmayalsoarisefromthedeploymentofby-catchobserversortrainingintheuseofnewgearThesecostscanbepaidbyfishingcompaniesorindivid-ualsorbygovernmentsNGOsorseafoodconsumersWhetherornotcompensationforcostsincurredbyfishersisseenasappropri-atedependsonwhetherby-catchreductionisseenasasocialgoodthatfishersareproviding(inwhichcasetheyshouldbecompensatedforit)orasputtingrighttheharmthattheyaredoingtobiodiver-sitywhilegeneratingtheirownprivategain(ineconomiclanguagewhetherby-catchisviewedasanunpricedexternalityinwhichcasetheyshouldpay)Italsodependsonwhethereconomichardshipwillensueacaseforcompensationofby-catchreductioncostsincurredbypeopledependenton fishing for their livelihoodsmaybemoresympatheticallyreceivedbyotheractorsthanacasemadebyalargemultinationalfishingcompany

Ifby-catchisseenasanunpricedexternalityitmightbesociallyoptimaltotaxfishersfortheirby-catchsothatthisexternalityisin-ternalizedThisplacesanexplicitpriceuponby-catch(Boyce1996Pascoeetal2010SquiresampGarcia2014)Theby-catchprice islikely to be incorporated into the price of the target species andtherebybecomespartofthetargetspeciescostThispricecouldbeset differently for different demographic classesof theby-caughtspecies depending on the impact the loss of an individualwouldhaveonthepopulationAllelsebeingequalputtingapriceonby-catchmeans that theseafoodproduct that is the targetcatchbe-comesmoreexpensiveandconsumershave topaymore for theirseafoodreducingdemandTheninprincipleeveryfirminthesup-plychaineveryvesselandeveryconsumerhaveanincentivetore-duceby-catchuntileacheconomicactorrsquosmarginalcostofby-catchreductionequals thecommonpriceofby-catch that theyall faceOffsetsareonewaytopriceandinternalizetheby-catchexternalitycostIfanoffsettingactioniscostlytoimplementandmustbepaidforwith each unit of by-catch it implicitly prices the residual by-catch In this circumstance the effect from a financial standpointisthesameasaby-catchtaxwiththe levelsetbasedonthecostoftheoffsetVariousinstitutionalstructurestosupportthischargeperunitofby-catcharepossiblewithdifferentimplicationsintermsofthedistributionofcostsandbenefitsForexampleaninsuranceschemecouldbepaidintobyfishersthatpaysoutintheeventofaby-catcheventtherebyspreadingthecostofunavoidablerareby-catcheventsOratradablepermitschemecouldoperatesuchthatfisherswhoexperienceaby-catcheventcanbuyapermitwiththecostvaryingdependingondemandforpermits (henceprovidingavessel-levelincentivetoinnovatetoreduceby-catch)

If there isdemandforconservation inan internationalmarketthen price premiums and market access (through eco-labellingsupply chain certification other food sustainability campaignsWardampPhillips2010)orboycottsactingasstrategicthreatsfromconsumers (Kotchen 2013 Segerson 2010) could act as positiveornegativeeconomic leversonthe fisheryprovidingan incentivefor fishers to reduce their by-catch voluntarily (as has been sug-gested for the Brazilianmahi-mahi fishery Table3) For exampletheMarine StewardshipCouncil now includesby-catchmitigation

emspensp emsp | emsp11MILNER- GULLAND Et AL

intheircertificationprocess(MSC2014)Demand-ledleversmaybemoreorlessapplicableatdifferentlevelsinthehierarchyforexam-pleavoidancemayberelativelyhardtoevidencewhileoffsettingmaybelesseasytoselltoaconsumerthanminimizationorreme-diationConcerns about the unintended consequences of positiveincentives (particularlyfordirectsubsidiesratherthanconditionalincentives)maydeterminewhethertheyareanappropriateinstru-mentinagivencaseForexampletheymaybeinappropriateifthereisariskthattheadditionalmoneyisreinvestedinincreasedfishingcapacityor iftheremaybeconsumptionproductionorconserva-tionleakages(transferoftheproblemsomewhereelse)whetheratthe vessel fishery or trans-national levelHigh transactions costsmayalsolimitthebenefitsofincentivesschemes

Otherchangeswhichmayneedtobeincentivizedforsuccessfulimplementationofby-catchreductionpoliciesmaybelessamenabletofinancialmeasuresatleastpartlybecauseitislessclearhowtoassign financial value to theactionsor to thebenefits and losseswhichtheyproduceForexampleperceivedreductionsinsafetyforfishingcrews(fromweightedlonglinesfor instance)arecoststhatmaybehardtovaluefinanciallyOtherprerequisitesfor long-termsustainable behaviour change such as changes in social norms sothatfishingcommunitiesseeby-catchreductionasappropriatebe-haviourortechnicalskillacquisitionsothattheycanusenewmeth-odsmaybeincentivizedbycarefullydesignedinterventionsworkingwithfishers(Halletal2007)Conservationpoliciesbasedoneco-nomic incentives (extrinsicmotivation) are not always superior tothosebasedupon intrinsicmotivation Infact incentive-basedby-catch reduction policy instruments could even be counterproduc-tivebyreducingtheeffectivenessofintrinsicmotivationdependingupon the situation (although the empirical evidence on this topicisweak RodeGoacutemez-BaggethunampKrause 2015) If the changerequiredforby-catchreductiontoworkmeetscultural resistancethenparticipatory researchmightbeespeciallyeffective inbreak-ingdownbarriersbetweenthosewhowantby-catchreductiontotakeplaceandthosewhoactuallyhavetoimplementit(thefishers)ForexampleinAustraliathegovernment-fundedbodyOceanwatchfacilitatesengagementbetweencommunities thefishing industryseafood suppliers and government to improve knowledge sharing(wwwoceanwatchorgau)Innovationiscrucialinfisheriesandfish-ersareaccustomedtoadoptingnewtechnologyorprocessespo-tentiallymakingan incentivizedparticipatory researchprogrammeespeciallyfruitful

Sometimes the most efficient way to solve problems is a so-cial instrumentoran institutionalchange inplaceoforaswellasan economic instrument For example supporting developmentof fisherorganizations rather than instituting a vessel-level taxorsubsidy might provide the impetus needed to change behaviourInstitutingcatchshares(individualtransferablequotas)mayprovideanenablingenvironmentforby-catchreductionforexamplebypro-motingmoreeffectivemonitoring(Grimmetal2012)Experiencein terrestrial system produces similar insights incentive-basedschemeswhichalsobuildcommunitycohesionandsupportthede-velopment or strengthening of localmanagement institutions are

more effective in the longer run than direct economic incentives(Clementsetal2010)

6emsp |emspCONCLUSIONS

The framework we present here is novel It draws upon and ex-tends the frameworks for conceptualizing by-catch developed byHall (1996) and Hall Alverson andMetuzals (2000) It amalgam-atesHallrsquos frameworkwith themitigationhierarchyasused in theEnvironmental Impact Assessment literature (BBOP 2012) Thesuggestions about goals metric andmitigation actions are drawnfromtheempiricalby-catchliteratureandtheissueswediscussin-tegratetheconcernsoftheextensiveterrestrialandnascentmarineoffsetting literature with the by-catch literature The frameworkmakesclear thatanearlycrucial step is toclarify thegoalofanyby-catch reduction policyOverarching goals like those issued bytheConventiononBiologicalDiversity(egAichiTarget11that10ofmarinehabitatshouldbeunderprotectionby2020)needtobetranslatedintooperationaltermswithineachfisheryCurrentlyleg-islatedoragreedby-catch reductiongoals tend tobe less specificthantheycouldbeandthisleadstoproblemsininterpretingthesegoals inordertoplanaby-catchmitigationstrategy(seethecase-studies inTable3 for examples) This ambiguity is tobe expectedwithinnegotiatedtargetsbutitisachallengenonetheless(Maxwelletal2015)Usingacommonunitofby-catch impactsuchastheΔλTwhichweuseherewouldbehelpfulbothinclarifyingexpecta-tionsandevaluatingtheeffectivenessofelementsofthemitigationhierarchy

Once the by-catch goal is known options for implementingavoidanceminimizationremediationandoffsetscanbeclarified(asinTable2)Howeveroutsideof the interconnectedbiologyof theecosystemby-catch isembeddedwithinsocialandeconomicsys-temsDifferentunitsofanalysismaybeneededatdifferent levelsofthehierarchytocopewiththechallengesofincompleteoverlapbetween jurisdictional units fisheries target stocks and by-catchstocksJurisdictionalissuesareimportantandcomplexpotentiallyimpeding implementationFleets interact raisingtheriskofpolicyleakageforexampleifpeopleshifttootherfisheriesgearorliveli-hoodsThereforethescaleatwhicheachelementofthemitigationhierarchyisimplementedislikelytovarywithincentivestomitigateoftenbeingbest appliedat thevessel level focussedon reducingindividualmortalitywhileoffsettingisimplementedatthescaleoftheby-catchspeciesrsquostockWithtransboundaryspeciesunilateralconservationinonejurisdictioncreatesthepotentialforproductiontrade and conservation leakages For example a conserving Statecouldimplementtheavoidancestepandshutdownordramaticallycurtailitsownproductionofswordfishtoreduceseaturtleby-catchbuttheknock-oneffectmaybemoreimportationofswordfishfromfleetswithhigherseaturtleby-catch(RausserHamiltonKovachampStifter2009)

Translatingtheframeworkfromaspeciestoanecosystemlevelwill require consideration of the potential interactions between

12emsp |emsp emspensp MILNER- GULLAND Et AL

by-catchmitigationapproachestargetedatdifferentspecies(Serafyetal 2012) Actions to mitigate by-catch for one group of spe-cies can increase or decrease it for others and so a system-wideapproach isneededForexample changing fromJ-hooks tocirclehookstoreducemortalityofturtlesmaydecreaseorincreasesharkmortality(Andrakaetal2013GodinCarlsonampBurgener2012)In terrestrial systems similar interactions arise and value judge-mentsaremade(whetherexplicitlyorimplicitly)astowhatlossandgain of ldquobiodiversityrdquo translates to in operational terms andwhatelementsofbiodiversitymattermosttoimplementers

Uncertainty is high in ocean ecosystems creating both chal-lengesandopportunitiesinapplyingtheconceptofNNLthroughamitigationhierarchythatincludesoffsettingInparticularformarinemegafaunathereishighuncertaintyintheprocesseslinkinganyel-ementofthemitigationhierarchythroughtochangesinpopulationgrowthrateFurthermore impactscanbelong-termhardtomea-sureandspatiallydiffuseanduncertaintyisnotpredictablyspreadthroughthehierarchyThiscreatesadifferentsetofchallengestothosefacedinterrestrialsystemswhereatleastforsometypesofenvironmentalimpactthelinksbetweenactionandimpactarerel-ativelydirectandmeasurableanduncertaintygenerally increasesthroughthemitigationhierarchy (fromavoidthroughminimizere-mediatetooffset)

By-catch reduction measures have had significant successesoverthelastdecadesasaresultofsubstantialinvestmentoftimeand funding by researchers management authorities conserva-tionorganizationsandfishers(Coxetal2007)Howeverthissuc-cessisnotuniversalJustasforanyfisheriesmanagementissueapoorregulatoryregimelimitedcomplianceandlackofinforma-tionhampereffortstoreduceby-catchInsomeplaceshighlevelsofby-catch limitedoptions formitigationandweakgovernance(leadingtopoorenforcement)cancombinetomaketheby-catchproblemintractableOurframeworkwillnotsolvetheseproblemsHowever itbrings together the full rangeofapproaches forby-catchmitigationinastructuredandsystematicwaywhichrequiresatargettobeexpressedagainstwhichoutcomescanbeevaluatedByexposingareasofuncertaintyanddatadeficiencyitcouldchal-lengescientistsandmanagerstoobtainthedatarequiredproperlytoevaluate theeffectivenessofmitigationmeasuresThis couldthensupportandencourageclearerdecision-makingandprioriti-zationofactionsOurframeworkdemonstratesthattheprincipleof implementing thegoalofnonet loss throughamitigationhi-erarchy isasapplicable tomarinemegafaunaby-catchas to ter-restrial systems where it is already widely used in challengingdata-poorcircumstances

There isuntappedpotential forcost-effectiveby-catchmitiga-tionwhichcouldberealizedwiththeadoptionofthisframeworkandwithconsiderationofnewapproachestoincentivizingby-catchmitigationwithinthestepsofthehierarchyApplyingittoafewcase-studiesinpracticewilldemonstrateempiricallywhereandhowthepotentialforimprovedeffectivenesscouldbestberealizedExistinglegalframeworksoftenprecludeapproacheswhichimplicitlyorex-plicitly permit by-catch including the use of economic incentives

ornewapproachessuchasoffsetsHoweverinthiscontextofdy-namicuncertaintythedividendsofthinkingmorecreativelyaboutby-catchmitigationcouldbehigh

ACKNOWLEDG EMENTS

EJMG acknowledges the Pew Charitable Foundation for its sup-port of thiswork This article originated at a 2013workshop co-organized by NOAA-Fisheries and IUCN-CEEM-FEG entitledldquoMultidisciplinaryWorkshoptoAddressEcosystem-LevelImpactsofFisheriesBycatchonMarineMegafaunaBiodiversityConservationthrough Mitigation Policy Economic Instruments and TechnicalChangerdquo We thank the reviewers for their insightful commentswhichmuchimprovedthemanuscript

ORCID

E J Milner-Gulland httporcidorg0000-0003-0324-2710

R E FE R E N C E S

Alfaro-Shigueto J Dutton P H amp Mangel J (2007) Interactionsbetween leatherback turtles and Peruvian artisanal fisher-ies Chelonian Conservation and Biology 6 129ndash134 httpsdoiorg1027441071-8443(2007)6[129ibltap]20co2

Alfaro-Shigueto JMangel JCBernedoFDuttonPHSeminoffJAampGodleyB J (2011) Small-scale fisheriesofPeruAmajorsinkformarineturtles inthePacificJournal of Applied Ecology481432ndash1440httpsdoiorg101111j1365-2664201102040x

Alfaro-ShiguetoJMangelJCPajueloMDuttonPHSeminoffJ A amp Godley B J (2010) Where small can have a large im-pact Structure and characterization of small-scale fisheries inPeru Fisheries Research 106 8ndash17 httpsdoiorg101016jfishres201006004

Andraka SMugM HallM PonsM Pacheco L ParralesM hellipOrtega D (2013) Circle hooks Developing better fishing prac-ticesintheartisanallonglinefisheriesoftheEasternPacificOceanBiological Conservation 160 214ndash224 httpsdoiorg101016jbiocon201301019

ApostolopoulouEampAdamsWM(2017)BiodiversityoffsettingandconservationReframingnaturetosaveitOryx5123ndash31httpsdoiorg101017S0030605315000782

BaacuteezJCRealRGarciacutea-SotoCJoseacuteMMaciacuteasDampCamintildeasJA(2007)Loggerheadturtleby-catchdependsondistancetothecoastindependentoffishingeffortImplicationsforconservationandfish-eries management Marine Ecology Progress Series 338 249ndash256httpsdoiorg101017S0030605315000782

BBOP (2012) Standard on biodiversity offsets Business and biodiversity offsets programmeWashingtonDCForestTrends

Bishop J (2006) Standardizing fishery-dependent catch and ef-fort data in complex fisheries with technology change Reviews in Fish Biology and Fisheries 16 21ndash38 httpsdoiorg101007s11160-006-0004-9

BoyceJ(1996)AneconomicanalysisofthefisheriesbycatchproblemJournal of Environmental Economics and Management31 314ndash336httpsdoiorg101006jeem19960047

BugoniLManciniPLMonteiroDSNascimentoLampNevesTS(2008)SeabirdbycatchintheBrazilianpelagiclonglinefisheryandareviewofcaptureratesinthesouthwesternAtlanticOceanEndangered Species Research5137ndash147httpsdoiorg103354esr00115

emspensp emsp | emsp13MILNER- GULLAND Et AL

BullJWampBrownlieS(2017)Thetransitionfromnonetlosstoanetgainof biodiversity is far from trivialOryx51 53ndash59 httpsdoiorg101017S0030605315000861

BullJWBryantCBakerJampMilner-GullandEJ(2015December28)Developing measuring and communicating the outcomes of cor-porate biodiversity strategies [pdfdocument]RetrievedfromhttpwwwwildbusinessorgBull_etal_2015_WBLpdf

BullJWGordonAWatsonJEampMaronM(2016)Seekingcon-vergenceonthekeyconceptsinlsquononetlossrsquopolicyJournal of Applied Ecology531686ndash1693httpsdoiorg1011111365-266412726

BullJWHardyMJMoilanenAampGordonA (2015)Categoriesof flexibility in biodiversity offsetting and their implications forconservation Biological Conservation 192 522ndash532 httpsdoiorg101016jbiocon201508003

Bull JW Lloyd S P amp StrangeN (2017) Implementation gap be-tween the theory and practice of biodiversity offset multipliersConservation Lettershttpsdoiorg101111conl12335

Bull JW SuttleKBGordonA SinghN JampMilner-Gulland EJ(2013)BiodiversityoffsetsintheoryandpracticeOryx47369ndash380httpsdoiorg101017S003060531200172X

CampbellLMampCornwellML(2008)Humandimensionsofbycatchreduction technology Current assumptions and directions for fu-tureresearchEndangered Species Research5325ndash334httpsdoiorg103354esr00172

Caswell H Brault S Read A J amp Smith T D (1998) Harborporpoise and fisheries An uncertainty analysis of inciden-tal mortality Ecological Applications 8 1226ndash1238 httpsdoiorg1018901051-0761(1998)008[1226hpafau]20co2

ClementsTJohnANielsenKAnDTanSampMilner-GullandEJ (2010)Payments forbiodiversityconservation in thecontextofweak institutions Comparison of three programs from CambodiaEcological Economics 69 1283ndash1291 httpsdoiorg101016jecolecon200911010

CoxTLewisonRŽydelisRCrowderLSafinaCampReadA(2007)ComparingeffectivenessofexperimentalandimplementedbycatchreductionmeasuresTheidealandtherealConservation Biology211155ndash1164httpsdoiorg101111j1523-1739200700772x

CrollDADewarHDulvyNKFernandoDFrancisMPGalvaacuten-Magantildea F hellip Newton K M (2016) Vulnerabilities and fisher-ies impactsTheuncertain futureofmanta anddevil raysAquatic Conservation Marine and Freshwater Ecosystems 26 562ndash575httpsdoiorg101002aqc2591

Damalas D amp Vassilopoulou V (2013) Slack regulation com-pliance in the Mediterranean fisheries A paradigm from theGreek Aegean Sea demersal trawl fishery modelling discardogives Fisheries Management and Ecology 20 21ndash33 httpsdoiorg101111j1365-2400201200860x

DuttonDLDuttonPHChaloupkaMampBoulonRH(2005)IncreaseofaCaribbeanleatherbackturtleDermochelys coriaceanestingpop-ulation linked to long-termnestprotectionBiological Conservation126186ndash194httpsdoiorg101016jbiocon200505013

DuttonPJosephJSquiresDampWilliamsM(2011)Bellagioblue-print foractiononseaturtlesChapter2 InPDuttonDSquiresampM Ahmed (Eds) Conservation of pacific sea turtles (pp 15ndash36)HonoluluHIUniversityofHawaiiPress

DuttonPampSquiresD (2008)AholisticstrategyforPacificseatur-tlerecoveryOcean Development and International Law39200ndash222httpsdoiorg10108000908320802013685

FAO (2011 January 5) International guidelines on bycatch manage-ment and reduction of discards Rome Italy Food and AgricultureOrganisation [pdf document] Retrieved from httpwwwfaoorgdocrephelliptba0022t00pdf

Finkelstein M Bakker V Doak D F Sullivan B Lewison RSatterthwaite W H hellip Henry R W (2008) Evaluating the po-tential effectiveness of compensatory mitigation strategies for

marinebycatchPLoS ONE3 e2480httpsdoiorg101371jour-nalpone0002480

FowlerSJ(2016January5)Draft best practice mitigation guidelines for sharks and rays taken in purse- seine and long-line fisheries Convention on Migratory Species[pdfdocument]RetrievedfromhttpwwwcmsintsitesdefaultfilesdocumentCMS_Sharks_CWG1_Doc_3_2pdf

FrancisMP(2014)Survival and depth distribution of spinetail devilrays (Mobula japanica) released from purse-seine catches NIWA ClientReportNoWLG2014-2WellingtonNewZealandDepartmentofConservation

Fulton E A Smith A D Smith D C amp van Putten I E (2011)Human behaviour The key source of uncertainty in fish-eries management Fish and Fisheries 12 2ndash17 httpsdoiorg101111j1467-2979201000371x

GardnerTAHaseABrownlieSEkstromJMPilgrimJDSavyCEhellipTenKateK(2013)BiodiversityoffsetsandthechallengeofachievingnonetlossConservation Biology271254ndash1264httpsdoiorg101111cobi12118

GjertsenHHallMampSquiresD(2010)IncentivestoaddressbycatchInRAllenJJosephampDSquires(Eds)Conservation and manage-ment of transnational tuna fisheries (pp225ndash250)Ames IAWiley-Blackwellhttpsdoiorg1010029780813820262ch14

Gjertsen H Squires D Dutton P amp Eguchi T (2014) Cost-effectivenessofalternativeconservationstrategieswithapplicationtothePacificLeatherbackTurtleConservation Biology28140ndash149httpsdoiorg101111cobi12239

GodinACCarlson JKampBurgenerV (2012)Theeffectofcirclehooks on shark catchability and at-vessel mortality rates in long-lines fisheriesBulletin of Marine Science88 469ndash483 httpsdoiorg105343bms20111054

GrimmDBarkhornIFestaDBonzonKBoomhowerJHovlandV amp Blau J (2012) Assessing catch sharesrsquo effects evidencefrom Federal United States and associated British Columbianfisheries Marine Policy 36 644ndash657 httpsdoiorg101016jmarpol201110014

HallMA(1996)OnbycatchesReviews in Fish Biology and Fisheries6319ndash352httpsdoiorg101007BF00122585

HallMAAlversonDLampMetuzalsKI(2000)By-catchProblemsand solutions Marine Pollution Bulletin 41 204ndash219 httpsdoiorg101016S0025-326X(00)00111-9

HallMANakanoHClarke S Thomas SMolloy J PeckhamSHhellipHallSJ (2007)Workingwithfisherstoreduceby-catchesIn S J Kenelly (Ed)By-catch reduction in the worldrsquos fisheries (pp235ndash288) Dordrecht The Netherlands Springer httpsdoiorg101007978-1-4020-6078-6_8

HallM amp RomanM (2013)Bycatch and non-tuna catch in the tropi-cal tuna purse seine fisheries of the worldFisheriesandAquacultureTechnicalPaper568RomeItalyFAO

HallMASwimmerYampPargaM(2012)NoldquosilverbulletsrdquobutplentyofoptionsWorkingwiththeeasternpacificartisanalfisherstore-duceseaturtlemortalityinfisheriesInJASeminoffampBWallace(Eds)Sea turtles of the eastern pacific Advances in research and con-servation(pp136ndash153)TucsonAZUniversityofArizonaPress

HamnerRMWadePOremusMStanleyMBrownPConstantineR amp Baker C S (2014) Critically low abundance and limits tohuman-relatedmortalityfortheMauirsquosdolphinEndangered Species Research2687ndash92httpsdoiorg103354esr00621

HatchSA(2003)Statisticalpowerfordetectingtrendswithapplica-tions to seabird monitoringBiological Conservation 111 317ndash329httpsdoiorg101016S0006-3207(02)00301-4

HeppellSSCrowderLBampCrouseDT(1996)Modelstoevaluateheadstartingasamanagementtoolforlong-livedturtlesEcological Applications6556ndash565httpsdoiorg1023072269391

HoughPampRobertsonM(2009)MitigationunderSection404oftheCleanWater ActWhere it comes from what it meansWetlands

14emsp |emsp emspensp MILNER- GULLAND Et AL

Ecology and Management 17 15ndash33 httpsdoiorg101007s11273-008-9093-7

IATTC(2015)Resolution on the conservation of mobulid rays caught in as-sociation with fisheries in the IATTC convention area Inter-AmericanTropical TunaCommission89thAnnualMeetingResolutionC-15-04LaJollaCAInter-AmericanTropicalTunaCommission

IFC(2012)Performance standard 6 Biodiversity conservation and sustain-able management of natural resources January 1 2012WashingtonDCInternationalFinanceCorporation

Innes J Pascoe S Wilcox C Jennings S amp Paredes S (2015)MitigatingundesirableimpactsinthemarineenvironmentAreviewofmarket-basedmanagementmeasuresFrontiers in Marine Science276httpsdoiorg103389fmars201500076

JanniseCSquiresDSeminoffJampDuttonP (2010)Conservationinvestments andmitigationTheCaliforniadrift gillnet fishery andpacificseaturtles InRQGraftonRHilbornDSquiresMTaitampMJWilliams(Eds)Handbook of marine fisheries conservation and management(pp231ndash240)OxfordUKOxfordUniversityPress

Jones E amp FrancisM (2012)Protected rays ndash Occurrence and devel-opment of mitigation methods in the New Zealand tuna purse seine fishery Auckland New Zealand National Institute of Water andAtmosphericResearch

KormosRKormosCFHumleTLanjouwARainerHVicturineR hellipWilliamson E A (2014) Great apes and biodiversity offsetprojectsinAfricaThecasefornationaloffsetstrategiesPLoS ONE9(11)e111671httpsdoiorg101371journalpone0111671

KotchenMJ (2013)Voluntaryand information-basedapproachestoenvironmentalmanagementApubliceconomicsperspectiveReview of Environmental Economics and Policy 7(2) 276ndash295 httpsdoiorg101093reepret012

Kyriazi Z LejanoRMaes FampDegraer S (2015)Bargaining a netgaincompensationagreementbetweenamarinerenewableenergydeveloperandamarineprotectedareamanagerMarine Policy6040ndash48httpsdoiorg101016jmarpol201506005

LentRampSquiresD(2017)ReducingmarinemammalbycatchinglobalfisheriesAneconomicsapproachDeep Sea Research Part II Topical Studies in Oceanography 140 268ndash277 httpsdoiorg101016jdsr2201703005

Lewison R L Crowder L B Read A J amp Freeman S A (2004)Understanding impactsof fisheriesbycatchonmarinemegafaunaTrends in Ecology amp Evolution19598ndash604httpsdoiorg101016jtree200409004

MannC (2015)StrategiesforsustainablepolicydesignConstructiveassessmentofbiodiversityoffsetsandbankingEcosystem Services16266ndash274httpsdoiorg101016jecoser201507001

Marine Stewardship Council (2014 June 21) MSC fisheries certifica-tion requirements v20 [pdf doc] httpswwwmscorgdocumentsscheme-documentsfisheries-certification-scheme-documentsfisheries-certification-requirements-version-20

MaronM IvesCDKujalaHBullJWMaseykFJBekessyShellip Possingham H P (2016) Taming a wicked problem Resolvingcontroversies inbiodiversityoffsettingBioScience66(6)489ndash498httpsdoiorg101093bioscibiw038

MaxwellSLMilner-GullandEJJonesJPKnightATBunnefeldNNunoAhellipRhodesJR(2015)BeingsmartaboutSMARTenvi-ronmentaltargetsScience3471075ndash1076httpsdoiorg101126scienceaaa1451

Moilanen A Van Teeffelen A J Ben-Haim Y amp Ferrier S (2009)Howmuch compensation is enoughA framework for incorporat-inguncertaintyandtimediscountingwhencalculatingoffsetratiosfor impactedhabitatRestoration Ecology17 470ndash478 httpsdoiorg101111j1526-100X200800382x

MorarNToadvineTampBohannanBJ(2015)Biodiversityattwenty-fiveyearsRevolutionorredherringEthics Policy amp Environment1816ndash29httpsdoiorg1010802155008520151018380

OrphanidesCDampPalkaDL(2013)Analysisofharborporpoisegill-netbycatchcomplianceandenforcement trends in theUSnorth-western Atlantic January 1999 to May 2010 Endangered Species Research20251ndash269httpsdoiorg103354esr00499

Pascoe S Innes J Holland D Finas M Theacutebaud O TownsendR hellip Hutton T (2010) Use of incentive-based managementsystems to limit bycatch and discarding International Review of Environmental and Resource Economics 4 123ndash161 httpsdoiorg10156110100000032

PhalanBHayesG Brooks SMarshDHoward PCostelloeBhellip Whitaker S (2017) Avoiding impacts on biodiversity throughstrengthening the first stage of the mitigation hierarchy Oryxhttpsdoiorg101017S0030605316001034

Queacutetier F Regnery B amp Levrel H (2014) No net loss of biodiver-sity or paper offsets A critical review of the French no net losspolicy Environmental Science amp Policy 38 120ndash131 httpsdoiorg101016jenvsci201311009

RadzioTASmolinskyJAampRoosenburgWM(2013)Lowuseofre-quiredterrapinbycatchreductiondevicesinarecreationalcrabpotfisheryHerpetological Conservation and Biology8222ndash227

RaineyHJPollardEHBDutsonGEkstromJMLivingstoneSRTempleHJampPilgrimJD(2015)AreviewofcorporategoalsofnonetlossandnetpositiveimpactonbiodiversityOryx49232ndash238httpsdoiorg101017S0030605313001476

Rausser G C Hamilton S F Kovach M amp Stifter R (2009)UnintendedconsequencesThe spillovereffectsof commonprop-ertyregulationsMarine Policy3324ndash39httpsdoiorg101016jmarpol200803020

Rice J (2014) Evolution of international commitments for fisheriessustainability ICES Journal of Marine Science Journal du Conseil71157ndash165httpsdoiorg101093icesjmsfst078

RichardYampAbrahamER(2013)ApplicationofPotentialBiologicalRemoval methods to seabird populations New Zealand AquaticEnvironmentandBiodiversityReport108

RodeJGoacutemez-BaggethunEampKrauseT(2015)Motivationcrowd-ingbyeconomic incentives inconservationpolicyAreviewoftheempiricalevidenceEcological Economics117270ndash282httpsdoiorg101016jecolecon201411019

RogersAA(2013)SocialwelfareandmarinereservesIswillingnesstopayforconservationdependentonmanagementprocessAdiscretechoiceexperimentoftheNingalooMarineParkinAustraliaCanadian Journal of Agricultural EconomicsRevue Canadienne Drsquoagroeconomie61217ndash238httpsdoiorg101111cjag12008

Rosenberg A A amp McLeod K L (2005) Implementing ecosystem-basedapproachestomanagementfortheconservationofecosystemservicesMarine Ecology Progress Series300 270ndash274 httpsdoiorg103354meps300270

Segerson K (2010) Can voluntary programs reduce sea turtle by-catch Insights from the literature in environmental economics InRQGraftonRHilbornDSquiresMTaitampMJWilliams(Eds)Handbook of marine fisheries conservation and management(pp618ndash629)OxfordUKOxfordUniversityPress

Serafy JECookeS JDiazGAGraves JEHallMShivjiMampSwimmerY(2012)CirclehooksincommercialrecreationalandartisanalfisheriesResearchstatusandneedsforimprovedconser-vation and management Bulletin of Marine Science 88 371ndash391httpsdoiorg105343bms20121038

ShiodeDHu F ShigaM Yokota K amp Tokai T (2005)Midwaterfloatsystemforstandardizinghookdepthsontunalonglinestore-duce sea turtleby-catchFisheries Science71 1182ndash1184httpsdoiorg101111j1444-2906200501080x

Sims M Cox T amp Lewison R (2008) Modeling spatial patternsin fisheries bycatch Improving bycatch maps to aid fisheriesmanagement Ecological Applications 18 649ndash661 httpsdoiorg10189007-06851

emspensp emsp | emsp15MILNER- GULLAND Et AL

Squires D amp Garcia SM (2014) Ecosystem-level impacts of fisheries bycatch on marine megafauna Biodiversity conservation through miti-gation policy economic instruments and technical changeReportofthe IUCN-CEM-FEGScientificworkshopGland Switzerland 7ndash10October2013GlandSwitzerlandIUCN

SquiresDampGarciaSM(inpress)Fisheries bycatch in marine ecosys-tems Policy economic instruments and technical change ChichesterUKJWileyampSons

SwimmerYArauzRMcCrackenMMcNaughtonLBallesteroJMusylMhellipBrillR(2006)DivingbehavioranddelayedmortalityofoliveridleyseaturtlesLepidochelys olivaceaaftertheirreleasefromlongline fishing gearMarine Ecology Progress Series323 253ndash261httpsdoiorg103354meps323253

TolottiMTFilmalterJDBachPTravassosPSeretBampDagornL(2015)BanningisnotenoughThecomplexitiesofoceanicsharkmanagementbytunaregional fisheriesmanagementorganizationsGlobal Ecology and Conservation 4 1ndash7 httpsdoiorg101016jgecco201505003

Tuck G N Polacheck T amp Bulman C M (2003) Spatio-temporaltrendsoflonglinefishingeffortintheSouthernOceanandimplica-tionsforseabirdbycatchBiological Conservation1141ndash27httpsdoiorg101016S0006-3207(02)00378-6

UNEP-WCMC(2016)Marine no net loss A feasibility assessment of imple-menting no net loss of biodiversity in the seaCambridgeUKUnitedNationsEnvironmentProgramme

Vaissiegravere A-C Levrel H Pioch S amp Carlier A (2014) Biodiversityoffsets for offshore wind farm projects The current situation inEurope Marine Policy 48 172ndash183 httpsdoiorg101016jmarpol201403023

Wallace B P Heppell S S Lewison R L Kelez S amp CrowderL B (2008) Impacts of fisheries bycatch on loggerhead tur-tles worldwide inferred from reproductive value analy-ses Journal of Applied Ecology 45 1076ndash1085 httpsdoiorg101111j1365-2664200801507x

Wanless R M Ryan P G Altwegg R Angel A Cooper JCuthbert R amp Hilton G M (2009) From both sides Dire de-mographic consequences of carnivorous mice and longlining for

the critically endangered Tristan albatrosses on Gough IslandBiological Conservation 142 1710ndash1718 httpsdoiorg101016jbiocon200903008

WardP LawrenceEDarbyshireRampHindmarshS (2008) Large-scale experiment shows that nylon leaders reduce shark bycatchandbenefitpelagiclonglinefishersFisheries Research90100ndash108httpsdoiorg101016jfishres200709034

WardTampPhillipsB(2010)SeafoodecolabelingInRQGraftonRHilbornDSquiresMTaitampMJWilliams(Eds)Handbook of ma-rine fisheries conservation and management (pp 608ndash617) OxfordUKOxfordUniversityPress

WilcoxCampDonlanCJ (2007)Compensatorymitigationasasolu-tion to fisheries bycatch-biodiversity conservation conflictsFrontiers in Ecology and the Environment 5 325ndash331 httpsdoiorg1018901540-9295(2007)5[325cmaast]20co2

WilcoxCampDonlanCJ (2009)NeedforaclearandfairevaluationofbiodiversityoffsetsforfisheriesbycatchConservation Biology23770ndash772httpsdoiorg101111j1523-1739200901173x

Wolf SHartlBCarrollCNeelMCampGreenwaldDN (2015)Beyond PVAWhy recovery under the Endangered Species Act ismorethanpopulationviabilityBioScience65200ndash207httpsdoiorg101093bioscibiu218

ZedlerJBampCallawayJC (1999)TrackingwetlandrestorationDomitigation sites follow desired trajectories Restoration Ecology 769ndash73httpsdoiorg101046j1526-100X199907108x

Žydelis R Wallace B P Gilman E L amp Werner T B (2009)Conservation of marine megafauna through minimization of fish-eries bycatch Conservation Biology 23 608ndash616 httpsdoiorg101111j1523-1739200901172x

How to cite this articleMilner-GullandEJGarciaSArlidgeW etalTranslatingtheterrestrialmitigationhierarchytomarinemegafaunaby-catchFish Fish 2018001ndash15 httpsdoiorg101111faf12273

Page 3: Translating the terrestrial mitigation hierarchy to marine ......of marine megafauna by-catch in fisheries, going from defining an overarching goal with an associated quantitative

emspensp emsp | emsp3MILNER- GULLAND Et AL

ThenextstepistodefineaquantitativetargetandassociatedmetricbywhichthegoalwillbemeasuredInthecaseofby-catchofmarinemegafauna one relatively intuitive approach is to de-fine the target as zero net change in population growth rate ofthe focal species caused as a result of by-catch and associatedmitigationmeasures inthecontextofalltheotherfactors influ-encingthatpopulation(aswasdoneeginthestudiesreviewedbyLewisonCrowderReadampFreeman2004)Thedownsideofthis metric is its requirement for monitoring data that can pro-vide trends in population size over time decomposed into vitalrates(survivalfecundity)sothatthecontributionofby-catchandmitigationmeasures tochange inpopulationgrowth ratecanbediscerned Thismay be challenging formanymarinemegafauna(CaswellBraultReadampSmith1998)Othermore readilymon-itored targets couldbebasedonnumbersof animals for exam-plenotexceedingaPotentialBiologicalRemoval(PBR)threshold(RichardampAbraham2013)Thedownsideofnumbers-basedmet-ricsistheirmoreindirectrelationshipwiththeconservationstatusofthespeciesconcerned

Using themetric of net change in population growth rate thebaselinefromwhichgainsandlossesfromdifferentmeasurestakentomitigateby-catchareassessedcouldbeazeropopulationgrowthratesuchthatthepopulationremainsstableatthecurrentlevel(astatic baseline) the projected population growth rate of the spe-ciesintheabsenceofby-catchwhichcouldbepositiveornegativedependingontherelativeimportanceofby-catchinthecontextofotherthreats(adynamicbaseline)oranaspirationalbaselinesuchaspopulationgrowthatXperyeartothepointatwhichitreachessomedesiredsteady-stateabundance(whichwouldneedtobedy-namicgiventhatpopulationshavedensity-dependentgrowth)Suchabaseline is therefore a typeofcounterfactual againstwhichanyimprovement or deterioration in the population of the by-caughtspeciesasaresultoftheimplementationofthemitigationhierarchy

iscompared(iewhatwouldhavehappenedintheabsenceoftheby-catchmitigationmeasures)

Next the different approaches which can be used to attainNNL(orwhatevergoal isset)areassessed intermsoftheireffectonthechosenmetricforexamplethereductioninseabirdmortal-ityfromfittingtorilinesinafisherycanbeassessedintermsofitseffectonthegrowthrateofawanderingalbatross(Diomedea exu-lansDiomedeidae)populationThefourcategoriesoftheterrestrialmitigationhierarchyareavoidanceminimizationremediation(alsoknown as restoration or rebuilding) and offsetting In the case ofmarinemegafaunaby-catchwetakeldquoavoidancerdquotorepresentmea-surestakeninordertoreducetheprobabilityofencounterbetweenpotentially harmful gear and a potentially by-caught individualby separating fishing activity from individuals or stocks of poten-tialmegafaunaby-catch species (seeTable2 for example actions)We take ldquominimizationrdquo asmeasureswhich reduce theprobabilityofcapturebythegeargiventhattheencountercannotberealisti-callyldquoavoidedrdquoThesemeasuresoccuroncethereisspatio-temporaloverlapbetweena fishingvesselandamarinemegafauna individ-ualldquoRemediationrdquoalsooccursatseabutpost-captureandaimstoreduce theprobabilityofmortality givencapture ldquoOffsettingrdquo re-ferstomeasurestocompensateforby-catchmortalitythatoperateseparatelyfromthefocalfishingactivitybutwhichtargetthesamestockoftheby-caughtspecies

Inrealitytherearegreyareasbetweeneachofthesestagesandarangeofwaysinwhichby-catchmitigationmeasurescanbecat-egorizedForexample herewe include restorationand rebuildingactivitiesat thestock level inldquooffsettingrdquobecauseourframeworkis structuredaround individual-levelcaptureprobabilityHoweveranotherapproachmightbetocombineremediationatthe individ-uallevelinacategorywithrestorationrebuildingmeasuresthatim-provepopulationviabilityatthestocklevelsuchasrestockingandhabitatimprovementleavingoffsettingasmeasureswhichbenefit

Term Explanation

Goal Thedesiredchangeinbiodiversityforexamplenonetloss(NNL)ofbiodiversityasaresultofthecombinedeffectofthedamagingaction(egby-catch)andassociatedmitigationmeasures

Target Inourframeworkwedistinguishbetweentheoverallgoalatthepolicylevel(egNNL)andthequantitativetargetwhichoperationalizesthegoalforwhichametriccanbedefined

Metric TheunitsusedtomeasuregainsandlossesinbiodiversityinordertoevaluatewhetherthegoalhasbeenachievedInourcasethisisnetchangeinpopulationgrowthrateofthefocalspeciesasaresultofby-catch+mitigationmeasures

Baseline ThereferencepointagainstwhichNNLisassessedThiscouldbestatic(egcurrentpopulationgrowthrate)dynamic(projectedpopulationgrowthrateintheabsenceofby-catchbutcontinuationofotherprocessesaffectingvitalrates)oraspirational(desiredchangeinpopulationgrowthrate)

Counterfactual Theprojectedchangeinpopulationgrowthrateinthepresenceofby-catchbutabsenceofmitigationmeasuresagainstwhichNNLisassessed(egbusinessasusual)IfthebaselineisdynamicthecounterfactualisthesameasthebaselineotherwisebotharerequiredtofullydefinethescenarioagainstwhichNNLisevaluated

TABLE 1emspExplanationoftermsusedinthemitigationhierarchy

4emsp |emsp emspensp MILNER- GULLAND Et AL

thestockmoreindirectlyoractatthebroaderspecieslevel(suchasrestoration in other locations ormeasures to improve complianceand reduce uncertainty) Howeverwe feel that the clarity of theprobabilisticapproachinourframeworkwhichextendstheclassi-ficationbyHall(1996)isparticularlyhelpful

Ourdivisionofmitigationapproachesintothesecategoriescanberepresentedinthefollowingconceptualmodelrelatingtoapar-ticularby-catchspeciesinwhichtheunitisrateofchangeinpopu-lationsizeasaresultofby-catchanditsmitigation

HereΔλT is the target levelofoverallnetdamage inflictedbyby-catchonthespeciesconcernedmeasuredintermsofchangeinpopulationgrowthratewithrespecttotheagreedbaselineAzeroΔλTimpliesthatthereductioninpopulationgrowthratecausedbyby-catch after avoidance andmitigationmeasures have been im-plementedisbalancedbythegainengenderedbyoffsetmeasuresThereisalsothepossibilityforΔλTtobenegative(thereisstilladdi-tionalpopulationdeclineasaresultofby-catchevenaftermeasurestoreduceit)orpositive(equivalenttonet gainmeaningthatspeciespopulationgrowthishigherthanitwouldotherwisehavebeenasaresultofthecombinationofmeasurestakenunderthemitigationhierarchy)

f(EBtimesBPUE)istheeffectonpopulationgrowthrateoftheby-catch-relevantcomponentoffishingeffortbrokendownintotheby-catch-relevanteffortitselfEBandtheby-catchtakenperunitof that effort BPUEwhere f() is the effect of this effort on theby-caught speciesrsquo population dynamics Thiswould generally becalculatedastheoutputofapopulationmodelAreduction inEB isequivalenttoafisheryavoidingby-catchpartiallyorcompletelyIt could include restricting the fishery to particular areas or sea-sons modification of fishing practices and operations (eg set-tingthegeardeepertoavoiddepthswhereby-caughtspeciesare

prevalent)AreductioninBPUEistheresultoftheat-seameasuresencompassed intheldquominimizerdquoandldquoremediaterdquostepsofthemiti-gationhierarchy

By-catch-relevanteffortEBisasubsetoftheoverallfishingef-fort thatoccurs in thearea inwhichthere is riskofby-catch (E)Given thecomplexitiesof estimatingEB inmanycases itwill benecessarytoapproximateitbyE(egTuckPolacheckampBulman2003) Thismay be problematic for example Baacuteez etal (2007)show that loggerhead turtle (Caretta caretta Cheloniidae) by-catchintheMediterraneanwasnotcorrelatedwithfishingeffort(measuredasnumberofhooks)by-catchwasinsteadstronglyre-lated todistance from thecoastThey suggest that thiswasnotbecauseturtleabundance isa functionofdistance (whichwouldhave impliedagradient inEB) butbecause fisherbehaviourvar-iedalthoughtheyleftinvestigationofthemechanismsforfurtherresearchBPUEisafunctionofcatchabilityoftheby-caughtspe-ciesaswellasEB forexampleWardLawrenceDarbyshireandHindmarsh(2008)carriedoutamultispeciesanalysisoftheeffectsof nylon leaders on catch rates and showed that catch reducedwithnylonforsharksbluemarlin(Makaira nigricansIstiophoridae)and snake mackerel (Gempylus serpens Gempylidae) and in-creased for bigeye tuna (Thunnus obesus Scombridae) and blackmarlin(Istiompax indicaIstiophoridae)TherelationshipsbetweenEEB andBPUEare likely tobe complex and confoundedTherehavebeen limitedexplorationsof these relationships inby-catchdatasetswhich typically suffer from low sample sizes and zero-inflationrequiringspecializedmodellingtechniques (eg thespa-tiallyexplicitBayesianhierarchicalmodelsofSimsCoxampLewison2008)By-catchmitigationmayuseasuiteofinteractingmeasuresfrom several levels of the mitigation hierarchy (Table2) whichchangeovertimeaddingfurthertothecomplexityofseparatingE EBandBPUE(asdiscussedfortargetfisherydatabyBishop2006)Wedonothereattemptfurthertoclarifytheserelationshipsbutakeyresearchneedistodisentanglethesevariablesinanempiricalsetting

(1)ΔλT= f(

EBtimesBPUE)

minusOT

Step of the hierarchy Example measures

Avoidance Excludingfishingfromtheareas(no-fishingzones)seasons(closedseasons)ortimesofdaywherethesespeciesaremostvulnerable

Minimization Usingon-vesseltechnologieswhichaimtoreducethenumberofencounteredindividualsthatarecapturedduringfishingoperationssuchastorilinesforscaringseabirdsawayfromlonglinesorsonicdevicestosignalnetstomarinemammals

Remediation Deviceswhichenableindividualstoreleasethemselvesfromthegear(selectivitygridsturtleexcluderdevices)ortobereleased(egMedinapanelsoperatedintunapurse-seinefisheriestoletdolphinsescapebeforegettingonthedeck)orreleasingthemondeckandprovidingforasafereturntothesea(egalargemeshsoftwebbingcargonetcanbeusedtoldquosieverdquoarayfromthecatchandliftitoverthesideofthevesselFrancis2014)

Offsetting Eradicatinginvasivepredatorsonislandswhereseabirdsnestrestoringhabitatrestockingwithhatchery-raisedindividualsimprovingby-catchperformanceofothergeartypesinthearea

TABLE 2emspExamplesofmeasureswhichcanbetakenundereachstepofthemitigationhierarchy

emspensp emsp | emsp5MILNER- GULLAND Et AL

OT is the net effect on population growth rate of policiesaimingtoimprovetheoverallviabilityoftheby-caughtspeciesrsquopopulation representing ldquooffsettingrdquo of the damage caused Itrepresents the expected effects of measures to improve con-ditions for individuals which would not have been at risk ofby-catch at that particular stage in their lives or location Forexample supplementation in nesting areas (for turtles) resto-rationofnestinghabitat(forseabirds)orimplementationofpro-tectedareasaimedatdemographicgroupsnotdirectlyimpactedby fishing (calving areas for cetaceans juvenile concentrationsforfish)

3emsp |emspOPER ATIONALIZING THE FR AMEWORK

In Table3we illustrate the application of the by-catchmitigationframework using four examples from different fisheries and by-catchtaxaSpecificsolutionstoEquation1couldcomefromtakingintoaccount the regulatory cultural andeconomicconditions inaparticularfisheryForinstanceoncethefocalby-catchpopulationhasbeendefinedthenitispossibletosolvetheequationbyassign-ingfactorsaffectingdecision-makingincludingcostIfaleast-costapproachtoby-catchgoalsisappropriateEBBPUEandOT could be expressedasfunctionsofcosttosolvetheequationforagivenΔλT Another approachwould be tomaximizeΔλT subject to a budgetconstraint

Table3highlightsthatthereisnotalwayspotentialforeffec-tive action at each level of the hierarchy for some species (egoceanicwhitetipslonglines)theremaybelimitedpotentialatalllevelsTheframeworkisawayoforganizingandstructuringthink-ingaboutby-catchmitigationandenablingmitigationeffective-nesstobeassessedagainstaconcretelydefinedandmeasurabletargetItsfunctionisnottoproposenewwaysofdoingby-catchmitigationforcasesliketheseIfonusingtheframeworktoanal-yse the effectiveness of the measures available for a given by-caughtstockitisfoundthatitisnotpossibletoreachthechosentarget(egNNL)thendifficultdecisionsmustbemadeForexam-plethetargetmayneedtochangewhichcouldimplyanaccep-tanceofcontinuingdeclineoftheby-caughtstockOrthefisherymustbe restructured in away that reducesby-catcheffectively(maybeevencloseddown)Orinvestmentmustbemadeintotech-nological innovation todevelopnewways to reduceby-catch Ifitisfoundthatthedataareinadequatefortheanalysisrequiredthenthedecisionmustbemadeeithertoinvestinimprovingtheevidencebaseor to recognize that it is not possible to evaluatewhether by-catch mitigation has been effective in reaching theagreed goal The frameworkrsquosmain utility therefore is tomakethesechoicesexplicit

Equation1couldbeextendedtohandlemultiplespeciesvary-inggeartypesorheterogeneousby-catchreductionmethodsForinstanceBPUEcanbedecomposedintoseveralcomponentsrepre-sentingthedifferentstagesoftheprocessIfBPUErepresentsthesumofindividualsdeadonarrivalindividualscapturedanddyingon

thevessel and individualsdyingafter live releasewecan rewriteBPUEasaseriesoffactors

whereBDOAistheby-catchperuniteffortthatarrivestotheboatdeadBOBistheby-catchperuniteffortthatarrivestothevesselalivePDVistheproportiondyingonthevesselandPDRisthepro-portiondying after release For instance a higherproportionofby-catchofseaturtlesandotherspeciesarrivestotheboatdeadwhenusinglonglinesthataresetdeepsuchasthoseusedforbig-eyetunathatcanbesetmorethan300mdeepwhencomparedto a shallow set longline such as those used inmany nearshoreartisanal fisheries (Andrakaetal2013HallSwimmerampParga2012Swimmeretal2006)ThisdifferencewouldappearintheBDOA termSuchadecomposition illustratestheflexibilityofthisframeworkinhandlingfishery-andspecies-specificfeaturesandalsoservestohighlightareaswheredifferentmitigationmethodswouldhavethegreatestinfluence(egShiodeHuShigaYokotaampTokai2005)Anotherextensiontothebasicframeworkwouldbetoconsiderexplicitlytheuncertaintysurroundingdifferentel-ements of the conceptual model and the impact of this uncer-taintyonwhichelementofby-catchmitigationshouldbeafocus(Table3)

It is important tonote that this equation isnot a truebioeco-nomicequationtobesolvedRatheritisaconceptualframeworkinwhichwemakethecomponentsofthemitigationhierarchyexplicitinordertoguidethinkingtowardsamoreholisticapproachtoad-dressingby-catchItalsodoesnotrepresentahierarchysuchasisrequiredinterrestrialsystemsTomakethisequationintoahierar-chyratherthanamodelforleast-costmitigationofby-catchitcouldbesetupasagoalprogrammingfunctionwithsequentialsolutionstoeachelementsummedtoproducethefinalmitigationoutcomeInoperationaltermsthistranslatesintoapresumptionthatinvestmentandeffortshouldbefocusseddifferentiallyonsequentialelementsofthemodelstartingwithEBthenBPUEthenOTsothatoffsettingrelatesonly to theunavoidable residualharmonceall other stepshavebeentakenThismaybereflected intheemphasisplacedontheincentivesgiventofisherstochangebehaviourpertainingtose-quentialelementsofthehierarchyinthetimingoftheoffsetorinthedispositionofthefundingforresearchandconservationactionallocatedbygovernment

ResearchiscurrentlyongoingtooperationalizeEquation1tore-duceturtleby-catchofasmall-scalegillnetfisheryoperatingoutofSanJoseportPeru(Alfaro-Shiguetoetal2010)Currentlyasmall-scalecertificationschemeisundertrialbytheNGOProDelphinuswhich aims to give premium prices for fish caught by skippersabiding by best-practice by-catch reduction guidelines (J Alfaro-Shigueto and J Mangel personal communication) The researchentailscollectingdetailedeconomicdatafromallgillnetvesselstounderstand the economic costs involved in fishing operations tocalculatethepotentialadditionalcostsofmeasuresateachstagein

(2)BPUE=BDOA+PDVtimesBOB+(

1minusPDV)

timesBOBtimesPDR

6emsp |emsp emspensp MILNER- GULLAND Et AL

TABLE 3emspSummaryofoptionsforby-catchmitigationstructuredaccordingtothemitigationhierarchyforfourcase-studies

Fram

ewor

k st

ep

Cas

e- st

udy

Alb

atro

sses

lon

glin

esTu

rtle

slo

nglin

esRa

ysp

urse

sei

nes

Oce

anic

whi

tetip

slo

nglin

es

Definingtheproblem

Fisheryandspatial

extent

Braziliandomesticindustrialcoastallongline

fleet

EasternPacific(coastalandpelagic)

small-scalecommerciallonglinefishery

Tunapurse-seinefisheryof

theeasternPacific

AsianandEUlonglinetunafisheriesinthe

Indi

an o

cean

Targetspecies

Variousspeciesofsharkandswordfish

Mahi-mahi(

Cory

phae

na h

ippu

rus

Coryphaenidaeseasonal)tunasharks

(mostlysilkyC

arch

arhi

nus f

alci

form

is

Carcharinidae)billfish

Variousspeciesoftuna

Variousspeciesoftuna

By-catchspeciesof

conc

ern

Albatrossamppetrelspeciesparticularconcern

forcriticallyendangeredTristanalbatross

(Dio

med

ea d

aben

nenaDiomedeidae)

Oliveridley(L

epid

oche

lys o

livac

ea

Cheloniidae)greenblack(C

helo

nia

myd

asCheloniidae)hawksbill

(Ere

tmoc

hely

s im

bric

ataCheloniidae)

loggerhead(PeruandMexico)and

leatherback(D

erm

oche

lys c

oria

cea

Cheloniidae)

Sevenmobulidspecies

includingCITES-listedM

anta

bi

rost

ris(Mobulidae)and

M a

lfred

i(Mobulidae)

caughtmostlyalivein

dolphin-associatedor

free-schoolsets

OceanicwhitetipsharkVulnerableonIUCN

redlistretentionbannedbytunaRFMOs

listedonCITESAppendixII

By-catchtarget

(Δλ T)

BraziliangovernmentMinimizeby-catch

Rulesfocusontargetsforuseofminimizing

measuresratherthanonby-catchnumbers

NotwelldefinedRFMOssuggest

minimizingby-catchCouldconsiderPBR

foroliveridleyszerocatchforleather-

backs(reflectingtheirrespective

populationstatus)

IATTC(2015)zeroretention

storingorsellingandlive

releaseofby-caughtrays

whenpossibleImplies

by-catchminimization

Targetby-catchlevelnotdefineddueto

uncertaintyRFMOsbanretentionlanding

andtrans-shipment

Mitigationhierarchyelement

Avoid

[timeareaclosuresnight-timesetting]

[timeareaclosuresdeeperlines]

[timeareaclosures]

[deepsetting]

Minimize

[torilineslineweights]

[monofilamentlinecirclehooks(not

leatherbacks)]

ndash [hardtoavoidcatching]

[monofilamentlinecirclehooksbanon

steelleaders]

Remediate

ndash [hardtoreleasealive]

[improvedhandling]

[improvedhandling]

[shortsets]

Offset

[invasiveeradication]

[beachprotection]

[illegaltrade]

[informationgatheringillegaltrade]

Factorsaffectingoperationalization

Scopefor

incentives

Participatoryresearchonbarrierstouptakeof

minimizationmeasuresPositiveincentives

forthoseusingnewmeasurespaidforby

forexamplefisheries-widelevy

Certificationsustainabilitystandardsin

exportmarkets

Transitionalpaymentsto

promotebetterhandlingon

deckhenceimproving

survival

Ifinformationgatheringseenasavalidoffset

duetohighuncertaintyfundingatagging

schemecouldincentivizefisherstocollect

dataonsharkcatchratesurvivalof

releasedsharksby-catchhotspotsto

supportimprovementsacrossthewhole

mitigationframework

(Continues)

emspensp emsp | emsp7MILNER- GULLAND Et AL

themitigationhierarchy In theabsenceofhighqualitypopulationdatawithwhichtoparameterizeamodelaPBR-basedapproachisbeingusedtosetatargetby-catchlevel intermsofnumberof in-dividualsofeachoftheturtlespeciescaughtinthefisheryExpertopinionfromfishersandProdelphinusstaffsupplementedbydatafromalong-runningby-catchobserverprogrammeoperatingoutoftheport(Alfaro-Shiguetoetal2011)givesthepotentialreductioninturtleby-catchnumbersasaresultofagivenmitigationapproachInterviews and focus groups with fishers provide understandingof their preferences for different by-catchmitigation approachesbarriers and constraints to implementation and potential partici-pationindifferentincentiveschemesthiscanbesupplementedbyDiscreteChoiceExperimentsprovidingempiricalestimatesforpref-erencesforcombinationsofby-catchreductionmeasures(cfRogers2013)Thisfieldresearchproducesashort-listoffeasiblemitigationmeasuresateachstageinthemitigationhierarchyforcostingandtesting(egspecificareasortimesforfisheryclosureunderavoid-ancecombinationsofhooktypesandnetmodificationundermini-mizationtraininginturtlehandlingandreleaseforremediationandimprovingby-catchperformanceofothergeartypesintheareaforoffsetting)Thisenablestheanalysisoftheeffectivenessandcostof various combinations of by-catch reduction strategies framedwithinthefourstepsofthemitigationhierarchy(avoidminimizere-mediateoffset)withacleartargetby-catchreductiongoalinmind

4emsp |emspCOMPARING KE Y DEBATES BET WEEN TERRESTRIAL NNL AND BY- C ATCH MITIGATION

41emsp|emspThe hierarchical nature of mitigation

Terrestrial situationsareusuallyviewedas requiringastricthierar-chywithavoidanceminimizationandremediationtakingprecedenceoveroffsetsPartofthereasonforthishierarchymaybesocietalval-uesandexpectationsbut also it is a reflectionof reversibility anduncertaintyTheterrestrialmitigationhierarchywassetuptoaddresshabitatdestructioncausedbydevelopmentwhich iseffectively ir-reversiblehenceavoidanceisstrictlypreferredfromaconservationperspective Inpractice avoidancehasbeenaneglected step andmuchofthedisquietaboutbiodiversityoffsettinghasbeenbecauseofthetendencytopaylipservicetoavoidanceandfocusinsteadonoffsetswhich thenmay be implemented on paper only (HoughampRobertson2009Phalanetal2017)EvenwithperfectenforcementandcompliancewithmeasuresfurtherdownthemitigationhierarchythestrictavoidanceofhabitatlossismorecertaintolimitimpactthanreducinglossesinthecourseofapotentiallydamagingactionwhichismorecertainthanrestoringdamageafterthefactorcompensatingforitwithactionselsewhereOfteninterrestrialsystemsmultipliersareusedattheoffsetstagetoreflectthisuncertaintyrequiringthatanadditionalamountofequivalentlandisprotectedinanoffsetoverandabovetheamountthatislostduringthedevelopment(withtheratiooflandoffsettolanddestroyedinthe10sto100sdependingonthecircumstancesMoilanenVanTeeffelenBen-HaimampFerrierFr

amew

ork

step

Cas

e- st

udy

Alb

atro

sses

lon

glin

esTu

rtle

slo

nglin

esRa

ysp

urse

sei

nes

Oce

anic

whi

tetip

slo

nglin

es

Major

uncertainties

Lackofspecies-levelidentificationof

by-catchlackofunderstandingof

compliance

Lackofecologicalknowledgeofturtle

populationtrendsampdistribution

Potentialforsignificantadditional

by-catchfromcoastalgillnetfishery

Impactofcatchonmobulid

survivalPredictorsof

mobuliddistributions

Lackofobserversorreportingsoverylimited

understandingofby-catchlevelsspatio-

temporalencounterhotspotspost-release

survivalcompliance

Keyobstacle

Compliancewithexistingrulesmustbe

improved

Fundingforalternativestofishingata

largeenoughscaleLongtimelagand

uncertaintyinoffseteffectiveness

Limitedknowledgeofmobulid

distributionsmakes

avoidancedifficult

Lackofmonitoringlimitsoptions

Overallassessment

Existingmeasuresforimprovingimplementa-

tionofminimizationstepalreadyexistbut

needincentivizingoffsettingcouldprovide

short-termgainstocomplementthese

Targetedfundingcouldfacilitateimprove-

mentsthroughoutthehierarchyBest

approachmaydifferbyspecies(particu-

larlyleatherbacksvsothers)

Focusonremediationstepis

currentlythemainoption

avai

labl

e

Somepotentialforminimizationthrough

deepsettingbutchallengingtochange

behaviourinthisfisheryelectronic

monitoringsystemswouldhelp

Keyreferences

BugoniManciniMonteiroNascimentoamp

Neves(2008)Wanlessetal(2009)

Alfaro-ShiguetoDuttonampMangel(2007)

Halletal(2012)Andrakaetal(2013)

JonesampFrancis(2012)Hallamp

Roman(2013)Crolletal

(2016)Fowler(2016)

Tolottietal(2015)

Ticksindicatethepotentialforactionatdifferentstepsofthehierarchybasedonfeasibilitycurrentknowledgeandimpactonmortality(

=highpotential

=somepotential

=limitedpotential

ndash=nopotential)TextinbracketsgivessuggestedmeasuresateachlevelofthehierarchytheseareillustrativeratherthandefinitiveTheinformationforthecase-studiesisbasedontheexpertknowledge

oftheauthorsthroughtheirinvolvementinmanagementoftheby-catchissueinthesefisheriesRFMOregionalfisheriesmanagementorganizationPBRpotentialbiologicalremoval

TABLE 3emsp(Continued)

8emsp |emsp emspensp MILNER- GULLAND Et AL

2009)Bycontrastinfisheriessettingstherehavebeensuggestionsthatdependingonthelegalenvironmentitmaybemoreappropriateforoffsetstobeusedaspartofaleast-costconservationapproachalongsidemoretraditionalmitigationmethodsratherthanasthelaststep inamitigationhierarchy (DuttonJosephSquiresampWilliams2011DuttonampSquires2008WilcoxampDonlan2007)

42emsp|emspOut- of- kind offsets

Out-of-kind offsets are those which do not act to increase theimpact-affectedbiodiversityIntermsofourconceptualframeworktheyareoffsetswhichdonotacttoincreasethepopulationgrowthrateoftheby-catch-affectedfocalpopulation(Equation1)Forex-ampleonesuggestedbenefitof raising funds foroffsetting fromaby-catchtaxonfishersisthattheproceedsfromsuchataxcanfinanceoffsetselsewherewithintherangeoftheby-catch-affectedpopulation (Dutton amp Squires 2008) Although not a true offsetunderamitigationhierarchyfundsfromtheCaliforniadriftgillnetindustry in 2002 financed sea turtle nesting site conservation inBajaCaliforniaforcompensatorymitigationofseaturtleby-catch(Jannise Squires Seminoff amp Dutton 2010) In terrestrial (andmarine)systems itcanbemorechallengingtodefinethe impact-affected biodiversity because impact is rarely as clearly linkedtoagivenspeciesandstockas it is forby-catchBecauseofthisthelocationandbiodiversitytargetofconservationactionsfallingundertheldquooffsetrdquoheadinghassometimesbeenlooselyrelatedtotheactual impactBest-practicestandardsstatethatoffsetsmustbeimplementedasclosetothedamagingactivitiesaspossibleandfocusonbiodiversityassimilaraspossibletothatwhichhasbeenimpacted (BBOP 2012) However there have also been calls forldquoout-of-kindrdquooffsetsthatgivemoreconservationbang-for-buckbyfocussingonthreatenedspeciesorrarehabitatsorareasinneedofconservation rather than the impactedareasor specieswhichmay be considered less ldquovaluablerdquo for conservation (Bull Hardyetal2015)Thishasledtosubstantialdebateastotheappropri-atelimitsonthegeographicscaleandbiodiversityfocusforoffset-ting(egApostolopoulouampAdams2017)Italsodrawsattentiontothesubjectiveanduser-definednatureof theword ldquobiodiversityrdquo(Morar ToadvineampBohannan 2015) As it is impossible fully tooperationalizetheconceptimplementersofthemitigationhierar-chyhavelatitudetointerpretbiodiversityaccordingtoforexampleeaseofmeasurement perceived societal valueormitigation cost(Maron etal 2016) In our casewe take a narrow focus on theby-caughtspecies itself this is in linewithmuchof the literatureon by-catch but notwith the broader discourses on ecosystem-basedapproachestomarinemanagementandecosystemservices(RosenbergampMcLeod2005)Thesediscoursessuggest theneedforamorefunctionalecosystem-basedapproachtononetlossofbiodiversitythishasyettotranspireeitherinthemarineorintheterrestrialliteraturepossiblybecausesubstantialchallengesinde-finingimpact-affectedbiodiversitytheninevitablyensue

Asmarinemegafauna stocks are often transboundary andmi-gratorydefiningtheappropriatespatialunit foroffsettingmaybe

achallengebecause themosteffective location foranoffsetmayormaynotbewithintheareaofinfluenceofagivenfisheryClearlyandpreciselydefining the spatial unitwithinwhich themitigationhierarchywill be implemented during theprocess of defining theoverallgoal(suchasNNL)isvitalThisunitshouldreflectthescaleoverwhichanactionwillaffectλToffsetswhicharewithinthedis-tributionofthefocalstockoftheby-caughtspecies(asdefinedforEquation1)arenotout-of-kindHoweverchallengesemergewhenthe appropriate spatial unit for offsetting activities is different totheappropriatespatialunitforotherelementsofthemitigationhi-erarchywhicharelikelytobedefinedinsteadbyjurisdictionalareaor target fish stock distribution Inmany fisheries the species af-fectedbyby-catchmaynotbewellenoughknownandoffsetsmayaccordinglyneedtobebroadlytargetedtobenefitanypotentiallyaffectedspeciesTrueout-of-kindoffsetswouldincludefundingtheconservationofunaffectedspeciesorstocksofhabitatsnotusedbythefocalstockorcontributionstoaconservationfundwithoutaclearcommitmentthatthefundsaretobespentonincreasingλT for thefocalby-caughtstockTheseareunlikelytoformpartofbest-practiceguidanceforby-catchoffsets

43emsp|emspResearch as an offset

Arelatedareaofactivecontroversyformarineby-catchiswhetherresearchor informationgatheringshouldbeseenasavalidoffsetmechanism The rationale is that this research could be used toreduceuncertaintypromote innovationand thereby improveout-comes for by-caught species albeit indirectly An offset could beusedto incentivizebetterdatacollectionfor instanceusingaby-catchlevytopayfortaggingortoputby-catchobserversorelec-tronicmonitoringsystemsonboatsThismightbeapreludetolatermitigation or avoidance activities once more is known about thebiological settingWhether research activities could appropriatelybeconsideredaspartofanldquooffsetrdquoiscontroversialmdashinsomecasesan indirectbenefit to theby-caught stockmightbe clearly appar-ent(egtheoceanicwhitetip(Carcharinus longimanusCarcharinidae)case-studyinTable3)whileinothercasesusinginvestmentinre-searchasanoffsetcouldbeseenasacaseofmoralhazardpoten-tially compromising scientistsrsquo independence and having at best ahighlyindirectrelationshiptoNNLoftheby-caughtspeciesAnotherviewisthatreducinguncertaintyisacoreresponsibilityofoperatingafisherywhichthereforeshouldbebornebythemanagementau-thorityorfishingbusinessesInterrestrialsystemsthesedilemmasalsoexistbutthesentimentismuchmoreclearlyexpressedthatre-searchactivitiesarenotappropriateoffsets(BullGordonWatsonampMaron2016)

44emsp|emspIncentivizing implementation of mitigation measures

Thefactorsthatdrivedecision-makingaboutmegafaunaby-catchreduction (by skippers companies fishery managers policymak-ers and other stakeholders) include legal obligations tominimize

emspensp emsp | emsp9MILNER- GULLAND Et AL

by-catch at the national or international levels (eg FAO 2011Rice 2014) the availability and quality of technical fixes associ-atedcosts tofishers limitsonaccesstoseafoodmarketsaswellassocietalpressuresHowevermuchresearchonby-catchreduc-tion focuses on identifying and implementing technicalmeasuresto reduceBPUE rather thanon the social andeconomicbarriersto implementation (Campbell amp Cornwell 2008) Technologicalinnovation to improve BPUE needs to be appropriately incentiv-izedwitheffortsmadetoensurethatsuchmeasuresareascost-effective as possible for fishers (Gjertsen Hall amp Squires 2010Lent amp Squires 2017) However it often happens that even ap-parently suitable by-catchmeasures are notwidely implemented(eg Damalas amp Vassilopoulou 2013 Orphanides amp Palka 2013RadzioSmolinskyampRoosenburg2013)Inthesecasesthedegreeofnon-implementationandthereasonsbehinditneedstobeun-derstoodsoitcanbeaddressed(Coxetal2007)Thesetypesofconsiderationarealsonotwellresearchedintheterrestrialoffset-tingliteraturebecausecomplianceispoorlymonitored(BullSuttleGordonSinghampMilner-Gulland2013)andthereislittlesupportfor researchon thebarriers to implementationofamitigationhi-erarchyandhowtosupportdeveloperstoaddressthesebarriers(BullBryantBakerampMilner-Gulland2015)Thesocialimpactsofimplementingabiodiversitymitigationhierarchyonresourceusersarementioned inguidance (egBBOP2012)buthowtomeasureandaccountforthemisverypoorlyunderstoodThefewstudiesin-vestigatingdeliveryofpromisedoffsetmeasuresinterrestrialsys-temssuggestaverypoorrecord(QueacutetierRegneryampLevrel2014)Therefore the social side of implementing the mitigation hierar-chyand incentivizingcompliance isanarea thatneedsmore andmoreactiveresearchwithinboththeterrestrialandmarinerealms(FultonSmithSmithampvanPutten2011)Thisisparticularlytruewhentheburdenof implementingmitigationapproaches isbornebyrelativelysmall-scaleproducersratherthangovernmentsormul-tinationals(egthepelagiclonglinefisheriesinTable3)

45emsp|emspSocietal limits

Foraspeciesathighriskofextinctioncompleteavoidanceofby-catchmightbethemostdesirablepolicyfrombothamanagementagency and societal perspective In addition with emblematic orhighlythreatenedmarinemegafaunaitmaybeviewedbymembersof the public asmorallywrong to kill any individuals even ifmiti-gationisinplace(egMauirsquosdolphinHamneretal2014) leadingtopressureongovernmentstoreflectthisethicalconcerninregu-lationsThesedilemmasecho the issueof thresholds in terrestrialoffsetswhichrecognizesthattherearesomecriticalareasinwhichdevelopmentisnotsocietallyappropriateregardlessofthepoten-tialformitigationandotherareasinwhichthemitigationhierarchycan be appropriately applied (Bull etal 2013) Examples of loca-tionswhereathresholdapproach isseenasappropriate interres-trial systems include the habitat of highly endangered species orecosystemswhich are limited in extent and irreplaceable (such asoldgrowthforest) In terrestrialsystems therefore themitigation

hierarchyisseenasmostappropriateforapplicationinmorecom-monanddegradedhabitatssuchasfarmlandSimilarlyinfisheriestheremaybesomesituationsinwhichthestockssubjecttoby-catchare so precious or threatened that no level of threat from fishingcanbecontemplatedandotherswherefishingsubjecttoNNLandthemitigationhierarchyisasociallyacceptableapproachInsitua-tions inwhich trade-offs between conservation and developmentareseenasnecessaryoracceptablebywidersocietyasociallicencetooperatemaybegainedthroughadoptingoffsetsintheabsenceofregulationForexampleinsub-SaharanAfricaseverallargedevel-opmentprojectsareattemptingtooffsettheirimpactsongreatapesandtheirhabitats(Kormosetal2014)Aby-catchequivalentmightbe fishing companies voluntarily donating funds for turtle nestingbeachrestorationintheirareaofoperationinadditiontocomply-ingwithregulatoryby-catchmitigationmeasuresThesemeasuresmayimprovetheimageofthecompanywiththegeneralpublicbuttoavoidaccusationsofldquogreenwashingrdquotheireffectivenessneedstobeproperlyscrutinized(Bulletal2016)Transparentlyembeddingthesetypesofactionswithinamitigationhierarchysuchasweareproposing and critically evaluating their contribution to increasingthepopulationgrowthrate(asperEquation1)wouldbeonewaytopromptsuchscrutiny

46emsp|emspUncertainty

The nature of the uncertainties surrounding biology and enforce-ment in themarine setting raisesquestions about theorderingofsteps in themitigationhierarchy inaway that isdissimilar to ter-restrialsystemswherethehierarchyofuncertaintiesmaybecleareranduncertaintyisgenerallylowerForexampleitmaybethattheimpactonoverallpopulationgrowthrateofanoffsetmeasurelikeeradicating invasivespecies fromaseabirdnestinghabitat isbothless uncertain and more cost-effective than avoidance measuressuchasclosingareaswhichmayormaynotbefrequentedbyadultseabirds in a given time-periodGenerally though itmightbe as-sumedthatmeasureswhichtargetlifestagessubjecttohighlevelsofnaturalmortalityorwithinwhichindividualcontributiontoover-allpopulationgrowthrateislow(egheadstartingjuvenileturtles)maybelesseffectiveinachievingNNLthanmeasureswhichtargetreproductivelymatureadultfemales(suchaslivereleasesHeppellCrowderampCrouse1996)Howeverbeforeimplementinganoffsetthataimstoimprovethesurvivalofonelifestageinordertocom-pensatefortheby-catchmortalityofanotherarobustassessmentoftheconsequences(withassociateduncertainties)shouldbecar-ried out through detailed population modelling based on strongempiricalstudies(cfWallaceHeppellLewisonKelezampCrowder2008)Interrestrialsystemstherequirementsequentiallytoapplythemitigationhierarchyisbroadlyunchallengedbutactuallysimilararguments apply For example habitat restoration sits above off-settinginthehierarchyandyetitisalong-termuncertainprocesswhichmayinsomecircumstancesbemuchlesspreferabletoanoff-setusingawell-establishedapproachwhichishighlylikelytoleadtoconservationgains

10emsp |emsp emspensp MILNER- GULLAND Et AL

47emsp|emspTemporal considerations

Thetimingofoffsetsinrelationtootherelementsofthemitigationhierarchyhasbeenthesubjectofdebatewithintheterrestriallitera-tureThemainsuggestionforaddressingthetemporarylossofbio-diversitywhileoffsetscometofruitionhasbeenadoptingmitigationbankingwherebyoffsetsareimplementedinadvanceofpotentiallydamagingactivitiesprovidingbiodiversitycreditswhichcanbeusedtocompensateforlaterlossesThisbothremovesanelementofun-certaintyfromtheoffsetimplementationandreducesthetimelagbetweenlossandgain(Mann2015)Withrespecttomarinemega-faunaby-catchflexibilityintimingprovidesadditionalscopeforcostreduction and benefit enhancementwhichmay not be present intraditionalhabitat-basedterrestrialoffsetsForexampletemporarymeasuressuchasashort-termby-catchtaxtofundanoffsetmaybeusedifmitigationoravoidancemethodstaketimetocomeonlineorifatemporarynudgeisenoughtocausebehaviouralchangeThismightbethecaseifapolicywasneededtoinducefisherstotakeupnewgeartoavoidthecostofanoffsetorifconcernsaboutsafetyoryieldreductionsduringthetransitiontonewgearcouldbeallayedbyatemporarysubsidyforearlyadoptersorapaidparticipatorymoni-toringprogrammeto informwider implementation(egthemobu-lidandsharkcase-studiesinTable3)Justasforhabitatrestoration(ZedlerampCallaway 1999) by-catchoffset strategieswhich targetjuvenilestagesof long-livedspecies (eg turtleheadstartingor in-vasive removal fromseabirdnesting islands)may takemanyyearsfor their effects to become apparent in an increase in populationgrowthratesAdditionaluncertaintyisintroducedbythedifficultyinmonitoringpopulationsofmanyby-catch species (eg seabirdsHatch2003)leadingtouncertainestimatesoftheimpactofoffsetactivitiesonpopulationgrowth(seecase-studiesinTable3)Theseproblemsarenot insuperablehoweverpositivetrendshavebeenreportedinturtlepopulationsoverdecadesasaresultofnestpro-tection(egDuttonDuttonChaloupkaampBoulon2005)

5emsp |emspUSING INCENTIVES TO REDUCE BY- C ATCH

Manyoftheexamplesandprinciplesdiscussedaboveeitherimplic-itlyorexplicitlyrelatetotheeconomicsocialinstitutionalormoralincentivesoperatingondifferentactorsinsideandoutsidethefish-erywhichcanbepositiveornegativeWenowturntoadiscussionofhowincentivescanbeusedtoreduceby-catchwithinourframe-workIncentivescanbeputinplacetochangefisherbehaviourwithrespecttoanyoftheelementsoftheframework (avoidminimizeremediateandoffsetTable3)Althoughdiscussedintheliteraturemostof these incentive approaches are yet tobe implemented inthe realworldparticularly forby-catchThereforeuntil empiricalevidenceoftheireffectivenessisavailablethesesuggestionscomewithacaveat

Financial costsofby-catchmitigationactions canarise for in-stancefromlostcatchcapitalinvestmentsinnewgearormitigation

equipmentor the lossofaccesstoafisheryCostsmayalsoarisefromthedeploymentofby-catchobserversortrainingintheuseofnewgearThesecostscanbepaidbyfishingcompaniesorindivid-ualsorbygovernmentsNGOsorseafoodconsumersWhetherornotcompensationforcostsincurredbyfishersisseenasappropri-atedependsonwhetherby-catchreductionisseenasasocialgoodthatfishersareproviding(inwhichcasetheyshouldbecompensatedforit)orasputtingrighttheharmthattheyaredoingtobiodiver-sitywhilegeneratingtheirownprivategain(ineconomiclanguagewhetherby-catchisviewedasanunpricedexternalityinwhichcasetheyshouldpay)Italsodependsonwhethereconomichardshipwillensueacaseforcompensationofby-catchreductioncostsincurredbypeopledependenton fishing for their livelihoodsmaybemoresympatheticallyreceivedbyotheractorsthanacasemadebyalargemultinationalfishingcompany

Ifby-catchisseenasanunpricedexternalityitmightbesociallyoptimaltotaxfishersfortheirby-catchsothatthisexternalityisin-ternalizedThisplacesanexplicitpriceuponby-catch(Boyce1996Pascoeetal2010SquiresampGarcia2014)Theby-catchprice islikely to be incorporated into the price of the target species andtherebybecomespartofthetargetspeciescostThispricecouldbeset differently for different demographic classesof theby-caughtspecies depending on the impact the loss of an individualwouldhaveonthepopulationAllelsebeingequalputtingapriceonby-catchmeans that theseafoodproduct that is the targetcatchbe-comesmoreexpensiveandconsumershave topaymore for theirseafoodreducingdemandTheninprincipleeveryfirminthesup-plychaineveryvesselandeveryconsumerhaveanincentivetore-duceby-catchuntileacheconomicactorrsquosmarginalcostofby-catchreductionequals thecommonpriceofby-catch that theyall faceOffsetsareonewaytopriceandinternalizetheby-catchexternalitycostIfanoffsettingactioniscostlytoimplementandmustbepaidforwith each unit of by-catch it implicitly prices the residual by-catch In this circumstance the effect from a financial standpointisthesameasaby-catchtaxwiththe levelsetbasedonthecostoftheoffsetVariousinstitutionalstructurestosupportthischargeperunitofby-catcharepossiblewithdifferentimplicationsintermsofthedistributionofcostsandbenefitsForexampleaninsuranceschemecouldbepaidintobyfishersthatpaysoutintheeventofaby-catcheventtherebyspreadingthecostofunavoidablerareby-catcheventsOratradablepermitschemecouldoperatesuchthatfisherswhoexperienceaby-catcheventcanbuyapermitwiththecostvaryingdependingondemandforpermits (henceprovidingavessel-levelincentivetoinnovatetoreduceby-catch)

If there isdemandforconservation inan internationalmarketthen price premiums and market access (through eco-labellingsupply chain certification other food sustainability campaignsWardampPhillips2010)orboycottsactingasstrategicthreatsfromconsumers (Kotchen 2013 Segerson 2010) could act as positiveornegativeeconomic leversonthe fisheryprovidingan incentivefor fishers to reduce their by-catch voluntarily (as has been sug-gested for the Brazilianmahi-mahi fishery Table3) For exampletheMarine StewardshipCouncil now includesby-catchmitigation

emspensp emsp | emsp11MILNER- GULLAND Et AL

intheircertificationprocess(MSC2014)Demand-ledleversmaybemoreorlessapplicableatdifferentlevelsinthehierarchyforexam-pleavoidancemayberelativelyhardtoevidencewhileoffsettingmaybelesseasytoselltoaconsumerthanminimizationorreme-diationConcerns about the unintended consequences of positiveincentives (particularlyfordirectsubsidiesratherthanconditionalincentives)maydeterminewhethertheyareanappropriateinstru-mentinagivencaseForexampletheymaybeinappropriateifthereisariskthattheadditionalmoneyisreinvestedinincreasedfishingcapacityor iftheremaybeconsumptionproductionorconserva-tionleakages(transferoftheproblemsomewhereelse)whetheratthe vessel fishery or trans-national levelHigh transactions costsmayalsolimitthebenefitsofincentivesschemes

Otherchangeswhichmayneedtobeincentivizedforsuccessfulimplementationofby-catchreductionpoliciesmaybelessamenabletofinancialmeasuresatleastpartlybecauseitislessclearhowtoassign financial value to theactionsor to thebenefits and losseswhichtheyproduceForexampleperceivedreductionsinsafetyforfishingcrews(fromweightedlonglinesfor instance)arecoststhatmaybehardtovaluefinanciallyOtherprerequisitesfor long-termsustainable behaviour change such as changes in social norms sothatfishingcommunitiesseeby-catchreductionasappropriatebe-haviourortechnicalskillacquisitionsothattheycanusenewmeth-odsmaybeincentivizedbycarefullydesignedinterventionsworkingwithfishers(Halletal2007)Conservationpoliciesbasedoneco-nomic incentives (extrinsicmotivation) are not always superior tothosebasedupon intrinsicmotivation Infact incentive-basedby-catch reduction policy instruments could even be counterproduc-tivebyreducingtheeffectivenessofintrinsicmotivationdependingupon the situation (although the empirical evidence on this topicisweak RodeGoacutemez-BaggethunampKrause 2015) If the changerequiredforby-catchreductiontoworkmeetscultural resistancethenparticipatory researchmightbeespeciallyeffective inbreak-ingdownbarriersbetweenthosewhowantby-catchreductiontotakeplaceandthosewhoactuallyhavetoimplementit(thefishers)ForexampleinAustraliathegovernment-fundedbodyOceanwatchfacilitatesengagementbetweencommunities thefishing industryseafood suppliers and government to improve knowledge sharing(wwwoceanwatchorgau)Innovationiscrucialinfisheriesandfish-ersareaccustomedtoadoptingnewtechnologyorprocessespo-tentiallymakingan incentivizedparticipatory researchprogrammeespeciallyfruitful

Sometimes the most efficient way to solve problems is a so-cial instrumentoran institutionalchange inplaceoforaswellasan economic instrument For example supporting developmentof fisherorganizations rather than instituting a vessel-level taxorsubsidy might provide the impetus needed to change behaviourInstitutingcatchshares(individualtransferablequotas)mayprovideanenablingenvironmentforby-catchreductionforexamplebypro-motingmoreeffectivemonitoring(Grimmetal2012)Experiencein terrestrial system produces similar insights incentive-basedschemeswhichalsobuildcommunitycohesionandsupportthede-velopment or strengthening of localmanagement institutions are

more effective in the longer run than direct economic incentives(Clementsetal2010)

6emsp |emspCONCLUSIONS

The framework we present here is novel It draws upon and ex-tends the frameworks for conceptualizing by-catch developed byHall (1996) and Hall Alverson andMetuzals (2000) It amalgam-atesHallrsquos frameworkwith themitigationhierarchyasused in theEnvironmental Impact Assessment literature (BBOP 2012) Thesuggestions about goals metric andmitigation actions are drawnfromtheempiricalby-catchliteratureandtheissueswediscussin-tegratetheconcernsoftheextensiveterrestrialandnascentmarineoffsetting literature with the by-catch literature The frameworkmakesclear thatanearlycrucial step is toclarify thegoalofanyby-catch reduction policyOverarching goals like those issued bytheConventiononBiologicalDiversity(egAichiTarget11that10ofmarinehabitatshouldbeunderprotectionby2020)needtobetranslatedintooperationaltermswithineachfisheryCurrentlyleg-islatedoragreedby-catch reductiongoals tend tobe less specificthantheycouldbeandthisleadstoproblemsininterpretingthesegoals inordertoplanaby-catchmitigationstrategy(seethecase-studies inTable3 for examples) This ambiguity is tobe expectedwithinnegotiatedtargetsbutitisachallengenonetheless(Maxwelletal2015)Usingacommonunitofby-catch impactsuchastheΔλTwhichweuseherewouldbehelpfulbothinclarifyingexpecta-tionsandevaluatingtheeffectivenessofelementsofthemitigationhierarchy

Once the by-catch goal is known options for implementingavoidanceminimizationremediationandoffsetscanbeclarified(asinTable2)Howeveroutsideof the interconnectedbiologyof theecosystemby-catch isembeddedwithinsocialandeconomicsys-temsDifferentunitsofanalysismaybeneededatdifferent levelsofthehierarchytocopewiththechallengesofincompleteoverlapbetween jurisdictional units fisheries target stocks and by-catchstocksJurisdictionalissuesareimportantandcomplexpotentiallyimpeding implementationFleets interact raisingtheriskofpolicyleakageforexampleifpeopleshifttootherfisheriesgearorliveli-hoodsThereforethescaleatwhicheachelementofthemitigationhierarchyisimplementedislikelytovarywithincentivestomitigateoftenbeingbest appliedat thevessel level focussedon reducingindividualmortalitywhileoffsettingisimplementedatthescaleoftheby-catchspeciesrsquostockWithtransboundaryspeciesunilateralconservationinonejurisdictioncreatesthepotentialforproductiontrade and conservation leakages For example a conserving Statecouldimplementtheavoidancestepandshutdownordramaticallycurtailitsownproductionofswordfishtoreduceseaturtleby-catchbuttheknock-oneffectmaybemoreimportationofswordfishfromfleetswithhigherseaturtleby-catch(RausserHamiltonKovachampStifter2009)

Translatingtheframeworkfromaspeciestoanecosystemlevelwill require consideration of the potential interactions between

12emsp |emsp emspensp MILNER- GULLAND Et AL

by-catchmitigationapproachestargetedatdifferentspecies(Serafyetal 2012) Actions to mitigate by-catch for one group of spe-cies can increase or decrease it for others and so a system-wideapproach isneededForexample changing fromJ-hooks tocirclehookstoreducemortalityofturtlesmaydecreaseorincreasesharkmortality(Andrakaetal2013GodinCarlsonampBurgener2012)In terrestrial systems similar interactions arise and value judge-mentsaremade(whetherexplicitlyorimplicitly)astowhatlossandgain of ldquobiodiversityrdquo translates to in operational terms andwhatelementsofbiodiversitymattermosttoimplementers

Uncertainty is high in ocean ecosystems creating both chal-lengesandopportunitiesinapplyingtheconceptofNNLthroughamitigationhierarchythatincludesoffsettingInparticularformarinemegafaunathereishighuncertaintyintheprocesseslinkinganyel-ementofthemitigationhierarchythroughtochangesinpopulationgrowthrateFurthermore impactscanbelong-termhardtomea-sureandspatiallydiffuseanduncertaintyisnotpredictablyspreadthroughthehierarchyThiscreatesadifferentsetofchallengestothosefacedinterrestrialsystemswhereatleastforsometypesofenvironmentalimpactthelinksbetweenactionandimpactarerel-ativelydirectandmeasurableanduncertaintygenerally increasesthroughthemitigationhierarchy (fromavoidthroughminimizere-mediatetooffset)

By-catch reduction measures have had significant successesoverthelastdecadesasaresultofsubstantialinvestmentoftimeand funding by researchers management authorities conserva-tionorganizationsandfishers(Coxetal2007)Howeverthissuc-cessisnotuniversalJustasforanyfisheriesmanagementissueapoorregulatoryregimelimitedcomplianceandlackofinforma-tionhampereffortstoreduceby-catchInsomeplaceshighlevelsofby-catch limitedoptions formitigationandweakgovernance(leadingtopoorenforcement)cancombinetomaketheby-catchproblemintractableOurframeworkwillnotsolvetheseproblemsHowever itbrings together the full rangeofapproaches forby-catchmitigationinastructuredandsystematicwaywhichrequiresatargettobeexpressedagainstwhichoutcomescanbeevaluatedByexposingareasofuncertaintyanddatadeficiencyitcouldchal-lengescientistsandmanagerstoobtainthedatarequiredproperlytoevaluate theeffectivenessofmitigationmeasuresThis couldthensupportandencourageclearerdecision-makingandprioriti-zationofactionsOurframeworkdemonstratesthattheprincipleof implementing thegoalofnonet loss throughamitigationhi-erarchy isasapplicable tomarinemegafaunaby-catchas to ter-restrial systems where it is already widely used in challengingdata-poorcircumstances

There isuntappedpotential forcost-effectiveby-catchmitiga-tionwhichcouldberealizedwiththeadoptionofthisframeworkandwithconsiderationofnewapproachestoincentivizingby-catchmitigationwithinthestepsofthehierarchyApplyingittoafewcase-studiesinpracticewilldemonstrateempiricallywhereandhowthepotentialforimprovedeffectivenesscouldbestberealizedExistinglegalframeworksoftenprecludeapproacheswhichimplicitlyorex-plicitly permit by-catch including the use of economic incentives

ornewapproachessuchasoffsetsHoweverinthiscontextofdy-namicuncertaintythedividendsofthinkingmorecreativelyaboutby-catchmitigationcouldbehigh

ACKNOWLEDG EMENTS

EJMG acknowledges the Pew Charitable Foundation for its sup-port of thiswork This article originated at a 2013workshop co-organized by NOAA-Fisheries and IUCN-CEEM-FEG entitledldquoMultidisciplinaryWorkshoptoAddressEcosystem-LevelImpactsofFisheriesBycatchonMarineMegafaunaBiodiversityConservationthrough Mitigation Policy Economic Instruments and TechnicalChangerdquo We thank the reviewers for their insightful commentswhichmuchimprovedthemanuscript

ORCID

E J Milner-Gulland httporcidorg0000-0003-0324-2710

R E FE R E N C E S

Alfaro-Shigueto J Dutton P H amp Mangel J (2007) Interactionsbetween leatherback turtles and Peruvian artisanal fisher-ies Chelonian Conservation and Biology 6 129ndash134 httpsdoiorg1027441071-8443(2007)6[129ibltap]20co2

Alfaro-Shigueto JMangel JCBernedoFDuttonPHSeminoffJAampGodleyB J (2011) Small-scale fisheriesofPeruAmajorsinkformarineturtles inthePacificJournal of Applied Ecology481432ndash1440httpsdoiorg101111j1365-2664201102040x

Alfaro-ShiguetoJMangelJCPajueloMDuttonPHSeminoffJ A amp Godley B J (2010) Where small can have a large im-pact Structure and characterization of small-scale fisheries inPeru Fisheries Research 106 8ndash17 httpsdoiorg101016jfishres201006004

Andraka SMugM HallM PonsM Pacheco L ParralesM hellipOrtega D (2013) Circle hooks Developing better fishing prac-ticesintheartisanallonglinefisheriesoftheEasternPacificOceanBiological Conservation 160 214ndash224 httpsdoiorg101016jbiocon201301019

ApostolopoulouEampAdamsWM(2017)BiodiversityoffsettingandconservationReframingnaturetosaveitOryx5123ndash31httpsdoiorg101017S0030605315000782

BaacuteezJCRealRGarciacutea-SotoCJoseacuteMMaciacuteasDampCamintildeasJA(2007)Loggerheadturtleby-catchdependsondistancetothecoastindependentoffishingeffortImplicationsforconservationandfish-eries management Marine Ecology Progress Series 338 249ndash256httpsdoiorg101017S0030605315000782

BBOP (2012) Standard on biodiversity offsets Business and biodiversity offsets programmeWashingtonDCForestTrends

Bishop J (2006) Standardizing fishery-dependent catch and ef-fort data in complex fisheries with technology change Reviews in Fish Biology and Fisheries 16 21ndash38 httpsdoiorg101007s11160-006-0004-9

BoyceJ(1996)AneconomicanalysisofthefisheriesbycatchproblemJournal of Environmental Economics and Management31 314ndash336httpsdoiorg101006jeem19960047

BugoniLManciniPLMonteiroDSNascimentoLampNevesTS(2008)SeabirdbycatchintheBrazilianpelagiclonglinefisheryandareviewofcaptureratesinthesouthwesternAtlanticOceanEndangered Species Research5137ndash147httpsdoiorg103354esr00115

emspensp emsp | emsp13MILNER- GULLAND Et AL

BullJWampBrownlieS(2017)Thetransitionfromnonetlosstoanetgainof biodiversity is far from trivialOryx51 53ndash59 httpsdoiorg101017S0030605315000861

BullJWBryantCBakerJampMilner-GullandEJ(2015December28)Developing measuring and communicating the outcomes of cor-porate biodiversity strategies [pdfdocument]RetrievedfromhttpwwwwildbusinessorgBull_etal_2015_WBLpdf

BullJWGordonAWatsonJEampMaronM(2016)Seekingcon-vergenceonthekeyconceptsinlsquononetlossrsquopolicyJournal of Applied Ecology531686ndash1693httpsdoiorg1011111365-266412726

BullJWHardyMJMoilanenAampGordonA (2015)Categoriesof flexibility in biodiversity offsetting and their implications forconservation Biological Conservation 192 522ndash532 httpsdoiorg101016jbiocon201508003

Bull JW Lloyd S P amp StrangeN (2017) Implementation gap be-tween the theory and practice of biodiversity offset multipliersConservation Lettershttpsdoiorg101111conl12335

Bull JW SuttleKBGordonA SinghN JampMilner-Gulland EJ(2013)BiodiversityoffsetsintheoryandpracticeOryx47369ndash380httpsdoiorg101017S003060531200172X

CampbellLMampCornwellML(2008)Humandimensionsofbycatchreduction technology Current assumptions and directions for fu-tureresearchEndangered Species Research5325ndash334httpsdoiorg103354esr00172

Caswell H Brault S Read A J amp Smith T D (1998) Harborporpoise and fisheries An uncertainty analysis of inciden-tal mortality Ecological Applications 8 1226ndash1238 httpsdoiorg1018901051-0761(1998)008[1226hpafau]20co2

ClementsTJohnANielsenKAnDTanSampMilner-GullandEJ (2010)Payments forbiodiversityconservation in thecontextofweak institutions Comparison of three programs from CambodiaEcological Economics 69 1283ndash1291 httpsdoiorg101016jecolecon200911010

CoxTLewisonRŽydelisRCrowderLSafinaCampReadA(2007)ComparingeffectivenessofexperimentalandimplementedbycatchreductionmeasuresTheidealandtherealConservation Biology211155ndash1164httpsdoiorg101111j1523-1739200700772x

CrollDADewarHDulvyNKFernandoDFrancisMPGalvaacuten-Magantildea F hellip Newton K M (2016) Vulnerabilities and fisher-ies impactsTheuncertain futureofmanta anddevil raysAquatic Conservation Marine and Freshwater Ecosystems 26 562ndash575httpsdoiorg101002aqc2591

Damalas D amp Vassilopoulou V (2013) Slack regulation com-pliance in the Mediterranean fisheries A paradigm from theGreek Aegean Sea demersal trawl fishery modelling discardogives Fisheries Management and Ecology 20 21ndash33 httpsdoiorg101111j1365-2400201200860x

DuttonDLDuttonPHChaloupkaMampBoulonRH(2005)IncreaseofaCaribbeanleatherbackturtleDermochelys coriaceanestingpop-ulation linked to long-termnestprotectionBiological Conservation126186ndash194httpsdoiorg101016jbiocon200505013

DuttonPJosephJSquiresDampWilliamsM(2011)Bellagioblue-print foractiononseaturtlesChapter2 InPDuttonDSquiresampM Ahmed (Eds) Conservation of pacific sea turtles (pp 15ndash36)HonoluluHIUniversityofHawaiiPress

DuttonPampSquiresD (2008)AholisticstrategyforPacificseatur-tlerecoveryOcean Development and International Law39200ndash222httpsdoiorg10108000908320802013685

FAO (2011 January 5) International guidelines on bycatch manage-ment and reduction of discards Rome Italy Food and AgricultureOrganisation [pdf document] Retrieved from httpwwwfaoorgdocrephelliptba0022t00pdf

Finkelstein M Bakker V Doak D F Sullivan B Lewison RSatterthwaite W H hellip Henry R W (2008) Evaluating the po-tential effectiveness of compensatory mitigation strategies for

marinebycatchPLoS ONE3 e2480httpsdoiorg101371jour-nalpone0002480

FowlerSJ(2016January5)Draft best practice mitigation guidelines for sharks and rays taken in purse- seine and long-line fisheries Convention on Migratory Species[pdfdocument]RetrievedfromhttpwwwcmsintsitesdefaultfilesdocumentCMS_Sharks_CWG1_Doc_3_2pdf

FrancisMP(2014)Survival and depth distribution of spinetail devilrays (Mobula japanica) released from purse-seine catches NIWA ClientReportNoWLG2014-2WellingtonNewZealandDepartmentofConservation

Fulton E A Smith A D Smith D C amp van Putten I E (2011)Human behaviour The key source of uncertainty in fish-eries management Fish and Fisheries 12 2ndash17 httpsdoiorg101111j1467-2979201000371x

GardnerTAHaseABrownlieSEkstromJMPilgrimJDSavyCEhellipTenKateK(2013)BiodiversityoffsetsandthechallengeofachievingnonetlossConservation Biology271254ndash1264httpsdoiorg101111cobi12118

GjertsenHHallMampSquiresD(2010)IncentivestoaddressbycatchInRAllenJJosephampDSquires(Eds)Conservation and manage-ment of transnational tuna fisheries (pp225ndash250)Ames IAWiley-Blackwellhttpsdoiorg1010029780813820262ch14

Gjertsen H Squires D Dutton P amp Eguchi T (2014) Cost-effectivenessofalternativeconservationstrategieswithapplicationtothePacificLeatherbackTurtleConservation Biology28140ndash149httpsdoiorg101111cobi12239

GodinACCarlson JKampBurgenerV (2012)Theeffectofcirclehooks on shark catchability and at-vessel mortality rates in long-lines fisheriesBulletin of Marine Science88 469ndash483 httpsdoiorg105343bms20111054

GrimmDBarkhornIFestaDBonzonKBoomhowerJHovlandV amp Blau J (2012) Assessing catch sharesrsquo effects evidencefrom Federal United States and associated British Columbianfisheries Marine Policy 36 644ndash657 httpsdoiorg101016jmarpol201110014

HallMA(1996)OnbycatchesReviews in Fish Biology and Fisheries6319ndash352httpsdoiorg101007BF00122585

HallMAAlversonDLampMetuzalsKI(2000)By-catchProblemsand solutions Marine Pollution Bulletin 41 204ndash219 httpsdoiorg101016S0025-326X(00)00111-9

HallMANakanoHClarke S Thomas SMolloy J PeckhamSHhellipHallSJ (2007)Workingwithfisherstoreduceby-catchesIn S J Kenelly (Ed)By-catch reduction in the worldrsquos fisheries (pp235ndash288) Dordrecht The Netherlands Springer httpsdoiorg101007978-1-4020-6078-6_8

HallM amp RomanM (2013)Bycatch and non-tuna catch in the tropi-cal tuna purse seine fisheries of the worldFisheriesandAquacultureTechnicalPaper568RomeItalyFAO

HallMASwimmerYampPargaM(2012)NoldquosilverbulletsrdquobutplentyofoptionsWorkingwiththeeasternpacificartisanalfisherstore-duceseaturtlemortalityinfisheriesInJASeminoffampBWallace(Eds)Sea turtles of the eastern pacific Advances in research and con-servation(pp136ndash153)TucsonAZUniversityofArizonaPress

HamnerRMWadePOremusMStanleyMBrownPConstantineR amp Baker C S (2014) Critically low abundance and limits tohuman-relatedmortalityfortheMauirsquosdolphinEndangered Species Research2687ndash92httpsdoiorg103354esr00621

HatchSA(2003)Statisticalpowerfordetectingtrendswithapplica-tions to seabird monitoringBiological Conservation 111 317ndash329httpsdoiorg101016S0006-3207(02)00301-4

HeppellSSCrowderLBampCrouseDT(1996)Modelstoevaluateheadstartingasamanagementtoolforlong-livedturtlesEcological Applications6556ndash565httpsdoiorg1023072269391

HoughPampRobertsonM(2009)MitigationunderSection404oftheCleanWater ActWhere it comes from what it meansWetlands

14emsp |emsp emspensp MILNER- GULLAND Et AL

Ecology and Management 17 15ndash33 httpsdoiorg101007s11273-008-9093-7

IATTC(2015)Resolution on the conservation of mobulid rays caught in as-sociation with fisheries in the IATTC convention area Inter-AmericanTropical TunaCommission89thAnnualMeetingResolutionC-15-04LaJollaCAInter-AmericanTropicalTunaCommission

IFC(2012)Performance standard 6 Biodiversity conservation and sustain-able management of natural resources January 1 2012WashingtonDCInternationalFinanceCorporation

Innes J Pascoe S Wilcox C Jennings S amp Paredes S (2015)MitigatingundesirableimpactsinthemarineenvironmentAreviewofmarket-basedmanagementmeasuresFrontiers in Marine Science276httpsdoiorg103389fmars201500076

JanniseCSquiresDSeminoffJampDuttonP (2010)Conservationinvestments andmitigationTheCaliforniadrift gillnet fishery andpacificseaturtles InRQGraftonRHilbornDSquiresMTaitampMJWilliams(Eds)Handbook of marine fisheries conservation and management(pp231ndash240)OxfordUKOxfordUniversityPress

Jones E amp FrancisM (2012)Protected rays ndash Occurrence and devel-opment of mitigation methods in the New Zealand tuna purse seine fishery Auckland New Zealand National Institute of Water andAtmosphericResearch

KormosRKormosCFHumleTLanjouwARainerHVicturineR hellipWilliamson E A (2014) Great apes and biodiversity offsetprojectsinAfricaThecasefornationaloffsetstrategiesPLoS ONE9(11)e111671httpsdoiorg101371journalpone0111671

KotchenMJ (2013)Voluntaryand information-basedapproachestoenvironmentalmanagementApubliceconomicsperspectiveReview of Environmental Economics and Policy 7(2) 276ndash295 httpsdoiorg101093reepret012

Kyriazi Z LejanoRMaes FampDegraer S (2015)Bargaining a netgaincompensationagreementbetweenamarinerenewableenergydeveloperandamarineprotectedareamanagerMarine Policy6040ndash48httpsdoiorg101016jmarpol201506005

LentRampSquiresD(2017)ReducingmarinemammalbycatchinglobalfisheriesAneconomicsapproachDeep Sea Research Part II Topical Studies in Oceanography 140 268ndash277 httpsdoiorg101016jdsr2201703005

Lewison R L Crowder L B Read A J amp Freeman S A (2004)Understanding impactsof fisheriesbycatchonmarinemegafaunaTrends in Ecology amp Evolution19598ndash604httpsdoiorg101016jtree200409004

MannC (2015)StrategiesforsustainablepolicydesignConstructiveassessmentofbiodiversityoffsetsandbankingEcosystem Services16266ndash274httpsdoiorg101016jecoser201507001

Marine Stewardship Council (2014 June 21) MSC fisheries certifica-tion requirements v20 [pdf doc] httpswwwmscorgdocumentsscheme-documentsfisheries-certification-scheme-documentsfisheries-certification-requirements-version-20

MaronM IvesCDKujalaHBullJWMaseykFJBekessyShellip Possingham H P (2016) Taming a wicked problem Resolvingcontroversies inbiodiversityoffsettingBioScience66(6)489ndash498httpsdoiorg101093bioscibiw038

MaxwellSLMilner-GullandEJJonesJPKnightATBunnefeldNNunoAhellipRhodesJR(2015)BeingsmartaboutSMARTenvi-ronmentaltargetsScience3471075ndash1076httpsdoiorg101126scienceaaa1451

Moilanen A Van Teeffelen A J Ben-Haim Y amp Ferrier S (2009)Howmuch compensation is enoughA framework for incorporat-inguncertaintyandtimediscountingwhencalculatingoffsetratiosfor impactedhabitatRestoration Ecology17 470ndash478 httpsdoiorg101111j1526-100X200800382x

MorarNToadvineTampBohannanBJ(2015)Biodiversityattwenty-fiveyearsRevolutionorredherringEthics Policy amp Environment1816ndash29httpsdoiorg1010802155008520151018380

OrphanidesCDampPalkaDL(2013)Analysisofharborporpoisegill-netbycatchcomplianceandenforcement trends in theUSnorth-western Atlantic January 1999 to May 2010 Endangered Species Research20251ndash269httpsdoiorg103354esr00499

Pascoe S Innes J Holland D Finas M Theacutebaud O TownsendR hellip Hutton T (2010) Use of incentive-based managementsystems to limit bycatch and discarding International Review of Environmental and Resource Economics 4 123ndash161 httpsdoiorg10156110100000032

PhalanBHayesG Brooks SMarshDHoward PCostelloeBhellip Whitaker S (2017) Avoiding impacts on biodiversity throughstrengthening the first stage of the mitigation hierarchy Oryxhttpsdoiorg101017S0030605316001034

Queacutetier F Regnery B amp Levrel H (2014) No net loss of biodiver-sity or paper offsets A critical review of the French no net losspolicy Environmental Science amp Policy 38 120ndash131 httpsdoiorg101016jenvsci201311009

RadzioTASmolinskyJAampRoosenburgWM(2013)Lowuseofre-quiredterrapinbycatchreductiondevicesinarecreationalcrabpotfisheryHerpetological Conservation and Biology8222ndash227

RaineyHJPollardEHBDutsonGEkstromJMLivingstoneSRTempleHJampPilgrimJD(2015)AreviewofcorporategoalsofnonetlossandnetpositiveimpactonbiodiversityOryx49232ndash238httpsdoiorg101017S0030605313001476

Rausser G C Hamilton S F Kovach M amp Stifter R (2009)UnintendedconsequencesThe spillovereffectsof commonprop-ertyregulationsMarine Policy3324ndash39httpsdoiorg101016jmarpol200803020

Rice J (2014) Evolution of international commitments for fisheriessustainability ICES Journal of Marine Science Journal du Conseil71157ndash165httpsdoiorg101093icesjmsfst078

RichardYampAbrahamER(2013)ApplicationofPotentialBiologicalRemoval methods to seabird populations New Zealand AquaticEnvironmentandBiodiversityReport108

RodeJGoacutemez-BaggethunEampKrauseT(2015)Motivationcrowd-ingbyeconomic incentives inconservationpolicyAreviewoftheempiricalevidenceEcological Economics117270ndash282httpsdoiorg101016jecolecon201411019

RogersAA(2013)SocialwelfareandmarinereservesIswillingnesstopayforconservationdependentonmanagementprocessAdiscretechoiceexperimentoftheNingalooMarineParkinAustraliaCanadian Journal of Agricultural EconomicsRevue Canadienne Drsquoagroeconomie61217ndash238httpsdoiorg101111cjag12008

Rosenberg A A amp McLeod K L (2005) Implementing ecosystem-basedapproachestomanagementfortheconservationofecosystemservicesMarine Ecology Progress Series300 270ndash274 httpsdoiorg103354meps300270

Segerson K (2010) Can voluntary programs reduce sea turtle by-catch Insights from the literature in environmental economics InRQGraftonRHilbornDSquiresMTaitampMJWilliams(Eds)Handbook of marine fisheries conservation and management(pp618ndash629)OxfordUKOxfordUniversityPress

Serafy JECookeS JDiazGAGraves JEHallMShivjiMampSwimmerY(2012)CirclehooksincommercialrecreationalandartisanalfisheriesResearchstatusandneedsforimprovedconser-vation and management Bulletin of Marine Science 88 371ndash391httpsdoiorg105343bms20121038

ShiodeDHu F ShigaM Yokota K amp Tokai T (2005)Midwaterfloatsystemforstandardizinghookdepthsontunalonglinestore-duce sea turtleby-catchFisheries Science71 1182ndash1184httpsdoiorg101111j1444-2906200501080x

Sims M Cox T amp Lewison R (2008) Modeling spatial patternsin fisheries bycatch Improving bycatch maps to aid fisheriesmanagement Ecological Applications 18 649ndash661 httpsdoiorg10189007-06851

emspensp emsp | emsp15MILNER- GULLAND Et AL

Squires D amp Garcia SM (2014) Ecosystem-level impacts of fisheries bycatch on marine megafauna Biodiversity conservation through miti-gation policy economic instruments and technical changeReportofthe IUCN-CEM-FEGScientificworkshopGland Switzerland 7ndash10October2013GlandSwitzerlandIUCN

SquiresDampGarciaSM(inpress)Fisheries bycatch in marine ecosys-tems Policy economic instruments and technical change ChichesterUKJWileyampSons

SwimmerYArauzRMcCrackenMMcNaughtonLBallesteroJMusylMhellipBrillR(2006)DivingbehavioranddelayedmortalityofoliveridleyseaturtlesLepidochelys olivaceaaftertheirreleasefromlongline fishing gearMarine Ecology Progress Series323 253ndash261httpsdoiorg103354meps323253

TolottiMTFilmalterJDBachPTravassosPSeretBampDagornL(2015)BanningisnotenoughThecomplexitiesofoceanicsharkmanagementbytunaregional fisheriesmanagementorganizationsGlobal Ecology and Conservation 4 1ndash7 httpsdoiorg101016jgecco201505003

Tuck G N Polacheck T amp Bulman C M (2003) Spatio-temporaltrendsoflonglinefishingeffortintheSouthernOceanandimplica-tionsforseabirdbycatchBiological Conservation1141ndash27httpsdoiorg101016S0006-3207(02)00378-6

UNEP-WCMC(2016)Marine no net loss A feasibility assessment of imple-menting no net loss of biodiversity in the seaCambridgeUKUnitedNationsEnvironmentProgramme

Vaissiegravere A-C Levrel H Pioch S amp Carlier A (2014) Biodiversityoffsets for offshore wind farm projects The current situation inEurope Marine Policy 48 172ndash183 httpsdoiorg101016jmarpol201403023

Wallace B P Heppell S S Lewison R L Kelez S amp CrowderL B (2008) Impacts of fisheries bycatch on loggerhead tur-tles worldwide inferred from reproductive value analy-ses Journal of Applied Ecology 45 1076ndash1085 httpsdoiorg101111j1365-2664200801507x

Wanless R M Ryan P G Altwegg R Angel A Cooper JCuthbert R amp Hilton G M (2009) From both sides Dire de-mographic consequences of carnivorous mice and longlining for

the critically endangered Tristan albatrosses on Gough IslandBiological Conservation 142 1710ndash1718 httpsdoiorg101016jbiocon200903008

WardP LawrenceEDarbyshireRampHindmarshS (2008) Large-scale experiment shows that nylon leaders reduce shark bycatchandbenefitpelagiclonglinefishersFisheries Research90100ndash108httpsdoiorg101016jfishres200709034

WardTampPhillipsB(2010)SeafoodecolabelingInRQGraftonRHilbornDSquiresMTaitampMJWilliams(Eds)Handbook of ma-rine fisheries conservation and management (pp 608ndash617) OxfordUKOxfordUniversityPress

WilcoxCampDonlanCJ (2007)Compensatorymitigationasasolu-tion to fisheries bycatch-biodiversity conservation conflictsFrontiers in Ecology and the Environment 5 325ndash331 httpsdoiorg1018901540-9295(2007)5[325cmaast]20co2

WilcoxCampDonlanCJ (2009)NeedforaclearandfairevaluationofbiodiversityoffsetsforfisheriesbycatchConservation Biology23770ndash772httpsdoiorg101111j1523-1739200901173x

Wolf SHartlBCarrollCNeelMCampGreenwaldDN (2015)Beyond PVAWhy recovery under the Endangered Species Act ismorethanpopulationviabilityBioScience65200ndash207httpsdoiorg101093bioscibiu218

ZedlerJBampCallawayJC (1999)TrackingwetlandrestorationDomitigation sites follow desired trajectories Restoration Ecology 769ndash73httpsdoiorg101046j1526-100X199907108x

Žydelis R Wallace B P Gilman E L amp Werner T B (2009)Conservation of marine megafauna through minimization of fish-eries bycatch Conservation Biology 23 608ndash616 httpsdoiorg101111j1523-1739200901172x

How to cite this articleMilner-GullandEJGarciaSArlidgeW etalTranslatingtheterrestrialmitigationhierarchytomarinemegafaunaby-catchFish Fish 2018001ndash15 httpsdoiorg101111faf12273

Page 4: Translating the terrestrial mitigation hierarchy to marine ......of marine megafauna by-catch in fisheries, going from defining an overarching goal with an associated quantitative

4emsp |emsp emspensp MILNER- GULLAND Et AL

thestockmoreindirectlyoractatthebroaderspecieslevel(suchasrestoration in other locations ormeasures to improve complianceand reduce uncertainty) Howeverwe feel that the clarity of theprobabilisticapproachinourframeworkwhichextendstheclassi-ficationbyHall(1996)isparticularlyhelpful

Ourdivisionofmitigationapproachesintothesecategoriescanberepresentedinthefollowingconceptualmodelrelatingtoapar-ticularby-catchspeciesinwhichtheunitisrateofchangeinpopu-lationsizeasaresultofby-catchanditsmitigation

HereΔλT is the target levelofoverallnetdamage inflictedbyby-catchonthespeciesconcernedmeasuredintermsofchangeinpopulationgrowthratewithrespecttotheagreedbaselineAzeroΔλTimpliesthatthereductioninpopulationgrowthratecausedbyby-catch after avoidance andmitigationmeasures have been im-plementedisbalancedbythegainengenderedbyoffsetmeasuresThereisalsothepossibilityforΔλTtobenegative(thereisstilladdi-tionalpopulationdeclineasaresultofby-catchevenaftermeasurestoreduceit)orpositive(equivalenttonet gainmeaningthatspeciespopulationgrowthishigherthanitwouldotherwisehavebeenasaresultofthecombinationofmeasurestakenunderthemitigationhierarchy)

f(EBtimesBPUE)istheeffectonpopulationgrowthrateoftheby-catch-relevantcomponentoffishingeffortbrokendownintotheby-catch-relevanteffortitselfEBandtheby-catchtakenperunitof that effort BPUEwhere f() is the effect of this effort on theby-caught speciesrsquo population dynamics Thiswould generally becalculatedastheoutputofapopulationmodelAreduction inEB isequivalenttoafisheryavoidingby-catchpartiallyorcompletelyIt could include restricting the fishery to particular areas or sea-sons modification of fishing practices and operations (eg set-tingthegeardeepertoavoiddepthswhereby-caughtspeciesare

prevalent)AreductioninBPUEistheresultoftheat-seameasuresencompassed intheldquominimizerdquoandldquoremediaterdquostepsofthemiti-gationhierarchy

By-catch-relevanteffortEBisasubsetoftheoverallfishingef-fort thatoccurs in thearea inwhichthere is riskofby-catch (E)Given thecomplexitiesof estimatingEB inmanycases itwill benecessarytoapproximateitbyE(egTuckPolacheckampBulman2003) Thismay be problematic for example Baacuteez etal (2007)show that loggerhead turtle (Caretta caretta Cheloniidae) by-catchintheMediterraneanwasnotcorrelatedwithfishingeffort(measuredasnumberofhooks)by-catchwasinsteadstronglyre-lated todistance from thecoastThey suggest that thiswasnotbecauseturtleabundance isa functionofdistance (whichwouldhave impliedagradient inEB) butbecause fisherbehaviourvar-iedalthoughtheyleftinvestigationofthemechanismsforfurtherresearchBPUEisafunctionofcatchabilityoftheby-caughtspe-ciesaswellasEB forexampleWardLawrenceDarbyshireandHindmarsh(2008)carriedoutamultispeciesanalysisoftheeffectsof nylon leaders on catch rates and showed that catch reducedwithnylonforsharksbluemarlin(Makaira nigricansIstiophoridae)and snake mackerel (Gempylus serpens Gempylidae) and in-creased for bigeye tuna (Thunnus obesus Scombridae) and blackmarlin(Istiompax indicaIstiophoridae)TherelationshipsbetweenEEB andBPUEare likely tobe complex and confoundedTherehavebeen limitedexplorationsof these relationships inby-catchdatasetswhich typically suffer from low sample sizes and zero-inflationrequiringspecializedmodellingtechniques (eg thespa-tiallyexplicitBayesianhierarchicalmodelsofSimsCoxampLewison2008)By-catchmitigationmayuseasuiteofinteractingmeasuresfrom several levels of the mitigation hierarchy (Table2) whichchangeovertimeaddingfurthertothecomplexityofseparatingE EBandBPUE(asdiscussedfortargetfisherydatabyBishop2006)Wedonothereattemptfurthertoclarifytheserelationshipsbutakeyresearchneedistodisentanglethesevariablesinanempiricalsetting

(1)ΔλT= f(

EBtimesBPUE)

minusOT

Step of the hierarchy Example measures

Avoidance Excludingfishingfromtheareas(no-fishingzones)seasons(closedseasons)ortimesofdaywherethesespeciesaremostvulnerable

Minimization Usingon-vesseltechnologieswhichaimtoreducethenumberofencounteredindividualsthatarecapturedduringfishingoperationssuchastorilinesforscaringseabirdsawayfromlonglinesorsonicdevicestosignalnetstomarinemammals

Remediation Deviceswhichenableindividualstoreleasethemselvesfromthegear(selectivitygridsturtleexcluderdevices)ortobereleased(egMedinapanelsoperatedintunapurse-seinefisheriestoletdolphinsescapebeforegettingonthedeck)orreleasingthemondeckandprovidingforasafereturntothesea(egalargemeshsoftwebbingcargonetcanbeusedtoldquosieverdquoarayfromthecatchandliftitoverthesideofthevesselFrancis2014)

Offsetting Eradicatinginvasivepredatorsonislandswhereseabirdsnestrestoringhabitatrestockingwithhatchery-raisedindividualsimprovingby-catchperformanceofothergeartypesinthearea

TABLE 2emspExamplesofmeasureswhichcanbetakenundereachstepofthemitigationhierarchy

emspensp emsp | emsp5MILNER- GULLAND Et AL

OT is the net effect on population growth rate of policiesaimingtoimprovetheoverallviabilityoftheby-caughtspeciesrsquopopulation representing ldquooffsettingrdquo of the damage caused Itrepresents the expected effects of measures to improve con-ditions for individuals which would not have been at risk ofby-catch at that particular stage in their lives or location Forexample supplementation in nesting areas (for turtles) resto-rationofnestinghabitat(forseabirds)orimplementationofpro-tectedareasaimedatdemographicgroupsnotdirectlyimpactedby fishing (calving areas for cetaceans juvenile concentrationsforfish)

3emsp |emspOPER ATIONALIZING THE FR AMEWORK

In Table3we illustrate the application of the by-catchmitigationframework using four examples from different fisheries and by-catchtaxaSpecificsolutionstoEquation1couldcomefromtakingintoaccount the regulatory cultural andeconomicconditions inaparticularfisheryForinstanceoncethefocalby-catchpopulationhasbeendefinedthenitispossibletosolvetheequationbyassign-ingfactorsaffectingdecision-makingincludingcostIfaleast-costapproachtoby-catchgoalsisappropriateEBBPUEandOT could be expressedasfunctionsofcosttosolvetheequationforagivenΔλT Another approachwould be tomaximizeΔλT subject to a budgetconstraint

Table3highlightsthatthereisnotalwayspotentialforeffec-tive action at each level of the hierarchy for some species (egoceanicwhitetipslonglines)theremaybelimitedpotentialatalllevelsTheframeworkisawayoforganizingandstructuringthink-ingaboutby-catchmitigationandenablingmitigationeffective-nesstobeassessedagainstaconcretelydefinedandmeasurabletargetItsfunctionisnottoproposenewwaysofdoingby-catchmitigationforcasesliketheseIfonusingtheframeworktoanal-yse the effectiveness of the measures available for a given by-caughtstockitisfoundthatitisnotpossibletoreachthechosentarget(egNNL)thendifficultdecisionsmustbemadeForexam-plethetargetmayneedtochangewhichcouldimplyanaccep-tanceofcontinuingdeclineoftheby-caughtstockOrthefisherymustbe restructured in away that reducesby-catcheffectively(maybeevencloseddown)Orinvestmentmustbemadeintotech-nological innovation todevelopnewways to reduceby-catch Ifitisfoundthatthedataareinadequatefortheanalysisrequiredthenthedecisionmustbemadeeithertoinvestinimprovingtheevidencebaseor to recognize that it is not possible to evaluatewhether by-catch mitigation has been effective in reaching theagreed goal The frameworkrsquosmain utility therefore is tomakethesechoicesexplicit

Equation1couldbeextendedtohandlemultiplespeciesvary-inggeartypesorheterogeneousby-catchreductionmethodsForinstanceBPUEcanbedecomposedintoseveralcomponentsrepre-sentingthedifferentstagesoftheprocessIfBPUErepresentsthesumofindividualsdeadonarrivalindividualscapturedanddyingon

thevessel and individualsdyingafter live releasewecan rewriteBPUEasaseriesoffactors

whereBDOAistheby-catchperuniteffortthatarrivestotheboatdeadBOBistheby-catchperuniteffortthatarrivestothevesselalivePDVistheproportiondyingonthevesselandPDRisthepro-portiondying after release For instance a higherproportionofby-catchofseaturtlesandotherspeciesarrivestotheboatdeadwhenusinglonglinesthataresetdeepsuchasthoseusedforbig-eyetunathatcanbesetmorethan300mdeepwhencomparedto a shallow set longline such as those used inmany nearshoreartisanal fisheries (Andrakaetal2013HallSwimmerampParga2012Swimmeretal2006)ThisdifferencewouldappearintheBDOA termSuchadecomposition illustratestheflexibilityofthisframeworkinhandlingfishery-andspecies-specificfeaturesandalsoservestohighlightareaswheredifferentmitigationmethodswouldhavethegreatestinfluence(egShiodeHuShigaYokotaampTokai2005)Anotherextensiontothebasicframeworkwouldbetoconsiderexplicitlytheuncertaintysurroundingdifferentel-ements of the conceptual model and the impact of this uncer-taintyonwhichelementofby-catchmitigationshouldbeafocus(Table3)

It is important tonote that this equation isnot a truebioeco-nomicequationtobesolvedRatheritisaconceptualframeworkinwhichwemakethecomponentsofthemitigationhierarchyexplicitinordertoguidethinkingtowardsamoreholisticapproachtoad-dressingby-catchItalsodoesnotrepresentahierarchysuchasisrequiredinterrestrialsystemsTomakethisequationintoahierar-chyratherthanamodelforleast-costmitigationofby-catchitcouldbesetupasagoalprogrammingfunctionwithsequentialsolutionstoeachelementsummedtoproducethefinalmitigationoutcomeInoperationaltermsthistranslatesintoapresumptionthatinvestmentandeffortshouldbefocusseddifferentiallyonsequentialelementsofthemodelstartingwithEBthenBPUEthenOTsothatoffsettingrelatesonly to theunavoidable residualharmonceall other stepshavebeentakenThismaybereflected intheemphasisplacedontheincentivesgiventofisherstochangebehaviourpertainingtose-quentialelementsofthehierarchyinthetimingoftheoffsetorinthedispositionofthefundingforresearchandconservationactionallocatedbygovernment

ResearchiscurrentlyongoingtooperationalizeEquation1tore-duceturtleby-catchofasmall-scalegillnetfisheryoperatingoutofSanJoseportPeru(Alfaro-Shiguetoetal2010)Currentlyasmall-scalecertificationschemeisundertrialbytheNGOProDelphinuswhich aims to give premium prices for fish caught by skippersabiding by best-practice by-catch reduction guidelines (J Alfaro-Shigueto and J Mangel personal communication) The researchentailscollectingdetailedeconomicdatafromallgillnetvesselstounderstand the economic costs involved in fishing operations tocalculatethepotentialadditionalcostsofmeasuresateachstagein

(2)BPUE=BDOA+PDVtimesBOB+(

1minusPDV)

timesBOBtimesPDR

6emsp |emsp emspensp MILNER- GULLAND Et AL

TABLE 3emspSummaryofoptionsforby-catchmitigationstructuredaccordingtothemitigationhierarchyforfourcase-studies

Fram

ewor

k st

ep

Cas

e- st

udy

Alb

atro

sses

lon

glin

esTu

rtle

slo

nglin

esRa

ysp

urse

sei

nes

Oce

anic

whi

tetip

slo

nglin

es

Definingtheproblem

Fisheryandspatial

extent

Braziliandomesticindustrialcoastallongline

fleet

EasternPacific(coastalandpelagic)

small-scalecommerciallonglinefishery

Tunapurse-seinefisheryof

theeasternPacific

AsianandEUlonglinetunafisheriesinthe

Indi

an o

cean

Targetspecies

Variousspeciesofsharkandswordfish

Mahi-mahi(

Cory

phae

na h

ippu

rus

Coryphaenidaeseasonal)tunasharks

(mostlysilkyC

arch

arhi

nus f

alci

form

is

Carcharinidae)billfish

Variousspeciesoftuna

Variousspeciesoftuna

By-catchspeciesof

conc

ern

Albatrossamppetrelspeciesparticularconcern

forcriticallyendangeredTristanalbatross

(Dio

med

ea d

aben

nenaDiomedeidae)

Oliveridley(L

epid

oche

lys o

livac

ea

Cheloniidae)greenblack(C

helo

nia

myd

asCheloniidae)hawksbill

(Ere

tmoc

hely

s im

bric

ataCheloniidae)

loggerhead(PeruandMexico)and

leatherback(D

erm

oche

lys c

oria

cea

Cheloniidae)

Sevenmobulidspecies

includingCITES-listedM

anta

bi

rost

ris(Mobulidae)and

M a

lfred

i(Mobulidae)

caughtmostlyalivein

dolphin-associatedor

free-schoolsets

OceanicwhitetipsharkVulnerableonIUCN

redlistretentionbannedbytunaRFMOs

listedonCITESAppendixII

By-catchtarget

(Δλ T)

BraziliangovernmentMinimizeby-catch

Rulesfocusontargetsforuseofminimizing

measuresratherthanonby-catchnumbers

NotwelldefinedRFMOssuggest

minimizingby-catchCouldconsiderPBR

foroliveridleyszerocatchforleather-

backs(reflectingtheirrespective

populationstatus)

IATTC(2015)zeroretention

storingorsellingandlive

releaseofby-caughtrays

whenpossibleImplies

by-catchminimization

Targetby-catchlevelnotdefineddueto

uncertaintyRFMOsbanretentionlanding

andtrans-shipment

Mitigationhierarchyelement

Avoid

[timeareaclosuresnight-timesetting]

[timeareaclosuresdeeperlines]

[timeareaclosures]

[deepsetting]

Minimize

[torilineslineweights]

[monofilamentlinecirclehooks(not

leatherbacks)]

ndash [hardtoavoidcatching]

[monofilamentlinecirclehooksbanon

steelleaders]

Remediate

ndash [hardtoreleasealive]

[improvedhandling]

[improvedhandling]

[shortsets]

Offset

[invasiveeradication]

[beachprotection]

[illegaltrade]

[informationgatheringillegaltrade]

Factorsaffectingoperationalization

Scopefor

incentives

Participatoryresearchonbarrierstouptakeof

minimizationmeasuresPositiveincentives

forthoseusingnewmeasurespaidforby

forexamplefisheries-widelevy

Certificationsustainabilitystandardsin

exportmarkets

Transitionalpaymentsto

promotebetterhandlingon

deckhenceimproving

survival

Ifinformationgatheringseenasavalidoffset

duetohighuncertaintyfundingatagging

schemecouldincentivizefisherstocollect

dataonsharkcatchratesurvivalof

releasedsharksby-catchhotspotsto

supportimprovementsacrossthewhole

mitigationframework

(Continues)

emspensp emsp | emsp7MILNER- GULLAND Et AL

themitigationhierarchy In theabsenceofhighqualitypopulationdatawithwhichtoparameterizeamodelaPBR-basedapproachisbeingusedtosetatargetby-catchlevel intermsofnumberof in-dividualsofeachoftheturtlespeciescaughtinthefisheryExpertopinionfromfishersandProdelphinusstaffsupplementedbydatafromalong-runningby-catchobserverprogrammeoperatingoutoftheport(Alfaro-Shiguetoetal2011)givesthepotentialreductioninturtleby-catchnumbersasaresultofagivenmitigationapproachInterviews and focus groups with fishers provide understandingof their preferences for different by-catchmitigation approachesbarriers and constraints to implementation and potential partici-pationindifferentincentiveschemesthiscanbesupplementedbyDiscreteChoiceExperimentsprovidingempiricalestimatesforpref-erencesforcombinationsofby-catchreductionmeasures(cfRogers2013)Thisfieldresearchproducesashort-listoffeasiblemitigationmeasuresateachstageinthemitigationhierarchyforcostingandtesting(egspecificareasortimesforfisheryclosureunderavoid-ancecombinationsofhooktypesandnetmodificationundermini-mizationtraininginturtlehandlingandreleaseforremediationandimprovingby-catchperformanceofothergeartypesintheareaforoffsetting)Thisenablestheanalysisoftheeffectivenessandcostof various combinations of by-catch reduction strategies framedwithinthefourstepsofthemitigationhierarchy(avoidminimizere-mediateoffset)withacleartargetby-catchreductiongoalinmind

4emsp |emspCOMPARING KE Y DEBATES BET WEEN TERRESTRIAL NNL AND BY- C ATCH MITIGATION

41emsp|emspThe hierarchical nature of mitigation

Terrestrial situationsareusuallyviewedas requiringastricthierar-chywithavoidanceminimizationandremediationtakingprecedenceoveroffsetsPartofthereasonforthishierarchymaybesocietalval-uesandexpectationsbut also it is a reflectionof reversibility anduncertaintyTheterrestrialmitigationhierarchywassetuptoaddresshabitatdestructioncausedbydevelopmentwhich iseffectively ir-reversiblehenceavoidanceisstrictlypreferredfromaconservationperspective Inpractice avoidancehasbeenaneglected step andmuchofthedisquietaboutbiodiversityoffsettinghasbeenbecauseofthetendencytopaylipservicetoavoidanceandfocusinsteadonoffsetswhich thenmay be implemented on paper only (HoughampRobertson2009Phalanetal2017)EvenwithperfectenforcementandcompliancewithmeasuresfurtherdownthemitigationhierarchythestrictavoidanceofhabitatlossismorecertaintolimitimpactthanreducinglossesinthecourseofapotentiallydamagingactionwhichismorecertainthanrestoringdamageafterthefactorcompensatingforitwithactionselsewhereOfteninterrestrialsystemsmultipliersareusedattheoffsetstagetoreflectthisuncertaintyrequiringthatanadditionalamountofequivalentlandisprotectedinanoffsetoverandabovetheamountthatislostduringthedevelopment(withtheratiooflandoffsettolanddestroyedinthe10sto100sdependingonthecircumstancesMoilanenVanTeeffelenBen-HaimampFerrierFr

amew

ork

step

Cas

e- st

udy

Alb

atro

sses

lon

glin

esTu

rtle

slo

nglin

esRa

ysp

urse

sei

nes

Oce

anic

whi

tetip

slo

nglin

es

Major

uncertainties

Lackofspecies-levelidentificationof

by-catchlackofunderstandingof

compliance

Lackofecologicalknowledgeofturtle

populationtrendsampdistribution

Potentialforsignificantadditional

by-catchfromcoastalgillnetfishery

Impactofcatchonmobulid

survivalPredictorsof

mobuliddistributions

Lackofobserversorreportingsoverylimited

understandingofby-catchlevelsspatio-

temporalencounterhotspotspost-release

survivalcompliance

Keyobstacle

Compliancewithexistingrulesmustbe

improved

Fundingforalternativestofishingata

largeenoughscaleLongtimelagand

uncertaintyinoffseteffectiveness

Limitedknowledgeofmobulid

distributionsmakes

avoidancedifficult

Lackofmonitoringlimitsoptions

Overallassessment

Existingmeasuresforimprovingimplementa-

tionofminimizationstepalreadyexistbut

needincentivizingoffsettingcouldprovide

short-termgainstocomplementthese

Targetedfundingcouldfacilitateimprove-

mentsthroughoutthehierarchyBest

approachmaydifferbyspecies(particu-

larlyleatherbacksvsothers)

Focusonremediationstepis

currentlythemainoption

avai

labl

e

Somepotentialforminimizationthrough

deepsettingbutchallengingtochange

behaviourinthisfisheryelectronic

monitoringsystemswouldhelp

Keyreferences

BugoniManciniMonteiroNascimentoamp

Neves(2008)Wanlessetal(2009)

Alfaro-ShiguetoDuttonampMangel(2007)

Halletal(2012)Andrakaetal(2013)

JonesampFrancis(2012)Hallamp

Roman(2013)Crolletal

(2016)Fowler(2016)

Tolottietal(2015)

Ticksindicatethepotentialforactionatdifferentstepsofthehierarchybasedonfeasibilitycurrentknowledgeandimpactonmortality(

=highpotential

=somepotential

=limitedpotential

ndash=nopotential)TextinbracketsgivessuggestedmeasuresateachlevelofthehierarchytheseareillustrativeratherthandefinitiveTheinformationforthecase-studiesisbasedontheexpertknowledge

oftheauthorsthroughtheirinvolvementinmanagementoftheby-catchissueinthesefisheriesRFMOregionalfisheriesmanagementorganizationPBRpotentialbiologicalremoval

TABLE 3emsp(Continued)

8emsp |emsp emspensp MILNER- GULLAND Et AL

2009)Bycontrastinfisheriessettingstherehavebeensuggestionsthatdependingonthelegalenvironmentitmaybemoreappropriateforoffsetstobeusedaspartofaleast-costconservationapproachalongsidemoretraditionalmitigationmethodsratherthanasthelaststep inamitigationhierarchy (DuttonJosephSquiresampWilliams2011DuttonampSquires2008WilcoxampDonlan2007)

42emsp|emspOut- of- kind offsets

Out-of-kind offsets are those which do not act to increase theimpact-affectedbiodiversityIntermsofourconceptualframeworktheyareoffsetswhichdonotacttoincreasethepopulationgrowthrateoftheby-catch-affectedfocalpopulation(Equation1)Forex-ampleonesuggestedbenefitof raising funds foroffsetting fromaby-catchtaxonfishersisthattheproceedsfromsuchataxcanfinanceoffsetselsewherewithintherangeoftheby-catch-affectedpopulation (Dutton amp Squires 2008) Although not a true offsetunderamitigationhierarchyfundsfromtheCaliforniadriftgillnetindustry in 2002 financed sea turtle nesting site conservation inBajaCaliforniaforcompensatorymitigationofseaturtleby-catch(Jannise Squires Seminoff amp Dutton 2010) In terrestrial (andmarine)systems itcanbemorechallengingtodefinethe impact-affected biodiversity because impact is rarely as clearly linkedtoagivenspeciesandstockas it is forby-catchBecauseofthisthelocationandbiodiversitytargetofconservationactionsfallingundertheldquooffsetrdquoheadinghassometimesbeenlooselyrelatedtotheactual impactBest-practicestandardsstatethatoffsetsmustbeimplementedasclosetothedamagingactivitiesaspossibleandfocusonbiodiversityassimilaraspossibletothatwhichhasbeenimpacted (BBOP 2012) However there have also been calls forldquoout-of-kindrdquooffsetsthatgivemoreconservationbang-for-buckbyfocussingonthreatenedspeciesorrarehabitatsorareasinneedofconservation rather than the impactedareasor specieswhichmay be considered less ldquovaluablerdquo for conservation (Bull Hardyetal2015)Thishasledtosubstantialdebateastotheappropri-atelimitsonthegeographicscaleandbiodiversityfocusforoffset-ting(egApostolopoulouampAdams2017)Italsodrawsattentiontothesubjectiveanduser-definednatureof theword ldquobiodiversityrdquo(Morar ToadvineampBohannan 2015) As it is impossible fully tooperationalizetheconceptimplementersofthemitigationhierar-chyhavelatitudetointerpretbiodiversityaccordingtoforexampleeaseofmeasurement perceived societal valueormitigation cost(Maron etal 2016) In our casewe take a narrow focus on theby-caughtspecies itself this is in linewithmuchof the literatureon by-catch but notwith the broader discourses on ecosystem-basedapproachestomarinemanagementandecosystemservices(RosenbergampMcLeod2005)Thesediscoursessuggest theneedforamorefunctionalecosystem-basedapproachtononetlossofbiodiversitythishasyettotranspireeitherinthemarineorintheterrestrialliteraturepossiblybecausesubstantialchallengesinde-finingimpact-affectedbiodiversitytheninevitablyensue

Asmarinemegafauna stocks are often transboundary andmi-gratorydefiningtheappropriatespatialunit foroffsettingmaybe

achallengebecause themosteffective location foranoffsetmayormaynotbewithintheareaofinfluenceofagivenfisheryClearlyandpreciselydefining the spatial unitwithinwhich themitigationhierarchywill be implemented during theprocess of defining theoverallgoal(suchasNNL)isvitalThisunitshouldreflectthescaleoverwhichanactionwillaffectλToffsetswhicharewithinthedis-tributionofthefocalstockoftheby-caughtspecies(asdefinedforEquation1)arenotout-of-kindHoweverchallengesemergewhenthe appropriate spatial unit for offsetting activities is different totheappropriatespatialunitforotherelementsofthemitigationhi-erarchywhicharelikelytobedefinedinsteadbyjurisdictionalareaor target fish stock distribution Inmany fisheries the species af-fectedbyby-catchmaynotbewellenoughknownandoffsetsmayaccordinglyneedtobebroadlytargetedtobenefitanypotentiallyaffectedspeciesTrueout-of-kindoffsetswouldincludefundingtheconservationofunaffectedspeciesorstocksofhabitatsnotusedbythefocalstockorcontributionstoaconservationfundwithoutaclearcommitmentthatthefundsaretobespentonincreasingλT for thefocalby-caughtstockTheseareunlikelytoformpartofbest-practiceguidanceforby-catchoffsets

43emsp|emspResearch as an offset

Arelatedareaofactivecontroversyformarineby-catchiswhetherresearchor informationgatheringshouldbeseenasavalidoffsetmechanism The rationale is that this research could be used toreduceuncertaintypromote innovationand thereby improveout-comes for by-caught species albeit indirectly An offset could beusedto incentivizebetterdatacollectionfor instanceusingaby-catchlevytopayfortaggingortoputby-catchobserversorelec-tronicmonitoringsystemsonboatsThismightbeapreludetolatermitigation or avoidance activities once more is known about thebiological settingWhether research activities could appropriatelybeconsideredaspartofanldquooffsetrdquoiscontroversialmdashinsomecasesan indirectbenefit to theby-caught stockmightbe clearly appar-ent(egtheoceanicwhitetip(Carcharinus longimanusCarcharinidae)case-studyinTable3)whileinothercasesusinginvestmentinre-searchasanoffsetcouldbeseenasacaseofmoralhazardpoten-tially compromising scientistsrsquo independence and having at best ahighlyindirectrelationshiptoNNLoftheby-caughtspeciesAnotherviewisthatreducinguncertaintyisacoreresponsibilityofoperatingafisherywhichthereforeshouldbebornebythemanagementau-thorityorfishingbusinessesInterrestrialsystemsthesedilemmasalsoexistbutthesentimentismuchmoreclearlyexpressedthatre-searchactivitiesarenotappropriateoffsets(BullGordonWatsonampMaron2016)

44emsp|emspIncentivizing implementation of mitigation measures

Thefactorsthatdrivedecision-makingaboutmegafaunaby-catchreduction (by skippers companies fishery managers policymak-ers and other stakeholders) include legal obligations tominimize

emspensp emsp | emsp9MILNER- GULLAND Et AL

by-catch at the national or international levels (eg FAO 2011Rice 2014) the availability and quality of technical fixes associ-atedcosts tofishers limitsonaccesstoseafoodmarketsaswellassocietalpressuresHowevermuchresearchonby-catchreduc-tion focuses on identifying and implementing technicalmeasuresto reduceBPUE rather thanon the social andeconomicbarriersto implementation (Campbell amp Cornwell 2008) Technologicalinnovation to improve BPUE needs to be appropriately incentiv-izedwitheffortsmadetoensurethatsuchmeasuresareascost-effective as possible for fishers (Gjertsen Hall amp Squires 2010Lent amp Squires 2017) However it often happens that even ap-parently suitable by-catchmeasures are notwidely implemented(eg Damalas amp Vassilopoulou 2013 Orphanides amp Palka 2013RadzioSmolinskyampRoosenburg2013)Inthesecasesthedegreeofnon-implementationandthereasonsbehinditneedstobeun-derstoodsoitcanbeaddressed(Coxetal2007)Thesetypesofconsiderationarealsonotwellresearchedintheterrestrialoffset-tingliteraturebecausecomplianceispoorlymonitored(BullSuttleGordonSinghampMilner-Gulland2013)andthereislittlesupportfor researchon thebarriers to implementationofamitigationhi-erarchyandhowtosupportdeveloperstoaddressthesebarriers(BullBryantBakerampMilner-Gulland2015)Thesocialimpactsofimplementingabiodiversitymitigationhierarchyonresourceusersarementioned inguidance (egBBOP2012)buthowtomeasureandaccountforthemisverypoorlyunderstoodThefewstudiesin-vestigatingdeliveryofpromisedoffsetmeasuresinterrestrialsys-temssuggestaverypoorrecord(QueacutetierRegneryampLevrel2014)Therefore the social side of implementing the mitigation hierar-chyand incentivizingcompliance isanarea thatneedsmore andmoreactiveresearchwithinboththeterrestrialandmarinerealms(FultonSmithSmithampvanPutten2011)Thisisparticularlytruewhentheburdenof implementingmitigationapproaches isbornebyrelativelysmall-scaleproducersratherthangovernmentsormul-tinationals(egthepelagiclonglinefisheriesinTable3)

45emsp|emspSocietal limits

Foraspeciesathighriskofextinctioncompleteavoidanceofby-catchmightbethemostdesirablepolicyfrombothamanagementagency and societal perspective In addition with emblematic orhighlythreatenedmarinemegafaunaitmaybeviewedbymembersof the public asmorallywrong to kill any individuals even ifmiti-gationisinplace(egMauirsquosdolphinHamneretal2014) leadingtopressureongovernmentstoreflectthisethicalconcerninregu-lationsThesedilemmasecho the issueof thresholds in terrestrialoffsetswhichrecognizesthattherearesomecriticalareasinwhichdevelopmentisnotsocietallyappropriateregardlessofthepoten-tialformitigationandotherareasinwhichthemitigationhierarchycan be appropriately applied (Bull etal 2013) Examples of loca-tionswhereathresholdapproach isseenasappropriate interres-trial systems include the habitat of highly endangered species orecosystemswhich are limited in extent and irreplaceable (such asoldgrowthforest) In terrestrialsystems therefore themitigation

hierarchyisseenasmostappropriateforapplicationinmorecom-monanddegradedhabitatssuchasfarmlandSimilarlyinfisheriestheremaybesomesituationsinwhichthestockssubjecttoby-catchare so precious or threatened that no level of threat from fishingcanbecontemplatedandotherswherefishingsubjecttoNNLandthemitigationhierarchyisasociallyacceptableapproachInsitua-tions inwhich trade-offs between conservation and developmentareseenasnecessaryoracceptablebywidersocietyasociallicencetooperatemaybegainedthroughadoptingoffsetsintheabsenceofregulationForexampleinsub-SaharanAfricaseverallargedevel-opmentprojectsareattemptingtooffsettheirimpactsongreatapesandtheirhabitats(Kormosetal2014)Aby-catchequivalentmightbe fishing companies voluntarily donating funds for turtle nestingbeachrestorationintheirareaofoperationinadditiontocomply-ingwithregulatoryby-catchmitigationmeasuresThesemeasuresmayimprovetheimageofthecompanywiththegeneralpublicbuttoavoidaccusationsofldquogreenwashingrdquotheireffectivenessneedstobeproperlyscrutinized(Bulletal2016)Transparentlyembeddingthesetypesofactionswithinamitigationhierarchysuchasweareproposing and critically evaluating their contribution to increasingthepopulationgrowthrate(asperEquation1)wouldbeonewaytopromptsuchscrutiny

46emsp|emspUncertainty

The nature of the uncertainties surrounding biology and enforce-ment in themarine setting raisesquestions about theorderingofsteps in themitigationhierarchy inaway that isdissimilar to ter-restrialsystemswherethehierarchyofuncertaintiesmaybecleareranduncertaintyisgenerallylowerForexampleitmaybethattheimpactonoverallpopulationgrowthrateofanoffsetmeasurelikeeradicating invasivespecies fromaseabirdnestinghabitat isbothless uncertain and more cost-effective than avoidance measuressuchasclosingareaswhichmayormaynotbefrequentedbyadultseabirds in a given time-periodGenerally though itmightbe as-sumedthatmeasureswhichtargetlifestagessubjecttohighlevelsofnaturalmortalityorwithinwhichindividualcontributiontoover-allpopulationgrowthrateislow(egheadstartingjuvenileturtles)maybelesseffectiveinachievingNNLthanmeasureswhichtargetreproductivelymatureadultfemales(suchaslivereleasesHeppellCrowderampCrouse1996)Howeverbeforeimplementinganoffsetthataimstoimprovethesurvivalofonelifestageinordertocom-pensatefortheby-catchmortalityofanotherarobustassessmentoftheconsequences(withassociateduncertainties)shouldbecar-ried out through detailed population modelling based on strongempiricalstudies(cfWallaceHeppellLewisonKelezampCrowder2008)Interrestrialsystemstherequirementsequentiallytoapplythemitigationhierarchyisbroadlyunchallengedbutactuallysimilararguments apply For example habitat restoration sits above off-settinginthehierarchyandyetitisalong-termuncertainprocesswhichmayinsomecircumstancesbemuchlesspreferabletoanoff-setusingawell-establishedapproachwhichishighlylikelytoleadtoconservationgains

10emsp |emsp emspensp MILNER- GULLAND Et AL

47emsp|emspTemporal considerations

Thetimingofoffsetsinrelationtootherelementsofthemitigationhierarchyhasbeenthesubjectofdebatewithintheterrestriallitera-tureThemainsuggestionforaddressingthetemporarylossofbio-diversitywhileoffsetscometofruitionhasbeenadoptingmitigationbankingwherebyoffsetsareimplementedinadvanceofpotentiallydamagingactivitiesprovidingbiodiversitycreditswhichcanbeusedtocompensateforlaterlossesThisbothremovesanelementofun-certaintyfromtheoffsetimplementationandreducesthetimelagbetweenlossandgain(Mann2015)Withrespecttomarinemega-faunaby-catchflexibilityintimingprovidesadditionalscopeforcostreduction and benefit enhancementwhichmay not be present intraditionalhabitat-basedterrestrialoffsetsForexampletemporarymeasuressuchasashort-termby-catchtaxtofundanoffsetmaybeusedifmitigationoravoidancemethodstaketimetocomeonlineorifatemporarynudgeisenoughtocausebehaviouralchangeThismightbethecaseifapolicywasneededtoinducefisherstotakeupnewgeartoavoidthecostofanoffsetorifconcernsaboutsafetyoryieldreductionsduringthetransitiontonewgearcouldbeallayedbyatemporarysubsidyforearlyadoptersorapaidparticipatorymoni-toringprogrammeto informwider implementation(egthemobu-lidandsharkcase-studiesinTable3)Justasforhabitatrestoration(ZedlerampCallaway 1999) by-catchoffset strategieswhich targetjuvenilestagesof long-livedspecies (eg turtleheadstartingor in-vasive removal fromseabirdnesting islands)may takemanyyearsfor their effects to become apparent in an increase in populationgrowthratesAdditionaluncertaintyisintroducedbythedifficultyinmonitoringpopulationsofmanyby-catch species (eg seabirdsHatch2003)leadingtouncertainestimatesoftheimpactofoffsetactivitiesonpopulationgrowth(seecase-studiesinTable3)Theseproblemsarenot insuperablehoweverpositivetrendshavebeenreportedinturtlepopulationsoverdecadesasaresultofnestpro-tection(egDuttonDuttonChaloupkaampBoulon2005)

5emsp |emspUSING INCENTIVES TO REDUCE BY- C ATCH

Manyoftheexamplesandprinciplesdiscussedaboveeitherimplic-itlyorexplicitlyrelatetotheeconomicsocialinstitutionalormoralincentivesoperatingondifferentactorsinsideandoutsidethefish-erywhichcanbepositiveornegativeWenowturntoadiscussionofhowincentivescanbeusedtoreduceby-catchwithinourframe-workIncentivescanbeputinplacetochangefisherbehaviourwithrespecttoanyoftheelementsoftheframework (avoidminimizeremediateandoffsetTable3)Althoughdiscussedintheliteraturemostof these incentive approaches are yet tobe implemented inthe realworldparticularly forby-catchThereforeuntil empiricalevidenceoftheireffectivenessisavailablethesesuggestionscomewithacaveat

Financial costsofby-catchmitigationactions canarise for in-stancefromlostcatchcapitalinvestmentsinnewgearormitigation

equipmentor the lossofaccesstoafisheryCostsmayalsoarisefromthedeploymentofby-catchobserversortrainingintheuseofnewgearThesecostscanbepaidbyfishingcompaniesorindivid-ualsorbygovernmentsNGOsorseafoodconsumersWhetherornotcompensationforcostsincurredbyfishersisseenasappropri-atedependsonwhetherby-catchreductionisseenasasocialgoodthatfishersareproviding(inwhichcasetheyshouldbecompensatedforit)orasputtingrighttheharmthattheyaredoingtobiodiver-sitywhilegeneratingtheirownprivategain(ineconomiclanguagewhetherby-catchisviewedasanunpricedexternalityinwhichcasetheyshouldpay)Italsodependsonwhethereconomichardshipwillensueacaseforcompensationofby-catchreductioncostsincurredbypeopledependenton fishing for their livelihoodsmaybemoresympatheticallyreceivedbyotheractorsthanacasemadebyalargemultinationalfishingcompany

Ifby-catchisseenasanunpricedexternalityitmightbesociallyoptimaltotaxfishersfortheirby-catchsothatthisexternalityisin-ternalizedThisplacesanexplicitpriceuponby-catch(Boyce1996Pascoeetal2010SquiresampGarcia2014)Theby-catchprice islikely to be incorporated into the price of the target species andtherebybecomespartofthetargetspeciescostThispricecouldbeset differently for different demographic classesof theby-caughtspecies depending on the impact the loss of an individualwouldhaveonthepopulationAllelsebeingequalputtingapriceonby-catchmeans that theseafoodproduct that is the targetcatchbe-comesmoreexpensiveandconsumershave topaymore for theirseafoodreducingdemandTheninprincipleeveryfirminthesup-plychaineveryvesselandeveryconsumerhaveanincentivetore-duceby-catchuntileacheconomicactorrsquosmarginalcostofby-catchreductionequals thecommonpriceofby-catch that theyall faceOffsetsareonewaytopriceandinternalizetheby-catchexternalitycostIfanoffsettingactioniscostlytoimplementandmustbepaidforwith each unit of by-catch it implicitly prices the residual by-catch In this circumstance the effect from a financial standpointisthesameasaby-catchtaxwiththe levelsetbasedonthecostoftheoffsetVariousinstitutionalstructurestosupportthischargeperunitofby-catcharepossiblewithdifferentimplicationsintermsofthedistributionofcostsandbenefitsForexampleaninsuranceschemecouldbepaidintobyfishersthatpaysoutintheeventofaby-catcheventtherebyspreadingthecostofunavoidablerareby-catcheventsOratradablepermitschemecouldoperatesuchthatfisherswhoexperienceaby-catcheventcanbuyapermitwiththecostvaryingdependingondemandforpermits (henceprovidingavessel-levelincentivetoinnovatetoreduceby-catch)

If there isdemandforconservation inan internationalmarketthen price premiums and market access (through eco-labellingsupply chain certification other food sustainability campaignsWardampPhillips2010)orboycottsactingasstrategicthreatsfromconsumers (Kotchen 2013 Segerson 2010) could act as positiveornegativeeconomic leversonthe fisheryprovidingan incentivefor fishers to reduce their by-catch voluntarily (as has been sug-gested for the Brazilianmahi-mahi fishery Table3) For exampletheMarine StewardshipCouncil now includesby-catchmitigation

emspensp emsp | emsp11MILNER- GULLAND Et AL

intheircertificationprocess(MSC2014)Demand-ledleversmaybemoreorlessapplicableatdifferentlevelsinthehierarchyforexam-pleavoidancemayberelativelyhardtoevidencewhileoffsettingmaybelesseasytoselltoaconsumerthanminimizationorreme-diationConcerns about the unintended consequences of positiveincentives (particularlyfordirectsubsidiesratherthanconditionalincentives)maydeterminewhethertheyareanappropriateinstru-mentinagivencaseForexampletheymaybeinappropriateifthereisariskthattheadditionalmoneyisreinvestedinincreasedfishingcapacityor iftheremaybeconsumptionproductionorconserva-tionleakages(transferoftheproblemsomewhereelse)whetheratthe vessel fishery or trans-national levelHigh transactions costsmayalsolimitthebenefitsofincentivesschemes

Otherchangeswhichmayneedtobeincentivizedforsuccessfulimplementationofby-catchreductionpoliciesmaybelessamenabletofinancialmeasuresatleastpartlybecauseitislessclearhowtoassign financial value to theactionsor to thebenefits and losseswhichtheyproduceForexampleperceivedreductionsinsafetyforfishingcrews(fromweightedlonglinesfor instance)arecoststhatmaybehardtovaluefinanciallyOtherprerequisitesfor long-termsustainable behaviour change such as changes in social norms sothatfishingcommunitiesseeby-catchreductionasappropriatebe-haviourortechnicalskillacquisitionsothattheycanusenewmeth-odsmaybeincentivizedbycarefullydesignedinterventionsworkingwithfishers(Halletal2007)Conservationpoliciesbasedoneco-nomic incentives (extrinsicmotivation) are not always superior tothosebasedupon intrinsicmotivation Infact incentive-basedby-catch reduction policy instruments could even be counterproduc-tivebyreducingtheeffectivenessofintrinsicmotivationdependingupon the situation (although the empirical evidence on this topicisweak RodeGoacutemez-BaggethunampKrause 2015) If the changerequiredforby-catchreductiontoworkmeetscultural resistancethenparticipatory researchmightbeespeciallyeffective inbreak-ingdownbarriersbetweenthosewhowantby-catchreductiontotakeplaceandthosewhoactuallyhavetoimplementit(thefishers)ForexampleinAustraliathegovernment-fundedbodyOceanwatchfacilitatesengagementbetweencommunities thefishing industryseafood suppliers and government to improve knowledge sharing(wwwoceanwatchorgau)Innovationiscrucialinfisheriesandfish-ersareaccustomedtoadoptingnewtechnologyorprocessespo-tentiallymakingan incentivizedparticipatory researchprogrammeespeciallyfruitful

Sometimes the most efficient way to solve problems is a so-cial instrumentoran institutionalchange inplaceoforaswellasan economic instrument For example supporting developmentof fisherorganizations rather than instituting a vessel-level taxorsubsidy might provide the impetus needed to change behaviourInstitutingcatchshares(individualtransferablequotas)mayprovideanenablingenvironmentforby-catchreductionforexamplebypro-motingmoreeffectivemonitoring(Grimmetal2012)Experiencein terrestrial system produces similar insights incentive-basedschemeswhichalsobuildcommunitycohesionandsupportthede-velopment or strengthening of localmanagement institutions are

more effective in the longer run than direct economic incentives(Clementsetal2010)

6emsp |emspCONCLUSIONS

The framework we present here is novel It draws upon and ex-tends the frameworks for conceptualizing by-catch developed byHall (1996) and Hall Alverson andMetuzals (2000) It amalgam-atesHallrsquos frameworkwith themitigationhierarchyasused in theEnvironmental Impact Assessment literature (BBOP 2012) Thesuggestions about goals metric andmitigation actions are drawnfromtheempiricalby-catchliteratureandtheissueswediscussin-tegratetheconcernsoftheextensiveterrestrialandnascentmarineoffsetting literature with the by-catch literature The frameworkmakesclear thatanearlycrucial step is toclarify thegoalofanyby-catch reduction policyOverarching goals like those issued bytheConventiononBiologicalDiversity(egAichiTarget11that10ofmarinehabitatshouldbeunderprotectionby2020)needtobetranslatedintooperationaltermswithineachfisheryCurrentlyleg-islatedoragreedby-catch reductiongoals tend tobe less specificthantheycouldbeandthisleadstoproblemsininterpretingthesegoals inordertoplanaby-catchmitigationstrategy(seethecase-studies inTable3 for examples) This ambiguity is tobe expectedwithinnegotiatedtargetsbutitisachallengenonetheless(Maxwelletal2015)Usingacommonunitofby-catch impactsuchastheΔλTwhichweuseherewouldbehelpfulbothinclarifyingexpecta-tionsandevaluatingtheeffectivenessofelementsofthemitigationhierarchy

Once the by-catch goal is known options for implementingavoidanceminimizationremediationandoffsetscanbeclarified(asinTable2)Howeveroutsideof the interconnectedbiologyof theecosystemby-catch isembeddedwithinsocialandeconomicsys-temsDifferentunitsofanalysismaybeneededatdifferent levelsofthehierarchytocopewiththechallengesofincompleteoverlapbetween jurisdictional units fisheries target stocks and by-catchstocksJurisdictionalissuesareimportantandcomplexpotentiallyimpeding implementationFleets interact raisingtheriskofpolicyleakageforexampleifpeopleshifttootherfisheriesgearorliveli-hoodsThereforethescaleatwhicheachelementofthemitigationhierarchyisimplementedislikelytovarywithincentivestomitigateoftenbeingbest appliedat thevessel level focussedon reducingindividualmortalitywhileoffsettingisimplementedatthescaleoftheby-catchspeciesrsquostockWithtransboundaryspeciesunilateralconservationinonejurisdictioncreatesthepotentialforproductiontrade and conservation leakages For example a conserving Statecouldimplementtheavoidancestepandshutdownordramaticallycurtailitsownproductionofswordfishtoreduceseaturtleby-catchbuttheknock-oneffectmaybemoreimportationofswordfishfromfleetswithhigherseaturtleby-catch(RausserHamiltonKovachampStifter2009)

Translatingtheframeworkfromaspeciestoanecosystemlevelwill require consideration of the potential interactions between

12emsp |emsp emspensp MILNER- GULLAND Et AL

by-catchmitigationapproachestargetedatdifferentspecies(Serafyetal 2012) Actions to mitigate by-catch for one group of spe-cies can increase or decrease it for others and so a system-wideapproach isneededForexample changing fromJ-hooks tocirclehookstoreducemortalityofturtlesmaydecreaseorincreasesharkmortality(Andrakaetal2013GodinCarlsonampBurgener2012)In terrestrial systems similar interactions arise and value judge-mentsaremade(whetherexplicitlyorimplicitly)astowhatlossandgain of ldquobiodiversityrdquo translates to in operational terms andwhatelementsofbiodiversitymattermosttoimplementers

Uncertainty is high in ocean ecosystems creating both chal-lengesandopportunitiesinapplyingtheconceptofNNLthroughamitigationhierarchythatincludesoffsettingInparticularformarinemegafaunathereishighuncertaintyintheprocesseslinkinganyel-ementofthemitigationhierarchythroughtochangesinpopulationgrowthrateFurthermore impactscanbelong-termhardtomea-sureandspatiallydiffuseanduncertaintyisnotpredictablyspreadthroughthehierarchyThiscreatesadifferentsetofchallengestothosefacedinterrestrialsystemswhereatleastforsometypesofenvironmentalimpactthelinksbetweenactionandimpactarerel-ativelydirectandmeasurableanduncertaintygenerally increasesthroughthemitigationhierarchy (fromavoidthroughminimizere-mediatetooffset)

By-catch reduction measures have had significant successesoverthelastdecadesasaresultofsubstantialinvestmentoftimeand funding by researchers management authorities conserva-tionorganizationsandfishers(Coxetal2007)Howeverthissuc-cessisnotuniversalJustasforanyfisheriesmanagementissueapoorregulatoryregimelimitedcomplianceandlackofinforma-tionhampereffortstoreduceby-catchInsomeplaceshighlevelsofby-catch limitedoptions formitigationandweakgovernance(leadingtopoorenforcement)cancombinetomaketheby-catchproblemintractableOurframeworkwillnotsolvetheseproblemsHowever itbrings together the full rangeofapproaches forby-catchmitigationinastructuredandsystematicwaywhichrequiresatargettobeexpressedagainstwhichoutcomescanbeevaluatedByexposingareasofuncertaintyanddatadeficiencyitcouldchal-lengescientistsandmanagerstoobtainthedatarequiredproperlytoevaluate theeffectivenessofmitigationmeasuresThis couldthensupportandencourageclearerdecision-makingandprioriti-zationofactionsOurframeworkdemonstratesthattheprincipleof implementing thegoalofnonet loss throughamitigationhi-erarchy isasapplicable tomarinemegafaunaby-catchas to ter-restrial systems where it is already widely used in challengingdata-poorcircumstances

There isuntappedpotential forcost-effectiveby-catchmitiga-tionwhichcouldberealizedwiththeadoptionofthisframeworkandwithconsiderationofnewapproachestoincentivizingby-catchmitigationwithinthestepsofthehierarchyApplyingittoafewcase-studiesinpracticewilldemonstrateempiricallywhereandhowthepotentialforimprovedeffectivenesscouldbestberealizedExistinglegalframeworksoftenprecludeapproacheswhichimplicitlyorex-plicitly permit by-catch including the use of economic incentives

ornewapproachessuchasoffsetsHoweverinthiscontextofdy-namicuncertaintythedividendsofthinkingmorecreativelyaboutby-catchmitigationcouldbehigh

ACKNOWLEDG EMENTS

EJMG acknowledges the Pew Charitable Foundation for its sup-port of thiswork This article originated at a 2013workshop co-organized by NOAA-Fisheries and IUCN-CEEM-FEG entitledldquoMultidisciplinaryWorkshoptoAddressEcosystem-LevelImpactsofFisheriesBycatchonMarineMegafaunaBiodiversityConservationthrough Mitigation Policy Economic Instruments and TechnicalChangerdquo We thank the reviewers for their insightful commentswhichmuchimprovedthemanuscript

ORCID

E J Milner-Gulland httporcidorg0000-0003-0324-2710

R E FE R E N C E S

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Alfaro-Shigueto JMangel JCBernedoFDuttonPHSeminoffJAampGodleyB J (2011) Small-scale fisheriesofPeruAmajorsinkformarineturtles inthePacificJournal of Applied Ecology481432ndash1440httpsdoiorg101111j1365-2664201102040x

Alfaro-ShiguetoJMangelJCPajueloMDuttonPHSeminoffJ A amp Godley B J (2010) Where small can have a large im-pact Structure and characterization of small-scale fisheries inPeru Fisheries Research 106 8ndash17 httpsdoiorg101016jfishres201006004

Andraka SMugM HallM PonsM Pacheco L ParralesM hellipOrtega D (2013) Circle hooks Developing better fishing prac-ticesintheartisanallonglinefisheriesoftheEasternPacificOceanBiological Conservation 160 214ndash224 httpsdoiorg101016jbiocon201301019

ApostolopoulouEampAdamsWM(2017)BiodiversityoffsettingandconservationReframingnaturetosaveitOryx5123ndash31httpsdoiorg101017S0030605315000782

BaacuteezJCRealRGarciacutea-SotoCJoseacuteMMaciacuteasDampCamintildeasJA(2007)Loggerheadturtleby-catchdependsondistancetothecoastindependentoffishingeffortImplicationsforconservationandfish-eries management Marine Ecology Progress Series 338 249ndash256httpsdoiorg101017S0030605315000782

BBOP (2012) Standard on biodiversity offsets Business and biodiversity offsets programmeWashingtonDCForestTrends

Bishop J (2006) Standardizing fishery-dependent catch and ef-fort data in complex fisheries with technology change Reviews in Fish Biology and Fisheries 16 21ndash38 httpsdoiorg101007s11160-006-0004-9

BoyceJ(1996)AneconomicanalysisofthefisheriesbycatchproblemJournal of Environmental Economics and Management31 314ndash336httpsdoiorg101006jeem19960047

BugoniLManciniPLMonteiroDSNascimentoLampNevesTS(2008)SeabirdbycatchintheBrazilianpelagiclonglinefisheryandareviewofcaptureratesinthesouthwesternAtlanticOceanEndangered Species Research5137ndash147httpsdoiorg103354esr00115

emspensp emsp | emsp13MILNER- GULLAND Et AL

BullJWampBrownlieS(2017)Thetransitionfromnonetlosstoanetgainof biodiversity is far from trivialOryx51 53ndash59 httpsdoiorg101017S0030605315000861

BullJWBryantCBakerJampMilner-GullandEJ(2015December28)Developing measuring and communicating the outcomes of cor-porate biodiversity strategies [pdfdocument]RetrievedfromhttpwwwwildbusinessorgBull_etal_2015_WBLpdf

BullJWGordonAWatsonJEampMaronM(2016)Seekingcon-vergenceonthekeyconceptsinlsquononetlossrsquopolicyJournal of Applied Ecology531686ndash1693httpsdoiorg1011111365-266412726

BullJWHardyMJMoilanenAampGordonA (2015)Categoriesof flexibility in biodiversity offsetting and their implications forconservation Biological Conservation 192 522ndash532 httpsdoiorg101016jbiocon201508003

Bull JW Lloyd S P amp StrangeN (2017) Implementation gap be-tween the theory and practice of biodiversity offset multipliersConservation Lettershttpsdoiorg101111conl12335

Bull JW SuttleKBGordonA SinghN JampMilner-Gulland EJ(2013)BiodiversityoffsetsintheoryandpracticeOryx47369ndash380httpsdoiorg101017S003060531200172X

CampbellLMampCornwellML(2008)Humandimensionsofbycatchreduction technology Current assumptions and directions for fu-tureresearchEndangered Species Research5325ndash334httpsdoiorg103354esr00172

Caswell H Brault S Read A J amp Smith T D (1998) Harborporpoise and fisheries An uncertainty analysis of inciden-tal mortality Ecological Applications 8 1226ndash1238 httpsdoiorg1018901051-0761(1998)008[1226hpafau]20co2

ClementsTJohnANielsenKAnDTanSampMilner-GullandEJ (2010)Payments forbiodiversityconservation in thecontextofweak institutions Comparison of three programs from CambodiaEcological Economics 69 1283ndash1291 httpsdoiorg101016jecolecon200911010

CoxTLewisonRŽydelisRCrowderLSafinaCampReadA(2007)ComparingeffectivenessofexperimentalandimplementedbycatchreductionmeasuresTheidealandtherealConservation Biology211155ndash1164httpsdoiorg101111j1523-1739200700772x

CrollDADewarHDulvyNKFernandoDFrancisMPGalvaacuten-Magantildea F hellip Newton K M (2016) Vulnerabilities and fisher-ies impactsTheuncertain futureofmanta anddevil raysAquatic Conservation Marine and Freshwater Ecosystems 26 562ndash575httpsdoiorg101002aqc2591

Damalas D amp Vassilopoulou V (2013) Slack regulation com-pliance in the Mediterranean fisheries A paradigm from theGreek Aegean Sea demersal trawl fishery modelling discardogives Fisheries Management and Ecology 20 21ndash33 httpsdoiorg101111j1365-2400201200860x

DuttonDLDuttonPHChaloupkaMampBoulonRH(2005)IncreaseofaCaribbeanleatherbackturtleDermochelys coriaceanestingpop-ulation linked to long-termnestprotectionBiological Conservation126186ndash194httpsdoiorg101016jbiocon200505013

DuttonPJosephJSquiresDampWilliamsM(2011)Bellagioblue-print foractiononseaturtlesChapter2 InPDuttonDSquiresampM Ahmed (Eds) Conservation of pacific sea turtles (pp 15ndash36)HonoluluHIUniversityofHawaiiPress

DuttonPampSquiresD (2008)AholisticstrategyforPacificseatur-tlerecoveryOcean Development and International Law39200ndash222httpsdoiorg10108000908320802013685

FAO (2011 January 5) International guidelines on bycatch manage-ment and reduction of discards Rome Italy Food and AgricultureOrganisation [pdf document] Retrieved from httpwwwfaoorgdocrephelliptba0022t00pdf

Finkelstein M Bakker V Doak D F Sullivan B Lewison RSatterthwaite W H hellip Henry R W (2008) Evaluating the po-tential effectiveness of compensatory mitigation strategies for

marinebycatchPLoS ONE3 e2480httpsdoiorg101371jour-nalpone0002480

FowlerSJ(2016January5)Draft best practice mitigation guidelines for sharks and rays taken in purse- seine and long-line fisheries Convention on Migratory Species[pdfdocument]RetrievedfromhttpwwwcmsintsitesdefaultfilesdocumentCMS_Sharks_CWG1_Doc_3_2pdf

FrancisMP(2014)Survival and depth distribution of spinetail devilrays (Mobula japanica) released from purse-seine catches NIWA ClientReportNoWLG2014-2WellingtonNewZealandDepartmentofConservation

Fulton E A Smith A D Smith D C amp van Putten I E (2011)Human behaviour The key source of uncertainty in fish-eries management Fish and Fisheries 12 2ndash17 httpsdoiorg101111j1467-2979201000371x

GardnerTAHaseABrownlieSEkstromJMPilgrimJDSavyCEhellipTenKateK(2013)BiodiversityoffsetsandthechallengeofachievingnonetlossConservation Biology271254ndash1264httpsdoiorg101111cobi12118

GjertsenHHallMampSquiresD(2010)IncentivestoaddressbycatchInRAllenJJosephampDSquires(Eds)Conservation and manage-ment of transnational tuna fisheries (pp225ndash250)Ames IAWiley-Blackwellhttpsdoiorg1010029780813820262ch14

Gjertsen H Squires D Dutton P amp Eguchi T (2014) Cost-effectivenessofalternativeconservationstrategieswithapplicationtothePacificLeatherbackTurtleConservation Biology28140ndash149httpsdoiorg101111cobi12239

GodinACCarlson JKampBurgenerV (2012)Theeffectofcirclehooks on shark catchability and at-vessel mortality rates in long-lines fisheriesBulletin of Marine Science88 469ndash483 httpsdoiorg105343bms20111054

GrimmDBarkhornIFestaDBonzonKBoomhowerJHovlandV amp Blau J (2012) Assessing catch sharesrsquo effects evidencefrom Federal United States and associated British Columbianfisheries Marine Policy 36 644ndash657 httpsdoiorg101016jmarpol201110014

HallMA(1996)OnbycatchesReviews in Fish Biology and Fisheries6319ndash352httpsdoiorg101007BF00122585

HallMAAlversonDLampMetuzalsKI(2000)By-catchProblemsand solutions Marine Pollution Bulletin 41 204ndash219 httpsdoiorg101016S0025-326X(00)00111-9

HallMANakanoHClarke S Thomas SMolloy J PeckhamSHhellipHallSJ (2007)Workingwithfisherstoreduceby-catchesIn S J Kenelly (Ed)By-catch reduction in the worldrsquos fisheries (pp235ndash288) Dordrecht The Netherlands Springer httpsdoiorg101007978-1-4020-6078-6_8

HallM amp RomanM (2013)Bycatch and non-tuna catch in the tropi-cal tuna purse seine fisheries of the worldFisheriesandAquacultureTechnicalPaper568RomeItalyFAO

HallMASwimmerYampPargaM(2012)NoldquosilverbulletsrdquobutplentyofoptionsWorkingwiththeeasternpacificartisanalfisherstore-duceseaturtlemortalityinfisheriesInJASeminoffampBWallace(Eds)Sea turtles of the eastern pacific Advances in research and con-servation(pp136ndash153)TucsonAZUniversityofArizonaPress

HamnerRMWadePOremusMStanleyMBrownPConstantineR amp Baker C S (2014) Critically low abundance and limits tohuman-relatedmortalityfortheMauirsquosdolphinEndangered Species Research2687ndash92httpsdoiorg103354esr00621

HatchSA(2003)Statisticalpowerfordetectingtrendswithapplica-tions to seabird monitoringBiological Conservation 111 317ndash329httpsdoiorg101016S0006-3207(02)00301-4

HeppellSSCrowderLBampCrouseDT(1996)Modelstoevaluateheadstartingasamanagementtoolforlong-livedturtlesEcological Applications6556ndash565httpsdoiorg1023072269391

HoughPampRobertsonM(2009)MitigationunderSection404oftheCleanWater ActWhere it comes from what it meansWetlands

14emsp |emsp emspensp MILNER- GULLAND Et AL

Ecology and Management 17 15ndash33 httpsdoiorg101007s11273-008-9093-7

IATTC(2015)Resolution on the conservation of mobulid rays caught in as-sociation with fisheries in the IATTC convention area Inter-AmericanTropical TunaCommission89thAnnualMeetingResolutionC-15-04LaJollaCAInter-AmericanTropicalTunaCommission

IFC(2012)Performance standard 6 Biodiversity conservation and sustain-able management of natural resources January 1 2012WashingtonDCInternationalFinanceCorporation

Innes J Pascoe S Wilcox C Jennings S amp Paredes S (2015)MitigatingundesirableimpactsinthemarineenvironmentAreviewofmarket-basedmanagementmeasuresFrontiers in Marine Science276httpsdoiorg103389fmars201500076

JanniseCSquiresDSeminoffJampDuttonP (2010)Conservationinvestments andmitigationTheCaliforniadrift gillnet fishery andpacificseaturtles InRQGraftonRHilbornDSquiresMTaitampMJWilliams(Eds)Handbook of marine fisheries conservation and management(pp231ndash240)OxfordUKOxfordUniversityPress

Jones E amp FrancisM (2012)Protected rays ndash Occurrence and devel-opment of mitigation methods in the New Zealand tuna purse seine fishery Auckland New Zealand National Institute of Water andAtmosphericResearch

KormosRKormosCFHumleTLanjouwARainerHVicturineR hellipWilliamson E A (2014) Great apes and biodiversity offsetprojectsinAfricaThecasefornationaloffsetstrategiesPLoS ONE9(11)e111671httpsdoiorg101371journalpone0111671

KotchenMJ (2013)Voluntaryand information-basedapproachestoenvironmentalmanagementApubliceconomicsperspectiveReview of Environmental Economics and Policy 7(2) 276ndash295 httpsdoiorg101093reepret012

Kyriazi Z LejanoRMaes FampDegraer S (2015)Bargaining a netgaincompensationagreementbetweenamarinerenewableenergydeveloperandamarineprotectedareamanagerMarine Policy6040ndash48httpsdoiorg101016jmarpol201506005

LentRampSquiresD(2017)ReducingmarinemammalbycatchinglobalfisheriesAneconomicsapproachDeep Sea Research Part II Topical Studies in Oceanography 140 268ndash277 httpsdoiorg101016jdsr2201703005

Lewison R L Crowder L B Read A J amp Freeman S A (2004)Understanding impactsof fisheriesbycatchonmarinemegafaunaTrends in Ecology amp Evolution19598ndash604httpsdoiorg101016jtree200409004

MannC (2015)StrategiesforsustainablepolicydesignConstructiveassessmentofbiodiversityoffsetsandbankingEcosystem Services16266ndash274httpsdoiorg101016jecoser201507001

Marine Stewardship Council (2014 June 21) MSC fisheries certifica-tion requirements v20 [pdf doc] httpswwwmscorgdocumentsscheme-documentsfisheries-certification-scheme-documentsfisheries-certification-requirements-version-20

MaronM IvesCDKujalaHBullJWMaseykFJBekessyShellip Possingham H P (2016) Taming a wicked problem Resolvingcontroversies inbiodiversityoffsettingBioScience66(6)489ndash498httpsdoiorg101093bioscibiw038

MaxwellSLMilner-GullandEJJonesJPKnightATBunnefeldNNunoAhellipRhodesJR(2015)BeingsmartaboutSMARTenvi-ronmentaltargetsScience3471075ndash1076httpsdoiorg101126scienceaaa1451

Moilanen A Van Teeffelen A J Ben-Haim Y amp Ferrier S (2009)Howmuch compensation is enoughA framework for incorporat-inguncertaintyandtimediscountingwhencalculatingoffsetratiosfor impactedhabitatRestoration Ecology17 470ndash478 httpsdoiorg101111j1526-100X200800382x

MorarNToadvineTampBohannanBJ(2015)Biodiversityattwenty-fiveyearsRevolutionorredherringEthics Policy amp Environment1816ndash29httpsdoiorg1010802155008520151018380

OrphanidesCDampPalkaDL(2013)Analysisofharborporpoisegill-netbycatchcomplianceandenforcement trends in theUSnorth-western Atlantic January 1999 to May 2010 Endangered Species Research20251ndash269httpsdoiorg103354esr00499

Pascoe S Innes J Holland D Finas M Theacutebaud O TownsendR hellip Hutton T (2010) Use of incentive-based managementsystems to limit bycatch and discarding International Review of Environmental and Resource Economics 4 123ndash161 httpsdoiorg10156110100000032

PhalanBHayesG Brooks SMarshDHoward PCostelloeBhellip Whitaker S (2017) Avoiding impacts on biodiversity throughstrengthening the first stage of the mitigation hierarchy Oryxhttpsdoiorg101017S0030605316001034

Queacutetier F Regnery B amp Levrel H (2014) No net loss of biodiver-sity or paper offsets A critical review of the French no net losspolicy Environmental Science amp Policy 38 120ndash131 httpsdoiorg101016jenvsci201311009

RadzioTASmolinskyJAampRoosenburgWM(2013)Lowuseofre-quiredterrapinbycatchreductiondevicesinarecreationalcrabpotfisheryHerpetological Conservation and Biology8222ndash227

RaineyHJPollardEHBDutsonGEkstromJMLivingstoneSRTempleHJampPilgrimJD(2015)AreviewofcorporategoalsofnonetlossandnetpositiveimpactonbiodiversityOryx49232ndash238httpsdoiorg101017S0030605313001476

Rausser G C Hamilton S F Kovach M amp Stifter R (2009)UnintendedconsequencesThe spillovereffectsof commonprop-ertyregulationsMarine Policy3324ndash39httpsdoiorg101016jmarpol200803020

Rice J (2014) Evolution of international commitments for fisheriessustainability ICES Journal of Marine Science Journal du Conseil71157ndash165httpsdoiorg101093icesjmsfst078

RichardYampAbrahamER(2013)ApplicationofPotentialBiologicalRemoval methods to seabird populations New Zealand AquaticEnvironmentandBiodiversityReport108

RodeJGoacutemez-BaggethunEampKrauseT(2015)Motivationcrowd-ingbyeconomic incentives inconservationpolicyAreviewoftheempiricalevidenceEcological Economics117270ndash282httpsdoiorg101016jecolecon201411019

RogersAA(2013)SocialwelfareandmarinereservesIswillingnesstopayforconservationdependentonmanagementprocessAdiscretechoiceexperimentoftheNingalooMarineParkinAustraliaCanadian Journal of Agricultural EconomicsRevue Canadienne Drsquoagroeconomie61217ndash238httpsdoiorg101111cjag12008

Rosenberg A A amp McLeod K L (2005) Implementing ecosystem-basedapproachestomanagementfortheconservationofecosystemservicesMarine Ecology Progress Series300 270ndash274 httpsdoiorg103354meps300270

Segerson K (2010) Can voluntary programs reduce sea turtle by-catch Insights from the literature in environmental economics InRQGraftonRHilbornDSquiresMTaitampMJWilliams(Eds)Handbook of marine fisheries conservation and management(pp618ndash629)OxfordUKOxfordUniversityPress

Serafy JECookeS JDiazGAGraves JEHallMShivjiMampSwimmerY(2012)CirclehooksincommercialrecreationalandartisanalfisheriesResearchstatusandneedsforimprovedconser-vation and management Bulletin of Marine Science 88 371ndash391httpsdoiorg105343bms20121038

ShiodeDHu F ShigaM Yokota K amp Tokai T (2005)Midwaterfloatsystemforstandardizinghookdepthsontunalonglinestore-duce sea turtleby-catchFisheries Science71 1182ndash1184httpsdoiorg101111j1444-2906200501080x

Sims M Cox T amp Lewison R (2008) Modeling spatial patternsin fisheries bycatch Improving bycatch maps to aid fisheriesmanagement Ecological Applications 18 649ndash661 httpsdoiorg10189007-06851

emspensp emsp | emsp15MILNER- GULLAND Et AL

Squires D amp Garcia SM (2014) Ecosystem-level impacts of fisheries bycatch on marine megafauna Biodiversity conservation through miti-gation policy economic instruments and technical changeReportofthe IUCN-CEM-FEGScientificworkshopGland Switzerland 7ndash10October2013GlandSwitzerlandIUCN

SquiresDampGarciaSM(inpress)Fisheries bycatch in marine ecosys-tems Policy economic instruments and technical change ChichesterUKJWileyampSons

SwimmerYArauzRMcCrackenMMcNaughtonLBallesteroJMusylMhellipBrillR(2006)DivingbehavioranddelayedmortalityofoliveridleyseaturtlesLepidochelys olivaceaaftertheirreleasefromlongline fishing gearMarine Ecology Progress Series323 253ndash261httpsdoiorg103354meps323253

TolottiMTFilmalterJDBachPTravassosPSeretBampDagornL(2015)BanningisnotenoughThecomplexitiesofoceanicsharkmanagementbytunaregional fisheriesmanagementorganizationsGlobal Ecology and Conservation 4 1ndash7 httpsdoiorg101016jgecco201505003

Tuck G N Polacheck T amp Bulman C M (2003) Spatio-temporaltrendsoflonglinefishingeffortintheSouthernOceanandimplica-tionsforseabirdbycatchBiological Conservation1141ndash27httpsdoiorg101016S0006-3207(02)00378-6

UNEP-WCMC(2016)Marine no net loss A feasibility assessment of imple-menting no net loss of biodiversity in the seaCambridgeUKUnitedNationsEnvironmentProgramme

Vaissiegravere A-C Levrel H Pioch S amp Carlier A (2014) Biodiversityoffsets for offshore wind farm projects The current situation inEurope Marine Policy 48 172ndash183 httpsdoiorg101016jmarpol201403023

Wallace B P Heppell S S Lewison R L Kelez S amp CrowderL B (2008) Impacts of fisheries bycatch on loggerhead tur-tles worldwide inferred from reproductive value analy-ses Journal of Applied Ecology 45 1076ndash1085 httpsdoiorg101111j1365-2664200801507x

Wanless R M Ryan P G Altwegg R Angel A Cooper JCuthbert R amp Hilton G M (2009) From both sides Dire de-mographic consequences of carnivorous mice and longlining for

the critically endangered Tristan albatrosses on Gough IslandBiological Conservation 142 1710ndash1718 httpsdoiorg101016jbiocon200903008

WardP LawrenceEDarbyshireRampHindmarshS (2008) Large-scale experiment shows that nylon leaders reduce shark bycatchandbenefitpelagiclonglinefishersFisheries Research90100ndash108httpsdoiorg101016jfishres200709034

WardTampPhillipsB(2010)SeafoodecolabelingInRQGraftonRHilbornDSquiresMTaitampMJWilliams(Eds)Handbook of ma-rine fisheries conservation and management (pp 608ndash617) OxfordUKOxfordUniversityPress

WilcoxCampDonlanCJ (2007)Compensatorymitigationasasolu-tion to fisheries bycatch-biodiversity conservation conflictsFrontiers in Ecology and the Environment 5 325ndash331 httpsdoiorg1018901540-9295(2007)5[325cmaast]20co2

WilcoxCampDonlanCJ (2009)NeedforaclearandfairevaluationofbiodiversityoffsetsforfisheriesbycatchConservation Biology23770ndash772httpsdoiorg101111j1523-1739200901173x

Wolf SHartlBCarrollCNeelMCampGreenwaldDN (2015)Beyond PVAWhy recovery under the Endangered Species Act ismorethanpopulationviabilityBioScience65200ndash207httpsdoiorg101093bioscibiu218

ZedlerJBampCallawayJC (1999)TrackingwetlandrestorationDomitigation sites follow desired trajectories Restoration Ecology 769ndash73httpsdoiorg101046j1526-100X199907108x

Žydelis R Wallace B P Gilman E L amp Werner T B (2009)Conservation of marine megafauna through minimization of fish-eries bycatch Conservation Biology 23 608ndash616 httpsdoiorg101111j1523-1739200901172x

How to cite this articleMilner-GullandEJGarciaSArlidgeW etalTranslatingtheterrestrialmitigationhierarchytomarinemegafaunaby-catchFish Fish 2018001ndash15 httpsdoiorg101111faf12273

Page 5: Translating the terrestrial mitigation hierarchy to marine ......of marine megafauna by-catch in fisheries, going from defining an overarching goal with an associated quantitative

emspensp emsp | emsp5MILNER- GULLAND Et AL

OT is the net effect on population growth rate of policiesaimingtoimprovetheoverallviabilityoftheby-caughtspeciesrsquopopulation representing ldquooffsettingrdquo of the damage caused Itrepresents the expected effects of measures to improve con-ditions for individuals which would not have been at risk ofby-catch at that particular stage in their lives or location Forexample supplementation in nesting areas (for turtles) resto-rationofnestinghabitat(forseabirds)orimplementationofpro-tectedareasaimedatdemographicgroupsnotdirectlyimpactedby fishing (calving areas for cetaceans juvenile concentrationsforfish)

3emsp |emspOPER ATIONALIZING THE FR AMEWORK

In Table3we illustrate the application of the by-catchmitigationframework using four examples from different fisheries and by-catchtaxaSpecificsolutionstoEquation1couldcomefromtakingintoaccount the regulatory cultural andeconomicconditions inaparticularfisheryForinstanceoncethefocalby-catchpopulationhasbeendefinedthenitispossibletosolvetheequationbyassign-ingfactorsaffectingdecision-makingincludingcostIfaleast-costapproachtoby-catchgoalsisappropriateEBBPUEandOT could be expressedasfunctionsofcosttosolvetheequationforagivenΔλT Another approachwould be tomaximizeΔλT subject to a budgetconstraint

Table3highlightsthatthereisnotalwayspotentialforeffec-tive action at each level of the hierarchy for some species (egoceanicwhitetipslonglines)theremaybelimitedpotentialatalllevelsTheframeworkisawayoforganizingandstructuringthink-ingaboutby-catchmitigationandenablingmitigationeffective-nesstobeassessedagainstaconcretelydefinedandmeasurabletargetItsfunctionisnottoproposenewwaysofdoingby-catchmitigationforcasesliketheseIfonusingtheframeworktoanal-yse the effectiveness of the measures available for a given by-caughtstockitisfoundthatitisnotpossibletoreachthechosentarget(egNNL)thendifficultdecisionsmustbemadeForexam-plethetargetmayneedtochangewhichcouldimplyanaccep-tanceofcontinuingdeclineoftheby-caughtstockOrthefisherymustbe restructured in away that reducesby-catcheffectively(maybeevencloseddown)Orinvestmentmustbemadeintotech-nological innovation todevelopnewways to reduceby-catch Ifitisfoundthatthedataareinadequatefortheanalysisrequiredthenthedecisionmustbemadeeithertoinvestinimprovingtheevidencebaseor to recognize that it is not possible to evaluatewhether by-catch mitigation has been effective in reaching theagreed goal The frameworkrsquosmain utility therefore is tomakethesechoicesexplicit

Equation1couldbeextendedtohandlemultiplespeciesvary-inggeartypesorheterogeneousby-catchreductionmethodsForinstanceBPUEcanbedecomposedintoseveralcomponentsrepre-sentingthedifferentstagesoftheprocessIfBPUErepresentsthesumofindividualsdeadonarrivalindividualscapturedanddyingon

thevessel and individualsdyingafter live releasewecan rewriteBPUEasaseriesoffactors

whereBDOAistheby-catchperuniteffortthatarrivestotheboatdeadBOBistheby-catchperuniteffortthatarrivestothevesselalivePDVistheproportiondyingonthevesselandPDRisthepro-portiondying after release For instance a higherproportionofby-catchofseaturtlesandotherspeciesarrivestotheboatdeadwhenusinglonglinesthataresetdeepsuchasthoseusedforbig-eyetunathatcanbesetmorethan300mdeepwhencomparedto a shallow set longline such as those used inmany nearshoreartisanal fisheries (Andrakaetal2013HallSwimmerampParga2012Swimmeretal2006)ThisdifferencewouldappearintheBDOA termSuchadecomposition illustratestheflexibilityofthisframeworkinhandlingfishery-andspecies-specificfeaturesandalsoservestohighlightareaswheredifferentmitigationmethodswouldhavethegreatestinfluence(egShiodeHuShigaYokotaampTokai2005)Anotherextensiontothebasicframeworkwouldbetoconsiderexplicitlytheuncertaintysurroundingdifferentel-ements of the conceptual model and the impact of this uncer-taintyonwhichelementofby-catchmitigationshouldbeafocus(Table3)

It is important tonote that this equation isnot a truebioeco-nomicequationtobesolvedRatheritisaconceptualframeworkinwhichwemakethecomponentsofthemitigationhierarchyexplicitinordertoguidethinkingtowardsamoreholisticapproachtoad-dressingby-catchItalsodoesnotrepresentahierarchysuchasisrequiredinterrestrialsystemsTomakethisequationintoahierar-chyratherthanamodelforleast-costmitigationofby-catchitcouldbesetupasagoalprogrammingfunctionwithsequentialsolutionstoeachelementsummedtoproducethefinalmitigationoutcomeInoperationaltermsthistranslatesintoapresumptionthatinvestmentandeffortshouldbefocusseddifferentiallyonsequentialelementsofthemodelstartingwithEBthenBPUEthenOTsothatoffsettingrelatesonly to theunavoidable residualharmonceall other stepshavebeentakenThismaybereflected intheemphasisplacedontheincentivesgiventofisherstochangebehaviourpertainingtose-quentialelementsofthehierarchyinthetimingoftheoffsetorinthedispositionofthefundingforresearchandconservationactionallocatedbygovernment

ResearchiscurrentlyongoingtooperationalizeEquation1tore-duceturtleby-catchofasmall-scalegillnetfisheryoperatingoutofSanJoseportPeru(Alfaro-Shiguetoetal2010)Currentlyasmall-scalecertificationschemeisundertrialbytheNGOProDelphinuswhich aims to give premium prices for fish caught by skippersabiding by best-practice by-catch reduction guidelines (J Alfaro-Shigueto and J Mangel personal communication) The researchentailscollectingdetailedeconomicdatafromallgillnetvesselstounderstand the economic costs involved in fishing operations tocalculatethepotentialadditionalcostsofmeasuresateachstagein

(2)BPUE=BDOA+PDVtimesBOB+(

1minusPDV)

timesBOBtimesPDR

6emsp |emsp emspensp MILNER- GULLAND Et AL

TABLE 3emspSummaryofoptionsforby-catchmitigationstructuredaccordingtothemitigationhierarchyforfourcase-studies

Fram

ewor

k st

ep

Cas

e- st

udy

Alb

atro

sses

lon

glin

esTu

rtle

slo

nglin

esRa

ysp

urse

sei

nes

Oce

anic

whi

tetip

slo

nglin

es

Definingtheproblem

Fisheryandspatial

extent

Braziliandomesticindustrialcoastallongline

fleet

EasternPacific(coastalandpelagic)

small-scalecommerciallonglinefishery

Tunapurse-seinefisheryof

theeasternPacific

AsianandEUlonglinetunafisheriesinthe

Indi

an o

cean

Targetspecies

Variousspeciesofsharkandswordfish

Mahi-mahi(

Cory

phae

na h

ippu

rus

Coryphaenidaeseasonal)tunasharks

(mostlysilkyC

arch

arhi

nus f

alci

form

is

Carcharinidae)billfish

Variousspeciesoftuna

Variousspeciesoftuna

By-catchspeciesof

conc

ern

Albatrossamppetrelspeciesparticularconcern

forcriticallyendangeredTristanalbatross

(Dio

med

ea d

aben

nenaDiomedeidae)

Oliveridley(L

epid

oche

lys o

livac

ea

Cheloniidae)greenblack(C

helo

nia

myd

asCheloniidae)hawksbill

(Ere

tmoc

hely

s im

bric

ataCheloniidae)

loggerhead(PeruandMexico)and

leatherback(D

erm

oche

lys c

oria

cea

Cheloniidae)

Sevenmobulidspecies

includingCITES-listedM

anta

bi

rost

ris(Mobulidae)and

M a

lfred

i(Mobulidae)

caughtmostlyalivein

dolphin-associatedor

free-schoolsets

OceanicwhitetipsharkVulnerableonIUCN

redlistretentionbannedbytunaRFMOs

listedonCITESAppendixII

By-catchtarget

(Δλ T)

BraziliangovernmentMinimizeby-catch

Rulesfocusontargetsforuseofminimizing

measuresratherthanonby-catchnumbers

NotwelldefinedRFMOssuggest

minimizingby-catchCouldconsiderPBR

foroliveridleyszerocatchforleather-

backs(reflectingtheirrespective

populationstatus)

IATTC(2015)zeroretention

storingorsellingandlive

releaseofby-caughtrays

whenpossibleImplies

by-catchminimization

Targetby-catchlevelnotdefineddueto

uncertaintyRFMOsbanretentionlanding

andtrans-shipment

Mitigationhierarchyelement

Avoid

[timeareaclosuresnight-timesetting]

[timeareaclosuresdeeperlines]

[timeareaclosures]

[deepsetting]

Minimize

[torilineslineweights]

[monofilamentlinecirclehooks(not

leatherbacks)]

ndash [hardtoavoidcatching]

[monofilamentlinecirclehooksbanon

steelleaders]

Remediate

ndash [hardtoreleasealive]

[improvedhandling]

[improvedhandling]

[shortsets]

Offset

[invasiveeradication]

[beachprotection]

[illegaltrade]

[informationgatheringillegaltrade]

Factorsaffectingoperationalization

Scopefor

incentives

Participatoryresearchonbarrierstouptakeof

minimizationmeasuresPositiveincentives

forthoseusingnewmeasurespaidforby

forexamplefisheries-widelevy

Certificationsustainabilitystandardsin

exportmarkets

Transitionalpaymentsto

promotebetterhandlingon

deckhenceimproving

survival

Ifinformationgatheringseenasavalidoffset

duetohighuncertaintyfundingatagging

schemecouldincentivizefisherstocollect

dataonsharkcatchratesurvivalof

releasedsharksby-catchhotspotsto

supportimprovementsacrossthewhole

mitigationframework

(Continues)

emspensp emsp | emsp7MILNER- GULLAND Et AL

themitigationhierarchy In theabsenceofhighqualitypopulationdatawithwhichtoparameterizeamodelaPBR-basedapproachisbeingusedtosetatargetby-catchlevel intermsofnumberof in-dividualsofeachoftheturtlespeciescaughtinthefisheryExpertopinionfromfishersandProdelphinusstaffsupplementedbydatafromalong-runningby-catchobserverprogrammeoperatingoutoftheport(Alfaro-Shiguetoetal2011)givesthepotentialreductioninturtleby-catchnumbersasaresultofagivenmitigationapproachInterviews and focus groups with fishers provide understandingof their preferences for different by-catchmitigation approachesbarriers and constraints to implementation and potential partici-pationindifferentincentiveschemesthiscanbesupplementedbyDiscreteChoiceExperimentsprovidingempiricalestimatesforpref-erencesforcombinationsofby-catchreductionmeasures(cfRogers2013)Thisfieldresearchproducesashort-listoffeasiblemitigationmeasuresateachstageinthemitigationhierarchyforcostingandtesting(egspecificareasortimesforfisheryclosureunderavoid-ancecombinationsofhooktypesandnetmodificationundermini-mizationtraininginturtlehandlingandreleaseforremediationandimprovingby-catchperformanceofothergeartypesintheareaforoffsetting)Thisenablestheanalysisoftheeffectivenessandcostof various combinations of by-catch reduction strategies framedwithinthefourstepsofthemitigationhierarchy(avoidminimizere-mediateoffset)withacleartargetby-catchreductiongoalinmind

4emsp |emspCOMPARING KE Y DEBATES BET WEEN TERRESTRIAL NNL AND BY- C ATCH MITIGATION

41emsp|emspThe hierarchical nature of mitigation

Terrestrial situationsareusuallyviewedas requiringastricthierar-chywithavoidanceminimizationandremediationtakingprecedenceoveroffsetsPartofthereasonforthishierarchymaybesocietalval-uesandexpectationsbut also it is a reflectionof reversibility anduncertaintyTheterrestrialmitigationhierarchywassetuptoaddresshabitatdestructioncausedbydevelopmentwhich iseffectively ir-reversiblehenceavoidanceisstrictlypreferredfromaconservationperspective Inpractice avoidancehasbeenaneglected step andmuchofthedisquietaboutbiodiversityoffsettinghasbeenbecauseofthetendencytopaylipservicetoavoidanceandfocusinsteadonoffsetswhich thenmay be implemented on paper only (HoughampRobertson2009Phalanetal2017)EvenwithperfectenforcementandcompliancewithmeasuresfurtherdownthemitigationhierarchythestrictavoidanceofhabitatlossismorecertaintolimitimpactthanreducinglossesinthecourseofapotentiallydamagingactionwhichismorecertainthanrestoringdamageafterthefactorcompensatingforitwithactionselsewhereOfteninterrestrialsystemsmultipliersareusedattheoffsetstagetoreflectthisuncertaintyrequiringthatanadditionalamountofequivalentlandisprotectedinanoffsetoverandabovetheamountthatislostduringthedevelopment(withtheratiooflandoffsettolanddestroyedinthe10sto100sdependingonthecircumstancesMoilanenVanTeeffelenBen-HaimampFerrierFr

amew

ork

step

Cas

e- st

udy

Alb

atro

sses

lon

glin

esTu

rtle

slo

nglin

esRa

ysp

urse

sei

nes

Oce

anic

whi

tetip

slo

nglin

es

Major

uncertainties

Lackofspecies-levelidentificationof

by-catchlackofunderstandingof

compliance

Lackofecologicalknowledgeofturtle

populationtrendsampdistribution

Potentialforsignificantadditional

by-catchfromcoastalgillnetfishery

Impactofcatchonmobulid

survivalPredictorsof

mobuliddistributions

Lackofobserversorreportingsoverylimited

understandingofby-catchlevelsspatio-

temporalencounterhotspotspost-release

survivalcompliance

Keyobstacle

Compliancewithexistingrulesmustbe

improved

Fundingforalternativestofishingata

largeenoughscaleLongtimelagand

uncertaintyinoffseteffectiveness

Limitedknowledgeofmobulid

distributionsmakes

avoidancedifficult

Lackofmonitoringlimitsoptions

Overallassessment

Existingmeasuresforimprovingimplementa-

tionofminimizationstepalreadyexistbut

needincentivizingoffsettingcouldprovide

short-termgainstocomplementthese

Targetedfundingcouldfacilitateimprove-

mentsthroughoutthehierarchyBest

approachmaydifferbyspecies(particu-

larlyleatherbacksvsothers)

Focusonremediationstepis

currentlythemainoption

avai

labl

e

Somepotentialforminimizationthrough

deepsettingbutchallengingtochange

behaviourinthisfisheryelectronic

monitoringsystemswouldhelp

Keyreferences

BugoniManciniMonteiroNascimentoamp

Neves(2008)Wanlessetal(2009)

Alfaro-ShiguetoDuttonampMangel(2007)

Halletal(2012)Andrakaetal(2013)

JonesampFrancis(2012)Hallamp

Roman(2013)Crolletal

(2016)Fowler(2016)

Tolottietal(2015)

Ticksindicatethepotentialforactionatdifferentstepsofthehierarchybasedonfeasibilitycurrentknowledgeandimpactonmortality(

=highpotential

=somepotential

=limitedpotential

ndash=nopotential)TextinbracketsgivessuggestedmeasuresateachlevelofthehierarchytheseareillustrativeratherthandefinitiveTheinformationforthecase-studiesisbasedontheexpertknowledge

oftheauthorsthroughtheirinvolvementinmanagementoftheby-catchissueinthesefisheriesRFMOregionalfisheriesmanagementorganizationPBRpotentialbiologicalremoval

TABLE 3emsp(Continued)

8emsp |emsp emspensp MILNER- GULLAND Et AL

2009)Bycontrastinfisheriessettingstherehavebeensuggestionsthatdependingonthelegalenvironmentitmaybemoreappropriateforoffsetstobeusedaspartofaleast-costconservationapproachalongsidemoretraditionalmitigationmethodsratherthanasthelaststep inamitigationhierarchy (DuttonJosephSquiresampWilliams2011DuttonampSquires2008WilcoxampDonlan2007)

42emsp|emspOut- of- kind offsets

Out-of-kind offsets are those which do not act to increase theimpact-affectedbiodiversityIntermsofourconceptualframeworktheyareoffsetswhichdonotacttoincreasethepopulationgrowthrateoftheby-catch-affectedfocalpopulation(Equation1)Forex-ampleonesuggestedbenefitof raising funds foroffsetting fromaby-catchtaxonfishersisthattheproceedsfromsuchataxcanfinanceoffsetselsewherewithintherangeoftheby-catch-affectedpopulation (Dutton amp Squires 2008) Although not a true offsetunderamitigationhierarchyfundsfromtheCaliforniadriftgillnetindustry in 2002 financed sea turtle nesting site conservation inBajaCaliforniaforcompensatorymitigationofseaturtleby-catch(Jannise Squires Seminoff amp Dutton 2010) In terrestrial (andmarine)systems itcanbemorechallengingtodefinethe impact-affected biodiversity because impact is rarely as clearly linkedtoagivenspeciesandstockas it is forby-catchBecauseofthisthelocationandbiodiversitytargetofconservationactionsfallingundertheldquooffsetrdquoheadinghassometimesbeenlooselyrelatedtotheactual impactBest-practicestandardsstatethatoffsetsmustbeimplementedasclosetothedamagingactivitiesaspossibleandfocusonbiodiversityassimilaraspossibletothatwhichhasbeenimpacted (BBOP 2012) However there have also been calls forldquoout-of-kindrdquooffsetsthatgivemoreconservationbang-for-buckbyfocussingonthreatenedspeciesorrarehabitatsorareasinneedofconservation rather than the impactedareasor specieswhichmay be considered less ldquovaluablerdquo for conservation (Bull Hardyetal2015)Thishasledtosubstantialdebateastotheappropri-atelimitsonthegeographicscaleandbiodiversityfocusforoffset-ting(egApostolopoulouampAdams2017)Italsodrawsattentiontothesubjectiveanduser-definednatureof theword ldquobiodiversityrdquo(Morar ToadvineampBohannan 2015) As it is impossible fully tooperationalizetheconceptimplementersofthemitigationhierar-chyhavelatitudetointerpretbiodiversityaccordingtoforexampleeaseofmeasurement perceived societal valueormitigation cost(Maron etal 2016) In our casewe take a narrow focus on theby-caughtspecies itself this is in linewithmuchof the literatureon by-catch but notwith the broader discourses on ecosystem-basedapproachestomarinemanagementandecosystemservices(RosenbergampMcLeod2005)Thesediscoursessuggest theneedforamorefunctionalecosystem-basedapproachtononetlossofbiodiversitythishasyettotranspireeitherinthemarineorintheterrestrialliteraturepossiblybecausesubstantialchallengesinde-finingimpact-affectedbiodiversitytheninevitablyensue

Asmarinemegafauna stocks are often transboundary andmi-gratorydefiningtheappropriatespatialunit foroffsettingmaybe

achallengebecause themosteffective location foranoffsetmayormaynotbewithintheareaofinfluenceofagivenfisheryClearlyandpreciselydefining the spatial unitwithinwhich themitigationhierarchywill be implemented during theprocess of defining theoverallgoal(suchasNNL)isvitalThisunitshouldreflectthescaleoverwhichanactionwillaffectλToffsetswhicharewithinthedis-tributionofthefocalstockoftheby-caughtspecies(asdefinedforEquation1)arenotout-of-kindHoweverchallengesemergewhenthe appropriate spatial unit for offsetting activities is different totheappropriatespatialunitforotherelementsofthemitigationhi-erarchywhicharelikelytobedefinedinsteadbyjurisdictionalareaor target fish stock distribution Inmany fisheries the species af-fectedbyby-catchmaynotbewellenoughknownandoffsetsmayaccordinglyneedtobebroadlytargetedtobenefitanypotentiallyaffectedspeciesTrueout-of-kindoffsetswouldincludefundingtheconservationofunaffectedspeciesorstocksofhabitatsnotusedbythefocalstockorcontributionstoaconservationfundwithoutaclearcommitmentthatthefundsaretobespentonincreasingλT for thefocalby-caughtstockTheseareunlikelytoformpartofbest-practiceguidanceforby-catchoffsets

43emsp|emspResearch as an offset

Arelatedareaofactivecontroversyformarineby-catchiswhetherresearchor informationgatheringshouldbeseenasavalidoffsetmechanism The rationale is that this research could be used toreduceuncertaintypromote innovationand thereby improveout-comes for by-caught species albeit indirectly An offset could beusedto incentivizebetterdatacollectionfor instanceusingaby-catchlevytopayfortaggingortoputby-catchobserversorelec-tronicmonitoringsystemsonboatsThismightbeapreludetolatermitigation or avoidance activities once more is known about thebiological settingWhether research activities could appropriatelybeconsideredaspartofanldquooffsetrdquoiscontroversialmdashinsomecasesan indirectbenefit to theby-caught stockmightbe clearly appar-ent(egtheoceanicwhitetip(Carcharinus longimanusCarcharinidae)case-studyinTable3)whileinothercasesusinginvestmentinre-searchasanoffsetcouldbeseenasacaseofmoralhazardpoten-tially compromising scientistsrsquo independence and having at best ahighlyindirectrelationshiptoNNLoftheby-caughtspeciesAnotherviewisthatreducinguncertaintyisacoreresponsibilityofoperatingafisherywhichthereforeshouldbebornebythemanagementau-thorityorfishingbusinessesInterrestrialsystemsthesedilemmasalsoexistbutthesentimentismuchmoreclearlyexpressedthatre-searchactivitiesarenotappropriateoffsets(BullGordonWatsonampMaron2016)

44emsp|emspIncentivizing implementation of mitigation measures

Thefactorsthatdrivedecision-makingaboutmegafaunaby-catchreduction (by skippers companies fishery managers policymak-ers and other stakeholders) include legal obligations tominimize

emspensp emsp | emsp9MILNER- GULLAND Et AL

by-catch at the national or international levels (eg FAO 2011Rice 2014) the availability and quality of technical fixes associ-atedcosts tofishers limitsonaccesstoseafoodmarketsaswellassocietalpressuresHowevermuchresearchonby-catchreduc-tion focuses on identifying and implementing technicalmeasuresto reduceBPUE rather thanon the social andeconomicbarriersto implementation (Campbell amp Cornwell 2008) Technologicalinnovation to improve BPUE needs to be appropriately incentiv-izedwitheffortsmadetoensurethatsuchmeasuresareascost-effective as possible for fishers (Gjertsen Hall amp Squires 2010Lent amp Squires 2017) However it often happens that even ap-parently suitable by-catchmeasures are notwidely implemented(eg Damalas amp Vassilopoulou 2013 Orphanides amp Palka 2013RadzioSmolinskyampRoosenburg2013)Inthesecasesthedegreeofnon-implementationandthereasonsbehinditneedstobeun-derstoodsoitcanbeaddressed(Coxetal2007)Thesetypesofconsiderationarealsonotwellresearchedintheterrestrialoffset-tingliteraturebecausecomplianceispoorlymonitored(BullSuttleGordonSinghampMilner-Gulland2013)andthereislittlesupportfor researchon thebarriers to implementationofamitigationhi-erarchyandhowtosupportdeveloperstoaddressthesebarriers(BullBryantBakerampMilner-Gulland2015)Thesocialimpactsofimplementingabiodiversitymitigationhierarchyonresourceusersarementioned inguidance (egBBOP2012)buthowtomeasureandaccountforthemisverypoorlyunderstoodThefewstudiesin-vestigatingdeliveryofpromisedoffsetmeasuresinterrestrialsys-temssuggestaverypoorrecord(QueacutetierRegneryampLevrel2014)Therefore the social side of implementing the mitigation hierar-chyand incentivizingcompliance isanarea thatneedsmore andmoreactiveresearchwithinboththeterrestrialandmarinerealms(FultonSmithSmithampvanPutten2011)Thisisparticularlytruewhentheburdenof implementingmitigationapproaches isbornebyrelativelysmall-scaleproducersratherthangovernmentsormul-tinationals(egthepelagiclonglinefisheriesinTable3)

45emsp|emspSocietal limits

Foraspeciesathighriskofextinctioncompleteavoidanceofby-catchmightbethemostdesirablepolicyfrombothamanagementagency and societal perspective In addition with emblematic orhighlythreatenedmarinemegafaunaitmaybeviewedbymembersof the public asmorallywrong to kill any individuals even ifmiti-gationisinplace(egMauirsquosdolphinHamneretal2014) leadingtopressureongovernmentstoreflectthisethicalconcerninregu-lationsThesedilemmasecho the issueof thresholds in terrestrialoffsetswhichrecognizesthattherearesomecriticalareasinwhichdevelopmentisnotsocietallyappropriateregardlessofthepoten-tialformitigationandotherareasinwhichthemitigationhierarchycan be appropriately applied (Bull etal 2013) Examples of loca-tionswhereathresholdapproach isseenasappropriate interres-trial systems include the habitat of highly endangered species orecosystemswhich are limited in extent and irreplaceable (such asoldgrowthforest) In terrestrialsystems therefore themitigation

hierarchyisseenasmostappropriateforapplicationinmorecom-monanddegradedhabitatssuchasfarmlandSimilarlyinfisheriestheremaybesomesituationsinwhichthestockssubjecttoby-catchare so precious or threatened that no level of threat from fishingcanbecontemplatedandotherswherefishingsubjecttoNNLandthemitigationhierarchyisasociallyacceptableapproachInsitua-tions inwhich trade-offs between conservation and developmentareseenasnecessaryoracceptablebywidersocietyasociallicencetooperatemaybegainedthroughadoptingoffsetsintheabsenceofregulationForexampleinsub-SaharanAfricaseverallargedevel-opmentprojectsareattemptingtooffsettheirimpactsongreatapesandtheirhabitats(Kormosetal2014)Aby-catchequivalentmightbe fishing companies voluntarily donating funds for turtle nestingbeachrestorationintheirareaofoperationinadditiontocomply-ingwithregulatoryby-catchmitigationmeasuresThesemeasuresmayimprovetheimageofthecompanywiththegeneralpublicbuttoavoidaccusationsofldquogreenwashingrdquotheireffectivenessneedstobeproperlyscrutinized(Bulletal2016)Transparentlyembeddingthesetypesofactionswithinamitigationhierarchysuchasweareproposing and critically evaluating their contribution to increasingthepopulationgrowthrate(asperEquation1)wouldbeonewaytopromptsuchscrutiny

46emsp|emspUncertainty

The nature of the uncertainties surrounding biology and enforce-ment in themarine setting raisesquestions about theorderingofsteps in themitigationhierarchy inaway that isdissimilar to ter-restrialsystemswherethehierarchyofuncertaintiesmaybecleareranduncertaintyisgenerallylowerForexampleitmaybethattheimpactonoverallpopulationgrowthrateofanoffsetmeasurelikeeradicating invasivespecies fromaseabirdnestinghabitat isbothless uncertain and more cost-effective than avoidance measuressuchasclosingareaswhichmayormaynotbefrequentedbyadultseabirds in a given time-periodGenerally though itmightbe as-sumedthatmeasureswhichtargetlifestagessubjecttohighlevelsofnaturalmortalityorwithinwhichindividualcontributiontoover-allpopulationgrowthrateislow(egheadstartingjuvenileturtles)maybelesseffectiveinachievingNNLthanmeasureswhichtargetreproductivelymatureadultfemales(suchaslivereleasesHeppellCrowderampCrouse1996)Howeverbeforeimplementinganoffsetthataimstoimprovethesurvivalofonelifestageinordertocom-pensatefortheby-catchmortalityofanotherarobustassessmentoftheconsequences(withassociateduncertainties)shouldbecar-ried out through detailed population modelling based on strongempiricalstudies(cfWallaceHeppellLewisonKelezampCrowder2008)Interrestrialsystemstherequirementsequentiallytoapplythemitigationhierarchyisbroadlyunchallengedbutactuallysimilararguments apply For example habitat restoration sits above off-settinginthehierarchyandyetitisalong-termuncertainprocesswhichmayinsomecircumstancesbemuchlesspreferabletoanoff-setusingawell-establishedapproachwhichishighlylikelytoleadtoconservationgains

10emsp |emsp emspensp MILNER- GULLAND Et AL

47emsp|emspTemporal considerations

Thetimingofoffsetsinrelationtootherelementsofthemitigationhierarchyhasbeenthesubjectofdebatewithintheterrestriallitera-tureThemainsuggestionforaddressingthetemporarylossofbio-diversitywhileoffsetscometofruitionhasbeenadoptingmitigationbankingwherebyoffsetsareimplementedinadvanceofpotentiallydamagingactivitiesprovidingbiodiversitycreditswhichcanbeusedtocompensateforlaterlossesThisbothremovesanelementofun-certaintyfromtheoffsetimplementationandreducesthetimelagbetweenlossandgain(Mann2015)Withrespecttomarinemega-faunaby-catchflexibilityintimingprovidesadditionalscopeforcostreduction and benefit enhancementwhichmay not be present intraditionalhabitat-basedterrestrialoffsetsForexampletemporarymeasuressuchasashort-termby-catchtaxtofundanoffsetmaybeusedifmitigationoravoidancemethodstaketimetocomeonlineorifatemporarynudgeisenoughtocausebehaviouralchangeThismightbethecaseifapolicywasneededtoinducefisherstotakeupnewgeartoavoidthecostofanoffsetorifconcernsaboutsafetyoryieldreductionsduringthetransitiontonewgearcouldbeallayedbyatemporarysubsidyforearlyadoptersorapaidparticipatorymoni-toringprogrammeto informwider implementation(egthemobu-lidandsharkcase-studiesinTable3)Justasforhabitatrestoration(ZedlerampCallaway 1999) by-catchoffset strategieswhich targetjuvenilestagesof long-livedspecies (eg turtleheadstartingor in-vasive removal fromseabirdnesting islands)may takemanyyearsfor their effects to become apparent in an increase in populationgrowthratesAdditionaluncertaintyisintroducedbythedifficultyinmonitoringpopulationsofmanyby-catch species (eg seabirdsHatch2003)leadingtouncertainestimatesoftheimpactofoffsetactivitiesonpopulationgrowth(seecase-studiesinTable3)Theseproblemsarenot insuperablehoweverpositivetrendshavebeenreportedinturtlepopulationsoverdecadesasaresultofnestpro-tection(egDuttonDuttonChaloupkaampBoulon2005)

5emsp |emspUSING INCENTIVES TO REDUCE BY- C ATCH

Manyoftheexamplesandprinciplesdiscussedaboveeitherimplic-itlyorexplicitlyrelatetotheeconomicsocialinstitutionalormoralincentivesoperatingondifferentactorsinsideandoutsidethefish-erywhichcanbepositiveornegativeWenowturntoadiscussionofhowincentivescanbeusedtoreduceby-catchwithinourframe-workIncentivescanbeputinplacetochangefisherbehaviourwithrespecttoanyoftheelementsoftheframework (avoidminimizeremediateandoffsetTable3)Althoughdiscussedintheliteraturemostof these incentive approaches are yet tobe implemented inthe realworldparticularly forby-catchThereforeuntil empiricalevidenceoftheireffectivenessisavailablethesesuggestionscomewithacaveat

Financial costsofby-catchmitigationactions canarise for in-stancefromlostcatchcapitalinvestmentsinnewgearormitigation

equipmentor the lossofaccesstoafisheryCostsmayalsoarisefromthedeploymentofby-catchobserversortrainingintheuseofnewgearThesecostscanbepaidbyfishingcompaniesorindivid-ualsorbygovernmentsNGOsorseafoodconsumersWhetherornotcompensationforcostsincurredbyfishersisseenasappropri-atedependsonwhetherby-catchreductionisseenasasocialgoodthatfishersareproviding(inwhichcasetheyshouldbecompensatedforit)orasputtingrighttheharmthattheyaredoingtobiodiver-sitywhilegeneratingtheirownprivategain(ineconomiclanguagewhetherby-catchisviewedasanunpricedexternalityinwhichcasetheyshouldpay)Italsodependsonwhethereconomichardshipwillensueacaseforcompensationofby-catchreductioncostsincurredbypeopledependenton fishing for their livelihoodsmaybemoresympatheticallyreceivedbyotheractorsthanacasemadebyalargemultinationalfishingcompany

Ifby-catchisseenasanunpricedexternalityitmightbesociallyoptimaltotaxfishersfortheirby-catchsothatthisexternalityisin-ternalizedThisplacesanexplicitpriceuponby-catch(Boyce1996Pascoeetal2010SquiresampGarcia2014)Theby-catchprice islikely to be incorporated into the price of the target species andtherebybecomespartofthetargetspeciescostThispricecouldbeset differently for different demographic classesof theby-caughtspecies depending on the impact the loss of an individualwouldhaveonthepopulationAllelsebeingequalputtingapriceonby-catchmeans that theseafoodproduct that is the targetcatchbe-comesmoreexpensiveandconsumershave topaymore for theirseafoodreducingdemandTheninprincipleeveryfirminthesup-plychaineveryvesselandeveryconsumerhaveanincentivetore-duceby-catchuntileacheconomicactorrsquosmarginalcostofby-catchreductionequals thecommonpriceofby-catch that theyall faceOffsetsareonewaytopriceandinternalizetheby-catchexternalitycostIfanoffsettingactioniscostlytoimplementandmustbepaidforwith each unit of by-catch it implicitly prices the residual by-catch In this circumstance the effect from a financial standpointisthesameasaby-catchtaxwiththe levelsetbasedonthecostoftheoffsetVariousinstitutionalstructurestosupportthischargeperunitofby-catcharepossiblewithdifferentimplicationsintermsofthedistributionofcostsandbenefitsForexampleaninsuranceschemecouldbepaidintobyfishersthatpaysoutintheeventofaby-catcheventtherebyspreadingthecostofunavoidablerareby-catcheventsOratradablepermitschemecouldoperatesuchthatfisherswhoexperienceaby-catcheventcanbuyapermitwiththecostvaryingdependingondemandforpermits (henceprovidingavessel-levelincentivetoinnovatetoreduceby-catch)

If there isdemandforconservation inan internationalmarketthen price premiums and market access (through eco-labellingsupply chain certification other food sustainability campaignsWardampPhillips2010)orboycottsactingasstrategicthreatsfromconsumers (Kotchen 2013 Segerson 2010) could act as positiveornegativeeconomic leversonthe fisheryprovidingan incentivefor fishers to reduce their by-catch voluntarily (as has been sug-gested for the Brazilianmahi-mahi fishery Table3) For exampletheMarine StewardshipCouncil now includesby-catchmitigation

emspensp emsp | emsp11MILNER- GULLAND Et AL

intheircertificationprocess(MSC2014)Demand-ledleversmaybemoreorlessapplicableatdifferentlevelsinthehierarchyforexam-pleavoidancemayberelativelyhardtoevidencewhileoffsettingmaybelesseasytoselltoaconsumerthanminimizationorreme-diationConcerns about the unintended consequences of positiveincentives (particularlyfordirectsubsidiesratherthanconditionalincentives)maydeterminewhethertheyareanappropriateinstru-mentinagivencaseForexampletheymaybeinappropriateifthereisariskthattheadditionalmoneyisreinvestedinincreasedfishingcapacityor iftheremaybeconsumptionproductionorconserva-tionleakages(transferoftheproblemsomewhereelse)whetheratthe vessel fishery or trans-national levelHigh transactions costsmayalsolimitthebenefitsofincentivesschemes

Otherchangeswhichmayneedtobeincentivizedforsuccessfulimplementationofby-catchreductionpoliciesmaybelessamenabletofinancialmeasuresatleastpartlybecauseitislessclearhowtoassign financial value to theactionsor to thebenefits and losseswhichtheyproduceForexampleperceivedreductionsinsafetyforfishingcrews(fromweightedlonglinesfor instance)arecoststhatmaybehardtovaluefinanciallyOtherprerequisitesfor long-termsustainable behaviour change such as changes in social norms sothatfishingcommunitiesseeby-catchreductionasappropriatebe-haviourortechnicalskillacquisitionsothattheycanusenewmeth-odsmaybeincentivizedbycarefullydesignedinterventionsworkingwithfishers(Halletal2007)Conservationpoliciesbasedoneco-nomic incentives (extrinsicmotivation) are not always superior tothosebasedupon intrinsicmotivation Infact incentive-basedby-catch reduction policy instruments could even be counterproduc-tivebyreducingtheeffectivenessofintrinsicmotivationdependingupon the situation (although the empirical evidence on this topicisweak RodeGoacutemez-BaggethunampKrause 2015) If the changerequiredforby-catchreductiontoworkmeetscultural resistancethenparticipatory researchmightbeespeciallyeffective inbreak-ingdownbarriersbetweenthosewhowantby-catchreductiontotakeplaceandthosewhoactuallyhavetoimplementit(thefishers)ForexampleinAustraliathegovernment-fundedbodyOceanwatchfacilitatesengagementbetweencommunities thefishing industryseafood suppliers and government to improve knowledge sharing(wwwoceanwatchorgau)Innovationiscrucialinfisheriesandfish-ersareaccustomedtoadoptingnewtechnologyorprocessespo-tentiallymakingan incentivizedparticipatory researchprogrammeespeciallyfruitful

Sometimes the most efficient way to solve problems is a so-cial instrumentoran institutionalchange inplaceoforaswellasan economic instrument For example supporting developmentof fisherorganizations rather than instituting a vessel-level taxorsubsidy might provide the impetus needed to change behaviourInstitutingcatchshares(individualtransferablequotas)mayprovideanenablingenvironmentforby-catchreductionforexamplebypro-motingmoreeffectivemonitoring(Grimmetal2012)Experiencein terrestrial system produces similar insights incentive-basedschemeswhichalsobuildcommunitycohesionandsupportthede-velopment or strengthening of localmanagement institutions are

more effective in the longer run than direct economic incentives(Clementsetal2010)

6emsp |emspCONCLUSIONS

The framework we present here is novel It draws upon and ex-tends the frameworks for conceptualizing by-catch developed byHall (1996) and Hall Alverson andMetuzals (2000) It amalgam-atesHallrsquos frameworkwith themitigationhierarchyasused in theEnvironmental Impact Assessment literature (BBOP 2012) Thesuggestions about goals metric andmitigation actions are drawnfromtheempiricalby-catchliteratureandtheissueswediscussin-tegratetheconcernsoftheextensiveterrestrialandnascentmarineoffsetting literature with the by-catch literature The frameworkmakesclear thatanearlycrucial step is toclarify thegoalofanyby-catch reduction policyOverarching goals like those issued bytheConventiononBiologicalDiversity(egAichiTarget11that10ofmarinehabitatshouldbeunderprotectionby2020)needtobetranslatedintooperationaltermswithineachfisheryCurrentlyleg-islatedoragreedby-catch reductiongoals tend tobe less specificthantheycouldbeandthisleadstoproblemsininterpretingthesegoals inordertoplanaby-catchmitigationstrategy(seethecase-studies inTable3 for examples) This ambiguity is tobe expectedwithinnegotiatedtargetsbutitisachallengenonetheless(Maxwelletal2015)Usingacommonunitofby-catch impactsuchastheΔλTwhichweuseherewouldbehelpfulbothinclarifyingexpecta-tionsandevaluatingtheeffectivenessofelementsofthemitigationhierarchy

Once the by-catch goal is known options for implementingavoidanceminimizationremediationandoffsetscanbeclarified(asinTable2)Howeveroutsideof the interconnectedbiologyof theecosystemby-catch isembeddedwithinsocialandeconomicsys-temsDifferentunitsofanalysismaybeneededatdifferent levelsofthehierarchytocopewiththechallengesofincompleteoverlapbetween jurisdictional units fisheries target stocks and by-catchstocksJurisdictionalissuesareimportantandcomplexpotentiallyimpeding implementationFleets interact raisingtheriskofpolicyleakageforexampleifpeopleshifttootherfisheriesgearorliveli-hoodsThereforethescaleatwhicheachelementofthemitigationhierarchyisimplementedislikelytovarywithincentivestomitigateoftenbeingbest appliedat thevessel level focussedon reducingindividualmortalitywhileoffsettingisimplementedatthescaleoftheby-catchspeciesrsquostockWithtransboundaryspeciesunilateralconservationinonejurisdictioncreatesthepotentialforproductiontrade and conservation leakages For example a conserving Statecouldimplementtheavoidancestepandshutdownordramaticallycurtailitsownproductionofswordfishtoreduceseaturtleby-catchbuttheknock-oneffectmaybemoreimportationofswordfishfromfleetswithhigherseaturtleby-catch(RausserHamiltonKovachampStifter2009)

Translatingtheframeworkfromaspeciestoanecosystemlevelwill require consideration of the potential interactions between

12emsp |emsp emspensp MILNER- GULLAND Et AL

by-catchmitigationapproachestargetedatdifferentspecies(Serafyetal 2012) Actions to mitigate by-catch for one group of spe-cies can increase or decrease it for others and so a system-wideapproach isneededForexample changing fromJ-hooks tocirclehookstoreducemortalityofturtlesmaydecreaseorincreasesharkmortality(Andrakaetal2013GodinCarlsonampBurgener2012)In terrestrial systems similar interactions arise and value judge-mentsaremade(whetherexplicitlyorimplicitly)astowhatlossandgain of ldquobiodiversityrdquo translates to in operational terms andwhatelementsofbiodiversitymattermosttoimplementers

Uncertainty is high in ocean ecosystems creating both chal-lengesandopportunitiesinapplyingtheconceptofNNLthroughamitigationhierarchythatincludesoffsettingInparticularformarinemegafaunathereishighuncertaintyintheprocesseslinkinganyel-ementofthemitigationhierarchythroughtochangesinpopulationgrowthrateFurthermore impactscanbelong-termhardtomea-sureandspatiallydiffuseanduncertaintyisnotpredictablyspreadthroughthehierarchyThiscreatesadifferentsetofchallengestothosefacedinterrestrialsystemswhereatleastforsometypesofenvironmentalimpactthelinksbetweenactionandimpactarerel-ativelydirectandmeasurableanduncertaintygenerally increasesthroughthemitigationhierarchy (fromavoidthroughminimizere-mediatetooffset)

By-catch reduction measures have had significant successesoverthelastdecadesasaresultofsubstantialinvestmentoftimeand funding by researchers management authorities conserva-tionorganizationsandfishers(Coxetal2007)Howeverthissuc-cessisnotuniversalJustasforanyfisheriesmanagementissueapoorregulatoryregimelimitedcomplianceandlackofinforma-tionhampereffortstoreduceby-catchInsomeplaceshighlevelsofby-catch limitedoptions formitigationandweakgovernance(leadingtopoorenforcement)cancombinetomaketheby-catchproblemintractableOurframeworkwillnotsolvetheseproblemsHowever itbrings together the full rangeofapproaches forby-catchmitigationinastructuredandsystematicwaywhichrequiresatargettobeexpressedagainstwhichoutcomescanbeevaluatedByexposingareasofuncertaintyanddatadeficiencyitcouldchal-lengescientistsandmanagerstoobtainthedatarequiredproperlytoevaluate theeffectivenessofmitigationmeasuresThis couldthensupportandencourageclearerdecision-makingandprioriti-zationofactionsOurframeworkdemonstratesthattheprincipleof implementing thegoalofnonet loss throughamitigationhi-erarchy isasapplicable tomarinemegafaunaby-catchas to ter-restrial systems where it is already widely used in challengingdata-poorcircumstances

There isuntappedpotential forcost-effectiveby-catchmitiga-tionwhichcouldberealizedwiththeadoptionofthisframeworkandwithconsiderationofnewapproachestoincentivizingby-catchmitigationwithinthestepsofthehierarchyApplyingittoafewcase-studiesinpracticewilldemonstrateempiricallywhereandhowthepotentialforimprovedeffectivenesscouldbestberealizedExistinglegalframeworksoftenprecludeapproacheswhichimplicitlyorex-plicitly permit by-catch including the use of economic incentives

ornewapproachessuchasoffsetsHoweverinthiscontextofdy-namicuncertaintythedividendsofthinkingmorecreativelyaboutby-catchmitigationcouldbehigh

ACKNOWLEDG EMENTS

EJMG acknowledges the Pew Charitable Foundation for its sup-port of thiswork This article originated at a 2013workshop co-organized by NOAA-Fisheries and IUCN-CEEM-FEG entitledldquoMultidisciplinaryWorkshoptoAddressEcosystem-LevelImpactsofFisheriesBycatchonMarineMegafaunaBiodiversityConservationthrough Mitigation Policy Economic Instruments and TechnicalChangerdquo We thank the reviewers for their insightful commentswhichmuchimprovedthemanuscript

ORCID

E J Milner-Gulland httporcidorg0000-0003-0324-2710

R E FE R E N C E S

Alfaro-Shigueto J Dutton P H amp Mangel J (2007) Interactionsbetween leatherback turtles and Peruvian artisanal fisher-ies Chelonian Conservation and Biology 6 129ndash134 httpsdoiorg1027441071-8443(2007)6[129ibltap]20co2

Alfaro-Shigueto JMangel JCBernedoFDuttonPHSeminoffJAampGodleyB J (2011) Small-scale fisheriesofPeruAmajorsinkformarineturtles inthePacificJournal of Applied Ecology481432ndash1440httpsdoiorg101111j1365-2664201102040x

Alfaro-ShiguetoJMangelJCPajueloMDuttonPHSeminoffJ A amp Godley B J (2010) Where small can have a large im-pact Structure and characterization of small-scale fisheries inPeru Fisheries Research 106 8ndash17 httpsdoiorg101016jfishres201006004

Andraka SMugM HallM PonsM Pacheco L ParralesM hellipOrtega D (2013) Circle hooks Developing better fishing prac-ticesintheartisanallonglinefisheriesoftheEasternPacificOceanBiological Conservation 160 214ndash224 httpsdoiorg101016jbiocon201301019

ApostolopoulouEampAdamsWM(2017)BiodiversityoffsettingandconservationReframingnaturetosaveitOryx5123ndash31httpsdoiorg101017S0030605315000782

BaacuteezJCRealRGarciacutea-SotoCJoseacuteMMaciacuteasDampCamintildeasJA(2007)Loggerheadturtleby-catchdependsondistancetothecoastindependentoffishingeffortImplicationsforconservationandfish-eries management Marine Ecology Progress Series 338 249ndash256httpsdoiorg101017S0030605315000782

BBOP (2012) Standard on biodiversity offsets Business and biodiversity offsets programmeWashingtonDCForestTrends

Bishop J (2006) Standardizing fishery-dependent catch and ef-fort data in complex fisheries with technology change Reviews in Fish Biology and Fisheries 16 21ndash38 httpsdoiorg101007s11160-006-0004-9

BoyceJ(1996)AneconomicanalysisofthefisheriesbycatchproblemJournal of Environmental Economics and Management31 314ndash336httpsdoiorg101006jeem19960047

BugoniLManciniPLMonteiroDSNascimentoLampNevesTS(2008)SeabirdbycatchintheBrazilianpelagiclonglinefisheryandareviewofcaptureratesinthesouthwesternAtlanticOceanEndangered Species Research5137ndash147httpsdoiorg103354esr00115

emspensp emsp | emsp13MILNER- GULLAND Et AL

BullJWampBrownlieS(2017)Thetransitionfromnonetlosstoanetgainof biodiversity is far from trivialOryx51 53ndash59 httpsdoiorg101017S0030605315000861

BullJWBryantCBakerJampMilner-GullandEJ(2015December28)Developing measuring and communicating the outcomes of cor-porate biodiversity strategies [pdfdocument]RetrievedfromhttpwwwwildbusinessorgBull_etal_2015_WBLpdf

BullJWGordonAWatsonJEampMaronM(2016)Seekingcon-vergenceonthekeyconceptsinlsquononetlossrsquopolicyJournal of Applied Ecology531686ndash1693httpsdoiorg1011111365-266412726

BullJWHardyMJMoilanenAampGordonA (2015)Categoriesof flexibility in biodiversity offsetting and their implications forconservation Biological Conservation 192 522ndash532 httpsdoiorg101016jbiocon201508003

Bull JW Lloyd S P amp StrangeN (2017) Implementation gap be-tween the theory and practice of biodiversity offset multipliersConservation Lettershttpsdoiorg101111conl12335

Bull JW SuttleKBGordonA SinghN JampMilner-Gulland EJ(2013)BiodiversityoffsetsintheoryandpracticeOryx47369ndash380httpsdoiorg101017S003060531200172X

CampbellLMampCornwellML(2008)Humandimensionsofbycatchreduction technology Current assumptions and directions for fu-tureresearchEndangered Species Research5325ndash334httpsdoiorg103354esr00172

Caswell H Brault S Read A J amp Smith T D (1998) Harborporpoise and fisheries An uncertainty analysis of inciden-tal mortality Ecological Applications 8 1226ndash1238 httpsdoiorg1018901051-0761(1998)008[1226hpafau]20co2

ClementsTJohnANielsenKAnDTanSampMilner-GullandEJ (2010)Payments forbiodiversityconservation in thecontextofweak institutions Comparison of three programs from CambodiaEcological Economics 69 1283ndash1291 httpsdoiorg101016jecolecon200911010

CoxTLewisonRŽydelisRCrowderLSafinaCampReadA(2007)ComparingeffectivenessofexperimentalandimplementedbycatchreductionmeasuresTheidealandtherealConservation Biology211155ndash1164httpsdoiorg101111j1523-1739200700772x

CrollDADewarHDulvyNKFernandoDFrancisMPGalvaacuten-Magantildea F hellip Newton K M (2016) Vulnerabilities and fisher-ies impactsTheuncertain futureofmanta anddevil raysAquatic Conservation Marine and Freshwater Ecosystems 26 562ndash575httpsdoiorg101002aqc2591

Damalas D amp Vassilopoulou V (2013) Slack regulation com-pliance in the Mediterranean fisheries A paradigm from theGreek Aegean Sea demersal trawl fishery modelling discardogives Fisheries Management and Ecology 20 21ndash33 httpsdoiorg101111j1365-2400201200860x

DuttonDLDuttonPHChaloupkaMampBoulonRH(2005)IncreaseofaCaribbeanleatherbackturtleDermochelys coriaceanestingpop-ulation linked to long-termnestprotectionBiological Conservation126186ndash194httpsdoiorg101016jbiocon200505013

DuttonPJosephJSquiresDampWilliamsM(2011)Bellagioblue-print foractiononseaturtlesChapter2 InPDuttonDSquiresampM Ahmed (Eds) Conservation of pacific sea turtles (pp 15ndash36)HonoluluHIUniversityofHawaiiPress

DuttonPampSquiresD (2008)AholisticstrategyforPacificseatur-tlerecoveryOcean Development and International Law39200ndash222httpsdoiorg10108000908320802013685

FAO (2011 January 5) International guidelines on bycatch manage-ment and reduction of discards Rome Italy Food and AgricultureOrganisation [pdf document] Retrieved from httpwwwfaoorgdocrephelliptba0022t00pdf

Finkelstein M Bakker V Doak D F Sullivan B Lewison RSatterthwaite W H hellip Henry R W (2008) Evaluating the po-tential effectiveness of compensatory mitigation strategies for

marinebycatchPLoS ONE3 e2480httpsdoiorg101371jour-nalpone0002480

FowlerSJ(2016January5)Draft best practice mitigation guidelines for sharks and rays taken in purse- seine and long-line fisheries Convention on Migratory Species[pdfdocument]RetrievedfromhttpwwwcmsintsitesdefaultfilesdocumentCMS_Sharks_CWG1_Doc_3_2pdf

FrancisMP(2014)Survival and depth distribution of spinetail devilrays (Mobula japanica) released from purse-seine catches NIWA ClientReportNoWLG2014-2WellingtonNewZealandDepartmentofConservation

Fulton E A Smith A D Smith D C amp van Putten I E (2011)Human behaviour The key source of uncertainty in fish-eries management Fish and Fisheries 12 2ndash17 httpsdoiorg101111j1467-2979201000371x

GardnerTAHaseABrownlieSEkstromJMPilgrimJDSavyCEhellipTenKateK(2013)BiodiversityoffsetsandthechallengeofachievingnonetlossConservation Biology271254ndash1264httpsdoiorg101111cobi12118

GjertsenHHallMampSquiresD(2010)IncentivestoaddressbycatchInRAllenJJosephampDSquires(Eds)Conservation and manage-ment of transnational tuna fisheries (pp225ndash250)Ames IAWiley-Blackwellhttpsdoiorg1010029780813820262ch14

Gjertsen H Squires D Dutton P amp Eguchi T (2014) Cost-effectivenessofalternativeconservationstrategieswithapplicationtothePacificLeatherbackTurtleConservation Biology28140ndash149httpsdoiorg101111cobi12239

GodinACCarlson JKampBurgenerV (2012)Theeffectofcirclehooks on shark catchability and at-vessel mortality rates in long-lines fisheriesBulletin of Marine Science88 469ndash483 httpsdoiorg105343bms20111054

GrimmDBarkhornIFestaDBonzonKBoomhowerJHovlandV amp Blau J (2012) Assessing catch sharesrsquo effects evidencefrom Federal United States and associated British Columbianfisheries Marine Policy 36 644ndash657 httpsdoiorg101016jmarpol201110014

HallMA(1996)OnbycatchesReviews in Fish Biology and Fisheries6319ndash352httpsdoiorg101007BF00122585

HallMAAlversonDLampMetuzalsKI(2000)By-catchProblemsand solutions Marine Pollution Bulletin 41 204ndash219 httpsdoiorg101016S0025-326X(00)00111-9

HallMANakanoHClarke S Thomas SMolloy J PeckhamSHhellipHallSJ (2007)Workingwithfisherstoreduceby-catchesIn S J Kenelly (Ed)By-catch reduction in the worldrsquos fisheries (pp235ndash288) Dordrecht The Netherlands Springer httpsdoiorg101007978-1-4020-6078-6_8

HallM amp RomanM (2013)Bycatch and non-tuna catch in the tropi-cal tuna purse seine fisheries of the worldFisheriesandAquacultureTechnicalPaper568RomeItalyFAO

HallMASwimmerYampPargaM(2012)NoldquosilverbulletsrdquobutplentyofoptionsWorkingwiththeeasternpacificartisanalfisherstore-duceseaturtlemortalityinfisheriesInJASeminoffampBWallace(Eds)Sea turtles of the eastern pacific Advances in research and con-servation(pp136ndash153)TucsonAZUniversityofArizonaPress

HamnerRMWadePOremusMStanleyMBrownPConstantineR amp Baker C S (2014) Critically low abundance and limits tohuman-relatedmortalityfortheMauirsquosdolphinEndangered Species Research2687ndash92httpsdoiorg103354esr00621

HatchSA(2003)Statisticalpowerfordetectingtrendswithapplica-tions to seabird monitoringBiological Conservation 111 317ndash329httpsdoiorg101016S0006-3207(02)00301-4

HeppellSSCrowderLBampCrouseDT(1996)Modelstoevaluateheadstartingasamanagementtoolforlong-livedturtlesEcological Applications6556ndash565httpsdoiorg1023072269391

HoughPampRobertsonM(2009)MitigationunderSection404oftheCleanWater ActWhere it comes from what it meansWetlands

14emsp |emsp emspensp MILNER- GULLAND Et AL

Ecology and Management 17 15ndash33 httpsdoiorg101007s11273-008-9093-7

IATTC(2015)Resolution on the conservation of mobulid rays caught in as-sociation with fisheries in the IATTC convention area Inter-AmericanTropical TunaCommission89thAnnualMeetingResolutionC-15-04LaJollaCAInter-AmericanTropicalTunaCommission

IFC(2012)Performance standard 6 Biodiversity conservation and sustain-able management of natural resources January 1 2012WashingtonDCInternationalFinanceCorporation

Innes J Pascoe S Wilcox C Jennings S amp Paredes S (2015)MitigatingundesirableimpactsinthemarineenvironmentAreviewofmarket-basedmanagementmeasuresFrontiers in Marine Science276httpsdoiorg103389fmars201500076

JanniseCSquiresDSeminoffJampDuttonP (2010)Conservationinvestments andmitigationTheCaliforniadrift gillnet fishery andpacificseaturtles InRQGraftonRHilbornDSquiresMTaitampMJWilliams(Eds)Handbook of marine fisheries conservation and management(pp231ndash240)OxfordUKOxfordUniversityPress

Jones E amp FrancisM (2012)Protected rays ndash Occurrence and devel-opment of mitigation methods in the New Zealand tuna purse seine fishery Auckland New Zealand National Institute of Water andAtmosphericResearch

KormosRKormosCFHumleTLanjouwARainerHVicturineR hellipWilliamson E A (2014) Great apes and biodiversity offsetprojectsinAfricaThecasefornationaloffsetstrategiesPLoS ONE9(11)e111671httpsdoiorg101371journalpone0111671

KotchenMJ (2013)Voluntaryand information-basedapproachestoenvironmentalmanagementApubliceconomicsperspectiveReview of Environmental Economics and Policy 7(2) 276ndash295 httpsdoiorg101093reepret012

Kyriazi Z LejanoRMaes FampDegraer S (2015)Bargaining a netgaincompensationagreementbetweenamarinerenewableenergydeveloperandamarineprotectedareamanagerMarine Policy6040ndash48httpsdoiorg101016jmarpol201506005

LentRampSquiresD(2017)ReducingmarinemammalbycatchinglobalfisheriesAneconomicsapproachDeep Sea Research Part II Topical Studies in Oceanography 140 268ndash277 httpsdoiorg101016jdsr2201703005

Lewison R L Crowder L B Read A J amp Freeman S A (2004)Understanding impactsof fisheriesbycatchonmarinemegafaunaTrends in Ecology amp Evolution19598ndash604httpsdoiorg101016jtree200409004

MannC (2015)StrategiesforsustainablepolicydesignConstructiveassessmentofbiodiversityoffsetsandbankingEcosystem Services16266ndash274httpsdoiorg101016jecoser201507001

Marine Stewardship Council (2014 June 21) MSC fisheries certifica-tion requirements v20 [pdf doc] httpswwwmscorgdocumentsscheme-documentsfisheries-certification-scheme-documentsfisheries-certification-requirements-version-20

MaronM IvesCDKujalaHBullJWMaseykFJBekessyShellip Possingham H P (2016) Taming a wicked problem Resolvingcontroversies inbiodiversityoffsettingBioScience66(6)489ndash498httpsdoiorg101093bioscibiw038

MaxwellSLMilner-GullandEJJonesJPKnightATBunnefeldNNunoAhellipRhodesJR(2015)BeingsmartaboutSMARTenvi-ronmentaltargetsScience3471075ndash1076httpsdoiorg101126scienceaaa1451

Moilanen A Van Teeffelen A J Ben-Haim Y amp Ferrier S (2009)Howmuch compensation is enoughA framework for incorporat-inguncertaintyandtimediscountingwhencalculatingoffsetratiosfor impactedhabitatRestoration Ecology17 470ndash478 httpsdoiorg101111j1526-100X200800382x

MorarNToadvineTampBohannanBJ(2015)Biodiversityattwenty-fiveyearsRevolutionorredherringEthics Policy amp Environment1816ndash29httpsdoiorg1010802155008520151018380

OrphanidesCDampPalkaDL(2013)Analysisofharborporpoisegill-netbycatchcomplianceandenforcement trends in theUSnorth-western Atlantic January 1999 to May 2010 Endangered Species Research20251ndash269httpsdoiorg103354esr00499

Pascoe S Innes J Holland D Finas M Theacutebaud O TownsendR hellip Hutton T (2010) Use of incentive-based managementsystems to limit bycatch and discarding International Review of Environmental and Resource Economics 4 123ndash161 httpsdoiorg10156110100000032

PhalanBHayesG Brooks SMarshDHoward PCostelloeBhellip Whitaker S (2017) Avoiding impacts on biodiversity throughstrengthening the first stage of the mitigation hierarchy Oryxhttpsdoiorg101017S0030605316001034

Queacutetier F Regnery B amp Levrel H (2014) No net loss of biodiver-sity or paper offsets A critical review of the French no net losspolicy Environmental Science amp Policy 38 120ndash131 httpsdoiorg101016jenvsci201311009

RadzioTASmolinskyJAampRoosenburgWM(2013)Lowuseofre-quiredterrapinbycatchreductiondevicesinarecreationalcrabpotfisheryHerpetological Conservation and Biology8222ndash227

RaineyHJPollardEHBDutsonGEkstromJMLivingstoneSRTempleHJampPilgrimJD(2015)AreviewofcorporategoalsofnonetlossandnetpositiveimpactonbiodiversityOryx49232ndash238httpsdoiorg101017S0030605313001476

Rausser G C Hamilton S F Kovach M amp Stifter R (2009)UnintendedconsequencesThe spillovereffectsof commonprop-ertyregulationsMarine Policy3324ndash39httpsdoiorg101016jmarpol200803020

Rice J (2014) Evolution of international commitments for fisheriessustainability ICES Journal of Marine Science Journal du Conseil71157ndash165httpsdoiorg101093icesjmsfst078

RichardYampAbrahamER(2013)ApplicationofPotentialBiologicalRemoval methods to seabird populations New Zealand AquaticEnvironmentandBiodiversityReport108

RodeJGoacutemez-BaggethunEampKrauseT(2015)Motivationcrowd-ingbyeconomic incentives inconservationpolicyAreviewoftheempiricalevidenceEcological Economics117270ndash282httpsdoiorg101016jecolecon201411019

RogersAA(2013)SocialwelfareandmarinereservesIswillingnesstopayforconservationdependentonmanagementprocessAdiscretechoiceexperimentoftheNingalooMarineParkinAustraliaCanadian Journal of Agricultural EconomicsRevue Canadienne Drsquoagroeconomie61217ndash238httpsdoiorg101111cjag12008

Rosenberg A A amp McLeod K L (2005) Implementing ecosystem-basedapproachestomanagementfortheconservationofecosystemservicesMarine Ecology Progress Series300 270ndash274 httpsdoiorg103354meps300270

Segerson K (2010) Can voluntary programs reduce sea turtle by-catch Insights from the literature in environmental economics InRQGraftonRHilbornDSquiresMTaitampMJWilliams(Eds)Handbook of marine fisheries conservation and management(pp618ndash629)OxfordUKOxfordUniversityPress

Serafy JECookeS JDiazGAGraves JEHallMShivjiMampSwimmerY(2012)CirclehooksincommercialrecreationalandartisanalfisheriesResearchstatusandneedsforimprovedconser-vation and management Bulletin of Marine Science 88 371ndash391httpsdoiorg105343bms20121038

ShiodeDHu F ShigaM Yokota K amp Tokai T (2005)Midwaterfloatsystemforstandardizinghookdepthsontunalonglinestore-duce sea turtleby-catchFisheries Science71 1182ndash1184httpsdoiorg101111j1444-2906200501080x

Sims M Cox T amp Lewison R (2008) Modeling spatial patternsin fisheries bycatch Improving bycatch maps to aid fisheriesmanagement Ecological Applications 18 649ndash661 httpsdoiorg10189007-06851

emspensp emsp | emsp15MILNER- GULLAND Et AL

Squires D amp Garcia SM (2014) Ecosystem-level impacts of fisheries bycatch on marine megafauna Biodiversity conservation through miti-gation policy economic instruments and technical changeReportofthe IUCN-CEM-FEGScientificworkshopGland Switzerland 7ndash10October2013GlandSwitzerlandIUCN

SquiresDampGarciaSM(inpress)Fisheries bycatch in marine ecosys-tems Policy economic instruments and technical change ChichesterUKJWileyampSons

SwimmerYArauzRMcCrackenMMcNaughtonLBallesteroJMusylMhellipBrillR(2006)DivingbehavioranddelayedmortalityofoliveridleyseaturtlesLepidochelys olivaceaaftertheirreleasefromlongline fishing gearMarine Ecology Progress Series323 253ndash261httpsdoiorg103354meps323253

TolottiMTFilmalterJDBachPTravassosPSeretBampDagornL(2015)BanningisnotenoughThecomplexitiesofoceanicsharkmanagementbytunaregional fisheriesmanagementorganizationsGlobal Ecology and Conservation 4 1ndash7 httpsdoiorg101016jgecco201505003

Tuck G N Polacheck T amp Bulman C M (2003) Spatio-temporaltrendsoflonglinefishingeffortintheSouthernOceanandimplica-tionsforseabirdbycatchBiological Conservation1141ndash27httpsdoiorg101016S0006-3207(02)00378-6

UNEP-WCMC(2016)Marine no net loss A feasibility assessment of imple-menting no net loss of biodiversity in the seaCambridgeUKUnitedNationsEnvironmentProgramme

Vaissiegravere A-C Levrel H Pioch S amp Carlier A (2014) Biodiversityoffsets for offshore wind farm projects The current situation inEurope Marine Policy 48 172ndash183 httpsdoiorg101016jmarpol201403023

Wallace B P Heppell S S Lewison R L Kelez S amp CrowderL B (2008) Impacts of fisheries bycatch on loggerhead tur-tles worldwide inferred from reproductive value analy-ses Journal of Applied Ecology 45 1076ndash1085 httpsdoiorg101111j1365-2664200801507x

Wanless R M Ryan P G Altwegg R Angel A Cooper JCuthbert R amp Hilton G M (2009) From both sides Dire de-mographic consequences of carnivorous mice and longlining for

the critically endangered Tristan albatrosses on Gough IslandBiological Conservation 142 1710ndash1718 httpsdoiorg101016jbiocon200903008

WardP LawrenceEDarbyshireRampHindmarshS (2008) Large-scale experiment shows that nylon leaders reduce shark bycatchandbenefitpelagiclonglinefishersFisheries Research90100ndash108httpsdoiorg101016jfishres200709034

WardTampPhillipsB(2010)SeafoodecolabelingInRQGraftonRHilbornDSquiresMTaitampMJWilliams(Eds)Handbook of ma-rine fisheries conservation and management (pp 608ndash617) OxfordUKOxfordUniversityPress

WilcoxCampDonlanCJ (2007)Compensatorymitigationasasolu-tion to fisheries bycatch-biodiversity conservation conflictsFrontiers in Ecology and the Environment 5 325ndash331 httpsdoiorg1018901540-9295(2007)5[325cmaast]20co2

WilcoxCampDonlanCJ (2009)NeedforaclearandfairevaluationofbiodiversityoffsetsforfisheriesbycatchConservation Biology23770ndash772httpsdoiorg101111j1523-1739200901173x

Wolf SHartlBCarrollCNeelMCampGreenwaldDN (2015)Beyond PVAWhy recovery under the Endangered Species Act ismorethanpopulationviabilityBioScience65200ndash207httpsdoiorg101093bioscibiu218

ZedlerJBampCallawayJC (1999)TrackingwetlandrestorationDomitigation sites follow desired trajectories Restoration Ecology 769ndash73httpsdoiorg101046j1526-100X199907108x

Žydelis R Wallace B P Gilman E L amp Werner T B (2009)Conservation of marine megafauna through minimization of fish-eries bycatch Conservation Biology 23 608ndash616 httpsdoiorg101111j1523-1739200901172x

How to cite this articleMilner-GullandEJGarciaSArlidgeW etalTranslatingtheterrestrialmitigationhierarchytomarinemegafaunaby-catchFish Fish 2018001ndash15 httpsdoiorg101111faf12273

Page 6: Translating the terrestrial mitigation hierarchy to marine ......of marine megafauna by-catch in fisheries, going from defining an overarching goal with an associated quantitative

6emsp |emsp emspensp MILNER- GULLAND Et AL

TABLE 3emspSummaryofoptionsforby-catchmitigationstructuredaccordingtothemitigationhierarchyforfourcase-studies

Fram

ewor

k st

ep

Cas

e- st

udy

Alb

atro

sses

lon

glin

esTu

rtle

slo

nglin

esRa

ysp

urse

sei

nes

Oce

anic

whi

tetip

slo

nglin

es

Definingtheproblem

Fisheryandspatial

extent

Braziliandomesticindustrialcoastallongline

fleet

EasternPacific(coastalandpelagic)

small-scalecommerciallonglinefishery

Tunapurse-seinefisheryof

theeasternPacific

AsianandEUlonglinetunafisheriesinthe

Indi

an o

cean

Targetspecies

Variousspeciesofsharkandswordfish

Mahi-mahi(

Cory

phae

na h

ippu

rus

Coryphaenidaeseasonal)tunasharks

(mostlysilkyC

arch

arhi

nus f

alci

form

is

Carcharinidae)billfish

Variousspeciesoftuna

Variousspeciesoftuna

By-catchspeciesof

conc

ern

Albatrossamppetrelspeciesparticularconcern

forcriticallyendangeredTristanalbatross

(Dio

med

ea d

aben

nenaDiomedeidae)

Oliveridley(L

epid

oche

lys o

livac

ea

Cheloniidae)greenblack(C

helo

nia

myd

asCheloniidae)hawksbill

(Ere

tmoc

hely

s im

bric

ataCheloniidae)

loggerhead(PeruandMexico)and

leatherback(D

erm

oche

lys c

oria

cea

Cheloniidae)

Sevenmobulidspecies

includingCITES-listedM

anta

bi

rost

ris(Mobulidae)and

M a

lfred

i(Mobulidae)

caughtmostlyalivein

dolphin-associatedor

free-schoolsets

OceanicwhitetipsharkVulnerableonIUCN

redlistretentionbannedbytunaRFMOs

listedonCITESAppendixII

By-catchtarget

(Δλ T)

BraziliangovernmentMinimizeby-catch

Rulesfocusontargetsforuseofminimizing

measuresratherthanonby-catchnumbers

NotwelldefinedRFMOssuggest

minimizingby-catchCouldconsiderPBR

foroliveridleyszerocatchforleather-

backs(reflectingtheirrespective

populationstatus)

IATTC(2015)zeroretention

storingorsellingandlive

releaseofby-caughtrays

whenpossibleImplies

by-catchminimization

Targetby-catchlevelnotdefineddueto

uncertaintyRFMOsbanretentionlanding

andtrans-shipment

Mitigationhierarchyelement

Avoid

[timeareaclosuresnight-timesetting]

[timeareaclosuresdeeperlines]

[timeareaclosures]

[deepsetting]

Minimize

[torilineslineweights]

[monofilamentlinecirclehooks(not

leatherbacks)]

ndash [hardtoavoidcatching]

[monofilamentlinecirclehooksbanon

steelleaders]

Remediate

ndash [hardtoreleasealive]

[improvedhandling]

[improvedhandling]

[shortsets]

Offset

[invasiveeradication]

[beachprotection]

[illegaltrade]

[informationgatheringillegaltrade]

Factorsaffectingoperationalization

Scopefor

incentives

Participatoryresearchonbarrierstouptakeof

minimizationmeasuresPositiveincentives

forthoseusingnewmeasurespaidforby

forexamplefisheries-widelevy

Certificationsustainabilitystandardsin

exportmarkets

Transitionalpaymentsto

promotebetterhandlingon

deckhenceimproving

survival

Ifinformationgatheringseenasavalidoffset

duetohighuncertaintyfundingatagging

schemecouldincentivizefisherstocollect

dataonsharkcatchratesurvivalof

releasedsharksby-catchhotspotsto

supportimprovementsacrossthewhole

mitigationframework

(Continues)

emspensp emsp | emsp7MILNER- GULLAND Et AL

themitigationhierarchy In theabsenceofhighqualitypopulationdatawithwhichtoparameterizeamodelaPBR-basedapproachisbeingusedtosetatargetby-catchlevel intermsofnumberof in-dividualsofeachoftheturtlespeciescaughtinthefisheryExpertopinionfromfishersandProdelphinusstaffsupplementedbydatafromalong-runningby-catchobserverprogrammeoperatingoutoftheport(Alfaro-Shiguetoetal2011)givesthepotentialreductioninturtleby-catchnumbersasaresultofagivenmitigationapproachInterviews and focus groups with fishers provide understandingof their preferences for different by-catchmitigation approachesbarriers and constraints to implementation and potential partici-pationindifferentincentiveschemesthiscanbesupplementedbyDiscreteChoiceExperimentsprovidingempiricalestimatesforpref-erencesforcombinationsofby-catchreductionmeasures(cfRogers2013)Thisfieldresearchproducesashort-listoffeasiblemitigationmeasuresateachstageinthemitigationhierarchyforcostingandtesting(egspecificareasortimesforfisheryclosureunderavoid-ancecombinationsofhooktypesandnetmodificationundermini-mizationtraininginturtlehandlingandreleaseforremediationandimprovingby-catchperformanceofothergeartypesintheareaforoffsetting)Thisenablestheanalysisoftheeffectivenessandcostof various combinations of by-catch reduction strategies framedwithinthefourstepsofthemitigationhierarchy(avoidminimizere-mediateoffset)withacleartargetby-catchreductiongoalinmind

4emsp |emspCOMPARING KE Y DEBATES BET WEEN TERRESTRIAL NNL AND BY- C ATCH MITIGATION

41emsp|emspThe hierarchical nature of mitigation

Terrestrial situationsareusuallyviewedas requiringastricthierar-chywithavoidanceminimizationandremediationtakingprecedenceoveroffsetsPartofthereasonforthishierarchymaybesocietalval-uesandexpectationsbut also it is a reflectionof reversibility anduncertaintyTheterrestrialmitigationhierarchywassetuptoaddresshabitatdestructioncausedbydevelopmentwhich iseffectively ir-reversiblehenceavoidanceisstrictlypreferredfromaconservationperspective Inpractice avoidancehasbeenaneglected step andmuchofthedisquietaboutbiodiversityoffsettinghasbeenbecauseofthetendencytopaylipservicetoavoidanceandfocusinsteadonoffsetswhich thenmay be implemented on paper only (HoughampRobertson2009Phalanetal2017)EvenwithperfectenforcementandcompliancewithmeasuresfurtherdownthemitigationhierarchythestrictavoidanceofhabitatlossismorecertaintolimitimpactthanreducinglossesinthecourseofapotentiallydamagingactionwhichismorecertainthanrestoringdamageafterthefactorcompensatingforitwithactionselsewhereOfteninterrestrialsystemsmultipliersareusedattheoffsetstagetoreflectthisuncertaintyrequiringthatanadditionalamountofequivalentlandisprotectedinanoffsetoverandabovetheamountthatislostduringthedevelopment(withtheratiooflandoffsettolanddestroyedinthe10sto100sdependingonthecircumstancesMoilanenVanTeeffelenBen-HaimampFerrierFr

amew

ork

step

Cas

e- st

udy

Alb

atro

sses

lon

glin

esTu

rtle

slo

nglin

esRa

ysp

urse

sei

nes

Oce

anic

whi

tetip

slo

nglin

es

Major

uncertainties

Lackofspecies-levelidentificationof

by-catchlackofunderstandingof

compliance

Lackofecologicalknowledgeofturtle

populationtrendsampdistribution

Potentialforsignificantadditional

by-catchfromcoastalgillnetfishery

Impactofcatchonmobulid

survivalPredictorsof

mobuliddistributions

Lackofobserversorreportingsoverylimited

understandingofby-catchlevelsspatio-

temporalencounterhotspotspost-release

survivalcompliance

Keyobstacle

Compliancewithexistingrulesmustbe

improved

Fundingforalternativestofishingata

largeenoughscaleLongtimelagand

uncertaintyinoffseteffectiveness

Limitedknowledgeofmobulid

distributionsmakes

avoidancedifficult

Lackofmonitoringlimitsoptions

Overallassessment

Existingmeasuresforimprovingimplementa-

tionofminimizationstepalreadyexistbut

needincentivizingoffsettingcouldprovide

short-termgainstocomplementthese

Targetedfundingcouldfacilitateimprove-

mentsthroughoutthehierarchyBest

approachmaydifferbyspecies(particu-

larlyleatherbacksvsothers)

Focusonremediationstepis

currentlythemainoption

avai

labl

e

Somepotentialforminimizationthrough

deepsettingbutchallengingtochange

behaviourinthisfisheryelectronic

monitoringsystemswouldhelp

Keyreferences

BugoniManciniMonteiroNascimentoamp

Neves(2008)Wanlessetal(2009)

Alfaro-ShiguetoDuttonampMangel(2007)

Halletal(2012)Andrakaetal(2013)

JonesampFrancis(2012)Hallamp

Roman(2013)Crolletal

(2016)Fowler(2016)

Tolottietal(2015)

Ticksindicatethepotentialforactionatdifferentstepsofthehierarchybasedonfeasibilitycurrentknowledgeandimpactonmortality(

=highpotential

=somepotential

=limitedpotential

ndash=nopotential)TextinbracketsgivessuggestedmeasuresateachlevelofthehierarchytheseareillustrativeratherthandefinitiveTheinformationforthecase-studiesisbasedontheexpertknowledge

oftheauthorsthroughtheirinvolvementinmanagementoftheby-catchissueinthesefisheriesRFMOregionalfisheriesmanagementorganizationPBRpotentialbiologicalremoval

TABLE 3emsp(Continued)

8emsp |emsp emspensp MILNER- GULLAND Et AL

2009)Bycontrastinfisheriessettingstherehavebeensuggestionsthatdependingonthelegalenvironmentitmaybemoreappropriateforoffsetstobeusedaspartofaleast-costconservationapproachalongsidemoretraditionalmitigationmethodsratherthanasthelaststep inamitigationhierarchy (DuttonJosephSquiresampWilliams2011DuttonampSquires2008WilcoxampDonlan2007)

42emsp|emspOut- of- kind offsets

Out-of-kind offsets are those which do not act to increase theimpact-affectedbiodiversityIntermsofourconceptualframeworktheyareoffsetswhichdonotacttoincreasethepopulationgrowthrateoftheby-catch-affectedfocalpopulation(Equation1)Forex-ampleonesuggestedbenefitof raising funds foroffsetting fromaby-catchtaxonfishersisthattheproceedsfromsuchataxcanfinanceoffsetselsewherewithintherangeoftheby-catch-affectedpopulation (Dutton amp Squires 2008) Although not a true offsetunderamitigationhierarchyfundsfromtheCaliforniadriftgillnetindustry in 2002 financed sea turtle nesting site conservation inBajaCaliforniaforcompensatorymitigationofseaturtleby-catch(Jannise Squires Seminoff amp Dutton 2010) In terrestrial (andmarine)systems itcanbemorechallengingtodefinethe impact-affected biodiversity because impact is rarely as clearly linkedtoagivenspeciesandstockas it is forby-catchBecauseofthisthelocationandbiodiversitytargetofconservationactionsfallingundertheldquooffsetrdquoheadinghassometimesbeenlooselyrelatedtotheactual impactBest-practicestandardsstatethatoffsetsmustbeimplementedasclosetothedamagingactivitiesaspossibleandfocusonbiodiversityassimilaraspossibletothatwhichhasbeenimpacted (BBOP 2012) However there have also been calls forldquoout-of-kindrdquooffsetsthatgivemoreconservationbang-for-buckbyfocussingonthreatenedspeciesorrarehabitatsorareasinneedofconservation rather than the impactedareasor specieswhichmay be considered less ldquovaluablerdquo for conservation (Bull Hardyetal2015)Thishasledtosubstantialdebateastotheappropri-atelimitsonthegeographicscaleandbiodiversityfocusforoffset-ting(egApostolopoulouampAdams2017)Italsodrawsattentiontothesubjectiveanduser-definednatureof theword ldquobiodiversityrdquo(Morar ToadvineampBohannan 2015) As it is impossible fully tooperationalizetheconceptimplementersofthemitigationhierar-chyhavelatitudetointerpretbiodiversityaccordingtoforexampleeaseofmeasurement perceived societal valueormitigation cost(Maron etal 2016) In our casewe take a narrow focus on theby-caughtspecies itself this is in linewithmuchof the literatureon by-catch but notwith the broader discourses on ecosystem-basedapproachestomarinemanagementandecosystemservices(RosenbergampMcLeod2005)Thesediscoursessuggest theneedforamorefunctionalecosystem-basedapproachtononetlossofbiodiversitythishasyettotranspireeitherinthemarineorintheterrestrialliteraturepossiblybecausesubstantialchallengesinde-finingimpact-affectedbiodiversitytheninevitablyensue

Asmarinemegafauna stocks are often transboundary andmi-gratorydefiningtheappropriatespatialunit foroffsettingmaybe

achallengebecause themosteffective location foranoffsetmayormaynotbewithintheareaofinfluenceofagivenfisheryClearlyandpreciselydefining the spatial unitwithinwhich themitigationhierarchywill be implemented during theprocess of defining theoverallgoal(suchasNNL)isvitalThisunitshouldreflectthescaleoverwhichanactionwillaffectλToffsetswhicharewithinthedis-tributionofthefocalstockoftheby-caughtspecies(asdefinedforEquation1)arenotout-of-kindHoweverchallengesemergewhenthe appropriate spatial unit for offsetting activities is different totheappropriatespatialunitforotherelementsofthemitigationhi-erarchywhicharelikelytobedefinedinsteadbyjurisdictionalareaor target fish stock distribution Inmany fisheries the species af-fectedbyby-catchmaynotbewellenoughknownandoffsetsmayaccordinglyneedtobebroadlytargetedtobenefitanypotentiallyaffectedspeciesTrueout-of-kindoffsetswouldincludefundingtheconservationofunaffectedspeciesorstocksofhabitatsnotusedbythefocalstockorcontributionstoaconservationfundwithoutaclearcommitmentthatthefundsaretobespentonincreasingλT for thefocalby-caughtstockTheseareunlikelytoformpartofbest-practiceguidanceforby-catchoffsets

43emsp|emspResearch as an offset

Arelatedareaofactivecontroversyformarineby-catchiswhetherresearchor informationgatheringshouldbeseenasavalidoffsetmechanism The rationale is that this research could be used toreduceuncertaintypromote innovationand thereby improveout-comes for by-caught species albeit indirectly An offset could beusedto incentivizebetterdatacollectionfor instanceusingaby-catchlevytopayfortaggingortoputby-catchobserversorelec-tronicmonitoringsystemsonboatsThismightbeapreludetolatermitigation or avoidance activities once more is known about thebiological settingWhether research activities could appropriatelybeconsideredaspartofanldquooffsetrdquoiscontroversialmdashinsomecasesan indirectbenefit to theby-caught stockmightbe clearly appar-ent(egtheoceanicwhitetip(Carcharinus longimanusCarcharinidae)case-studyinTable3)whileinothercasesusinginvestmentinre-searchasanoffsetcouldbeseenasacaseofmoralhazardpoten-tially compromising scientistsrsquo independence and having at best ahighlyindirectrelationshiptoNNLoftheby-caughtspeciesAnotherviewisthatreducinguncertaintyisacoreresponsibilityofoperatingafisherywhichthereforeshouldbebornebythemanagementau-thorityorfishingbusinessesInterrestrialsystemsthesedilemmasalsoexistbutthesentimentismuchmoreclearlyexpressedthatre-searchactivitiesarenotappropriateoffsets(BullGordonWatsonampMaron2016)

44emsp|emspIncentivizing implementation of mitigation measures

Thefactorsthatdrivedecision-makingaboutmegafaunaby-catchreduction (by skippers companies fishery managers policymak-ers and other stakeholders) include legal obligations tominimize

emspensp emsp | emsp9MILNER- GULLAND Et AL

by-catch at the national or international levels (eg FAO 2011Rice 2014) the availability and quality of technical fixes associ-atedcosts tofishers limitsonaccesstoseafoodmarketsaswellassocietalpressuresHowevermuchresearchonby-catchreduc-tion focuses on identifying and implementing technicalmeasuresto reduceBPUE rather thanon the social andeconomicbarriersto implementation (Campbell amp Cornwell 2008) Technologicalinnovation to improve BPUE needs to be appropriately incentiv-izedwitheffortsmadetoensurethatsuchmeasuresareascost-effective as possible for fishers (Gjertsen Hall amp Squires 2010Lent amp Squires 2017) However it often happens that even ap-parently suitable by-catchmeasures are notwidely implemented(eg Damalas amp Vassilopoulou 2013 Orphanides amp Palka 2013RadzioSmolinskyampRoosenburg2013)Inthesecasesthedegreeofnon-implementationandthereasonsbehinditneedstobeun-derstoodsoitcanbeaddressed(Coxetal2007)Thesetypesofconsiderationarealsonotwellresearchedintheterrestrialoffset-tingliteraturebecausecomplianceispoorlymonitored(BullSuttleGordonSinghampMilner-Gulland2013)andthereislittlesupportfor researchon thebarriers to implementationofamitigationhi-erarchyandhowtosupportdeveloperstoaddressthesebarriers(BullBryantBakerampMilner-Gulland2015)Thesocialimpactsofimplementingabiodiversitymitigationhierarchyonresourceusersarementioned inguidance (egBBOP2012)buthowtomeasureandaccountforthemisverypoorlyunderstoodThefewstudiesin-vestigatingdeliveryofpromisedoffsetmeasuresinterrestrialsys-temssuggestaverypoorrecord(QueacutetierRegneryampLevrel2014)Therefore the social side of implementing the mitigation hierar-chyand incentivizingcompliance isanarea thatneedsmore andmoreactiveresearchwithinboththeterrestrialandmarinerealms(FultonSmithSmithampvanPutten2011)Thisisparticularlytruewhentheburdenof implementingmitigationapproaches isbornebyrelativelysmall-scaleproducersratherthangovernmentsormul-tinationals(egthepelagiclonglinefisheriesinTable3)

45emsp|emspSocietal limits

Foraspeciesathighriskofextinctioncompleteavoidanceofby-catchmightbethemostdesirablepolicyfrombothamanagementagency and societal perspective In addition with emblematic orhighlythreatenedmarinemegafaunaitmaybeviewedbymembersof the public asmorallywrong to kill any individuals even ifmiti-gationisinplace(egMauirsquosdolphinHamneretal2014) leadingtopressureongovernmentstoreflectthisethicalconcerninregu-lationsThesedilemmasecho the issueof thresholds in terrestrialoffsetswhichrecognizesthattherearesomecriticalareasinwhichdevelopmentisnotsocietallyappropriateregardlessofthepoten-tialformitigationandotherareasinwhichthemitigationhierarchycan be appropriately applied (Bull etal 2013) Examples of loca-tionswhereathresholdapproach isseenasappropriate interres-trial systems include the habitat of highly endangered species orecosystemswhich are limited in extent and irreplaceable (such asoldgrowthforest) In terrestrialsystems therefore themitigation

hierarchyisseenasmostappropriateforapplicationinmorecom-monanddegradedhabitatssuchasfarmlandSimilarlyinfisheriestheremaybesomesituationsinwhichthestockssubjecttoby-catchare so precious or threatened that no level of threat from fishingcanbecontemplatedandotherswherefishingsubjecttoNNLandthemitigationhierarchyisasociallyacceptableapproachInsitua-tions inwhich trade-offs between conservation and developmentareseenasnecessaryoracceptablebywidersocietyasociallicencetooperatemaybegainedthroughadoptingoffsetsintheabsenceofregulationForexampleinsub-SaharanAfricaseverallargedevel-opmentprojectsareattemptingtooffsettheirimpactsongreatapesandtheirhabitats(Kormosetal2014)Aby-catchequivalentmightbe fishing companies voluntarily donating funds for turtle nestingbeachrestorationintheirareaofoperationinadditiontocomply-ingwithregulatoryby-catchmitigationmeasuresThesemeasuresmayimprovetheimageofthecompanywiththegeneralpublicbuttoavoidaccusationsofldquogreenwashingrdquotheireffectivenessneedstobeproperlyscrutinized(Bulletal2016)Transparentlyembeddingthesetypesofactionswithinamitigationhierarchysuchasweareproposing and critically evaluating their contribution to increasingthepopulationgrowthrate(asperEquation1)wouldbeonewaytopromptsuchscrutiny

46emsp|emspUncertainty

The nature of the uncertainties surrounding biology and enforce-ment in themarine setting raisesquestions about theorderingofsteps in themitigationhierarchy inaway that isdissimilar to ter-restrialsystemswherethehierarchyofuncertaintiesmaybecleareranduncertaintyisgenerallylowerForexampleitmaybethattheimpactonoverallpopulationgrowthrateofanoffsetmeasurelikeeradicating invasivespecies fromaseabirdnestinghabitat isbothless uncertain and more cost-effective than avoidance measuressuchasclosingareaswhichmayormaynotbefrequentedbyadultseabirds in a given time-periodGenerally though itmightbe as-sumedthatmeasureswhichtargetlifestagessubjecttohighlevelsofnaturalmortalityorwithinwhichindividualcontributiontoover-allpopulationgrowthrateislow(egheadstartingjuvenileturtles)maybelesseffectiveinachievingNNLthanmeasureswhichtargetreproductivelymatureadultfemales(suchaslivereleasesHeppellCrowderampCrouse1996)Howeverbeforeimplementinganoffsetthataimstoimprovethesurvivalofonelifestageinordertocom-pensatefortheby-catchmortalityofanotherarobustassessmentoftheconsequences(withassociateduncertainties)shouldbecar-ried out through detailed population modelling based on strongempiricalstudies(cfWallaceHeppellLewisonKelezampCrowder2008)Interrestrialsystemstherequirementsequentiallytoapplythemitigationhierarchyisbroadlyunchallengedbutactuallysimilararguments apply For example habitat restoration sits above off-settinginthehierarchyandyetitisalong-termuncertainprocesswhichmayinsomecircumstancesbemuchlesspreferabletoanoff-setusingawell-establishedapproachwhichishighlylikelytoleadtoconservationgains

10emsp |emsp emspensp MILNER- GULLAND Et AL

47emsp|emspTemporal considerations

Thetimingofoffsetsinrelationtootherelementsofthemitigationhierarchyhasbeenthesubjectofdebatewithintheterrestriallitera-tureThemainsuggestionforaddressingthetemporarylossofbio-diversitywhileoffsetscometofruitionhasbeenadoptingmitigationbankingwherebyoffsetsareimplementedinadvanceofpotentiallydamagingactivitiesprovidingbiodiversitycreditswhichcanbeusedtocompensateforlaterlossesThisbothremovesanelementofun-certaintyfromtheoffsetimplementationandreducesthetimelagbetweenlossandgain(Mann2015)Withrespecttomarinemega-faunaby-catchflexibilityintimingprovidesadditionalscopeforcostreduction and benefit enhancementwhichmay not be present intraditionalhabitat-basedterrestrialoffsetsForexampletemporarymeasuressuchasashort-termby-catchtaxtofundanoffsetmaybeusedifmitigationoravoidancemethodstaketimetocomeonlineorifatemporarynudgeisenoughtocausebehaviouralchangeThismightbethecaseifapolicywasneededtoinducefisherstotakeupnewgeartoavoidthecostofanoffsetorifconcernsaboutsafetyoryieldreductionsduringthetransitiontonewgearcouldbeallayedbyatemporarysubsidyforearlyadoptersorapaidparticipatorymoni-toringprogrammeto informwider implementation(egthemobu-lidandsharkcase-studiesinTable3)Justasforhabitatrestoration(ZedlerampCallaway 1999) by-catchoffset strategieswhich targetjuvenilestagesof long-livedspecies (eg turtleheadstartingor in-vasive removal fromseabirdnesting islands)may takemanyyearsfor their effects to become apparent in an increase in populationgrowthratesAdditionaluncertaintyisintroducedbythedifficultyinmonitoringpopulationsofmanyby-catch species (eg seabirdsHatch2003)leadingtouncertainestimatesoftheimpactofoffsetactivitiesonpopulationgrowth(seecase-studiesinTable3)Theseproblemsarenot insuperablehoweverpositivetrendshavebeenreportedinturtlepopulationsoverdecadesasaresultofnestpro-tection(egDuttonDuttonChaloupkaampBoulon2005)

5emsp |emspUSING INCENTIVES TO REDUCE BY- C ATCH

Manyoftheexamplesandprinciplesdiscussedaboveeitherimplic-itlyorexplicitlyrelatetotheeconomicsocialinstitutionalormoralincentivesoperatingondifferentactorsinsideandoutsidethefish-erywhichcanbepositiveornegativeWenowturntoadiscussionofhowincentivescanbeusedtoreduceby-catchwithinourframe-workIncentivescanbeputinplacetochangefisherbehaviourwithrespecttoanyoftheelementsoftheframework (avoidminimizeremediateandoffsetTable3)Althoughdiscussedintheliteraturemostof these incentive approaches are yet tobe implemented inthe realworldparticularly forby-catchThereforeuntil empiricalevidenceoftheireffectivenessisavailablethesesuggestionscomewithacaveat

Financial costsofby-catchmitigationactions canarise for in-stancefromlostcatchcapitalinvestmentsinnewgearormitigation

equipmentor the lossofaccesstoafisheryCostsmayalsoarisefromthedeploymentofby-catchobserversortrainingintheuseofnewgearThesecostscanbepaidbyfishingcompaniesorindivid-ualsorbygovernmentsNGOsorseafoodconsumersWhetherornotcompensationforcostsincurredbyfishersisseenasappropri-atedependsonwhetherby-catchreductionisseenasasocialgoodthatfishersareproviding(inwhichcasetheyshouldbecompensatedforit)orasputtingrighttheharmthattheyaredoingtobiodiver-sitywhilegeneratingtheirownprivategain(ineconomiclanguagewhetherby-catchisviewedasanunpricedexternalityinwhichcasetheyshouldpay)Italsodependsonwhethereconomichardshipwillensueacaseforcompensationofby-catchreductioncostsincurredbypeopledependenton fishing for their livelihoodsmaybemoresympatheticallyreceivedbyotheractorsthanacasemadebyalargemultinationalfishingcompany

Ifby-catchisseenasanunpricedexternalityitmightbesociallyoptimaltotaxfishersfortheirby-catchsothatthisexternalityisin-ternalizedThisplacesanexplicitpriceuponby-catch(Boyce1996Pascoeetal2010SquiresampGarcia2014)Theby-catchprice islikely to be incorporated into the price of the target species andtherebybecomespartofthetargetspeciescostThispricecouldbeset differently for different demographic classesof theby-caughtspecies depending on the impact the loss of an individualwouldhaveonthepopulationAllelsebeingequalputtingapriceonby-catchmeans that theseafoodproduct that is the targetcatchbe-comesmoreexpensiveandconsumershave topaymore for theirseafoodreducingdemandTheninprincipleeveryfirminthesup-plychaineveryvesselandeveryconsumerhaveanincentivetore-duceby-catchuntileacheconomicactorrsquosmarginalcostofby-catchreductionequals thecommonpriceofby-catch that theyall faceOffsetsareonewaytopriceandinternalizetheby-catchexternalitycostIfanoffsettingactioniscostlytoimplementandmustbepaidforwith each unit of by-catch it implicitly prices the residual by-catch In this circumstance the effect from a financial standpointisthesameasaby-catchtaxwiththe levelsetbasedonthecostoftheoffsetVariousinstitutionalstructurestosupportthischargeperunitofby-catcharepossiblewithdifferentimplicationsintermsofthedistributionofcostsandbenefitsForexampleaninsuranceschemecouldbepaidintobyfishersthatpaysoutintheeventofaby-catcheventtherebyspreadingthecostofunavoidablerareby-catcheventsOratradablepermitschemecouldoperatesuchthatfisherswhoexperienceaby-catcheventcanbuyapermitwiththecostvaryingdependingondemandforpermits (henceprovidingavessel-levelincentivetoinnovatetoreduceby-catch)

If there isdemandforconservation inan internationalmarketthen price premiums and market access (through eco-labellingsupply chain certification other food sustainability campaignsWardampPhillips2010)orboycottsactingasstrategicthreatsfromconsumers (Kotchen 2013 Segerson 2010) could act as positiveornegativeeconomic leversonthe fisheryprovidingan incentivefor fishers to reduce their by-catch voluntarily (as has been sug-gested for the Brazilianmahi-mahi fishery Table3) For exampletheMarine StewardshipCouncil now includesby-catchmitigation

emspensp emsp | emsp11MILNER- GULLAND Et AL

intheircertificationprocess(MSC2014)Demand-ledleversmaybemoreorlessapplicableatdifferentlevelsinthehierarchyforexam-pleavoidancemayberelativelyhardtoevidencewhileoffsettingmaybelesseasytoselltoaconsumerthanminimizationorreme-diationConcerns about the unintended consequences of positiveincentives (particularlyfordirectsubsidiesratherthanconditionalincentives)maydeterminewhethertheyareanappropriateinstru-mentinagivencaseForexampletheymaybeinappropriateifthereisariskthattheadditionalmoneyisreinvestedinincreasedfishingcapacityor iftheremaybeconsumptionproductionorconserva-tionleakages(transferoftheproblemsomewhereelse)whetheratthe vessel fishery or trans-national levelHigh transactions costsmayalsolimitthebenefitsofincentivesschemes

Otherchangeswhichmayneedtobeincentivizedforsuccessfulimplementationofby-catchreductionpoliciesmaybelessamenabletofinancialmeasuresatleastpartlybecauseitislessclearhowtoassign financial value to theactionsor to thebenefits and losseswhichtheyproduceForexampleperceivedreductionsinsafetyforfishingcrews(fromweightedlonglinesfor instance)arecoststhatmaybehardtovaluefinanciallyOtherprerequisitesfor long-termsustainable behaviour change such as changes in social norms sothatfishingcommunitiesseeby-catchreductionasappropriatebe-haviourortechnicalskillacquisitionsothattheycanusenewmeth-odsmaybeincentivizedbycarefullydesignedinterventionsworkingwithfishers(Halletal2007)Conservationpoliciesbasedoneco-nomic incentives (extrinsicmotivation) are not always superior tothosebasedupon intrinsicmotivation Infact incentive-basedby-catch reduction policy instruments could even be counterproduc-tivebyreducingtheeffectivenessofintrinsicmotivationdependingupon the situation (although the empirical evidence on this topicisweak RodeGoacutemez-BaggethunampKrause 2015) If the changerequiredforby-catchreductiontoworkmeetscultural resistancethenparticipatory researchmightbeespeciallyeffective inbreak-ingdownbarriersbetweenthosewhowantby-catchreductiontotakeplaceandthosewhoactuallyhavetoimplementit(thefishers)ForexampleinAustraliathegovernment-fundedbodyOceanwatchfacilitatesengagementbetweencommunities thefishing industryseafood suppliers and government to improve knowledge sharing(wwwoceanwatchorgau)Innovationiscrucialinfisheriesandfish-ersareaccustomedtoadoptingnewtechnologyorprocessespo-tentiallymakingan incentivizedparticipatory researchprogrammeespeciallyfruitful

Sometimes the most efficient way to solve problems is a so-cial instrumentoran institutionalchange inplaceoforaswellasan economic instrument For example supporting developmentof fisherorganizations rather than instituting a vessel-level taxorsubsidy might provide the impetus needed to change behaviourInstitutingcatchshares(individualtransferablequotas)mayprovideanenablingenvironmentforby-catchreductionforexamplebypro-motingmoreeffectivemonitoring(Grimmetal2012)Experiencein terrestrial system produces similar insights incentive-basedschemeswhichalsobuildcommunitycohesionandsupportthede-velopment or strengthening of localmanagement institutions are

more effective in the longer run than direct economic incentives(Clementsetal2010)

6emsp |emspCONCLUSIONS

The framework we present here is novel It draws upon and ex-tends the frameworks for conceptualizing by-catch developed byHall (1996) and Hall Alverson andMetuzals (2000) It amalgam-atesHallrsquos frameworkwith themitigationhierarchyasused in theEnvironmental Impact Assessment literature (BBOP 2012) Thesuggestions about goals metric andmitigation actions are drawnfromtheempiricalby-catchliteratureandtheissueswediscussin-tegratetheconcernsoftheextensiveterrestrialandnascentmarineoffsetting literature with the by-catch literature The frameworkmakesclear thatanearlycrucial step is toclarify thegoalofanyby-catch reduction policyOverarching goals like those issued bytheConventiononBiologicalDiversity(egAichiTarget11that10ofmarinehabitatshouldbeunderprotectionby2020)needtobetranslatedintooperationaltermswithineachfisheryCurrentlyleg-islatedoragreedby-catch reductiongoals tend tobe less specificthantheycouldbeandthisleadstoproblemsininterpretingthesegoals inordertoplanaby-catchmitigationstrategy(seethecase-studies inTable3 for examples) This ambiguity is tobe expectedwithinnegotiatedtargetsbutitisachallengenonetheless(Maxwelletal2015)Usingacommonunitofby-catch impactsuchastheΔλTwhichweuseherewouldbehelpfulbothinclarifyingexpecta-tionsandevaluatingtheeffectivenessofelementsofthemitigationhierarchy

Once the by-catch goal is known options for implementingavoidanceminimizationremediationandoffsetscanbeclarified(asinTable2)Howeveroutsideof the interconnectedbiologyof theecosystemby-catch isembeddedwithinsocialandeconomicsys-temsDifferentunitsofanalysismaybeneededatdifferent levelsofthehierarchytocopewiththechallengesofincompleteoverlapbetween jurisdictional units fisheries target stocks and by-catchstocksJurisdictionalissuesareimportantandcomplexpotentiallyimpeding implementationFleets interact raisingtheriskofpolicyleakageforexampleifpeopleshifttootherfisheriesgearorliveli-hoodsThereforethescaleatwhicheachelementofthemitigationhierarchyisimplementedislikelytovarywithincentivestomitigateoftenbeingbest appliedat thevessel level focussedon reducingindividualmortalitywhileoffsettingisimplementedatthescaleoftheby-catchspeciesrsquostockWithtransboundaryspeciesunilateralconservationinonejurisdictioncreatesthepotentialforproductiontrade and conservation leakages For example a conserving Statecouldimplementtheavoidancestepandshutdownordramaticallycurtailitsownproductionofswordfishtoreduceseaturtleby-catchbuttheknock-oneffectmaybemoreimportationofswordfishfromfleetswithhigherseaturtleby-catch(RausserHamiltonKovachampStifter2009)

Translatingtheframeworkfromaspeciestoanecosystemlevelwill require consideration of the potential interactions between

12emsp |emsp emspensp MILNER- GULLAND Et AL

by-catchmitigationapproachestargetedatdifferentspecies(Serafyetal 2012) Actions to mitigate by-catch for one group of spe-cies can increase or decrease it for others and so a system-wideapproach isneededForexample changing fromJ-hooks tocirclehookstoreducemortalityofturtlesmaydecreaseorincreasesharkmortality(Andrakaetal2013GodinCarlsonampBurgener2012)In terrestrial systems similar interactions arise and value judge-mentsaremade(whetherexplicitlyorimplicitly)astowhatlossandgain of ldquobiodiversityrdquo translates to in operational terms andwhatelementsofbiodiversitymattermosttoimplementers

Uncertainty is high in ocean ecosystems creating both chal-lengesandopportunitiesinapplyingtheconceptofNNLthroughamitigationhierarchythatincludesoffsettingInparticularformarinemegafaunathereishighuncertaintyintheprocesseslinkinganyel-ementofthemitigationhierarchythroughtochangesinpopulationgrowthrateFurthermore impactscanbelong-termhardtomea-sureandspatiallydiffuseanduncertaintyisnotpredictablyspreadthroughthehierarchyThiscreatesadifferentsetofchallengestothosefacedinterrestrialsystemswhereatleastforsometypesofenvironmentalimpactthelinksbetweenactionandimpactarerel-ativelydirectandmeasurableanduncertaintygenerally increasesthroughthemitigationhierarchy (fromavoidthroughminimizere-mediatetooffset)

By-catch reduction measures have had significant successesoverthelastdecadesasaresultofsubstantialinvestmentoftimeand funding by researchers management authorities conserva-tionorganizationsandfishers(Coxetal2007)Howeverthissuc-cessisnotuniversalJustasforanyfisheriesmanagementissueapoorregulatoryregimelimitedcomplianceandlackofinforma-tionhampereffortstoreduceby-catchInsomeplaceshighlevelsofby-catch limitedoptions formitigationandweakgovernance(leadingtopoorenforcement)cancombinetomaketheby-catchproblemintractableOurframeworkwillnotsolvetheseproblemsHowever itbrings together the full rangeofapproaches forby-catchmitigationinastructuredandsystematicwaywhichrequiresatargettobeexpressedagainstwhichoutcomescanbeevaluatedByexposingareasofuncertaintyanddatadeficiencyitcouldchal-lengescientistsandmanagerstoobtainthedatarequiredproperlytoevaluate theeffectivenessofmitigationmeasuresThis couldthensupportandencourageclearerdecision-makingandprioriti-zationofactionsOurframeworkdemonstratesthattheprincipleof implementing thegoalofnonet loss throughamitigationhi-erarchy isasapplicable tomarinemegafaunaby-catchas to ter-restrial systems where it is already widely used in challengingdata-poorcircumstances

There isuntappedpotential forcost-effectiveby-catchmitiga-tionwhichcouldberealizedwiththeadoptionofthisframeworkandwithconsiderationofnewapproachestoincentivizingby-catchmitigationwithinthestepsofthehierarchyApplyingittoafewcase-studiesinpracticewilldemonstrateempiricallywhereandhowthepotentialforimprovedeffectivenesscouldbestberealizedExistinglegalframeworksoftenprecludeapproacheswhichimplicitlyorex-plicitly permit by-catch including the use of economic incentives

ornewapproachessuchasoffsetsHoweverinthiscontextofdy-namicuncertaintythedividendsofthinkingmorecreativelyaboutby-catchmitigationcouldbehigh

ACKNOWLEDG EMENTS

EJMG acknowledges the Pew Charitable Foundation for its sup-port of thiswork This article originated at a 2013workshop co-organized by NOAA-Fisheries and IUCN-CEEM-FEG entitledldquoMultidisciplinaryWorkshoptoAddressEcosystem-LevelImpactsofFisheriesBycatchonMarineMegafaunaBiodiversityConservationthrough Mitigation Policy Economic Instruments and TechnicalChangerdquo We thank the reviewers for their insightful commentswhichmuchimprovedthemanuscript

ORCID

E J Milner-Gulland httporcidorg0000-0003-0324-2710

R E FE R E N C E S

Alfaro-Shigueto J Dutton P H amp Mangel J (2007) Interactionsbetween leatherback turtles and Peruvian artisanal fisher-ies Chelonian Conservation and Biology 6 129ndash134 httpsdoiorg1027441071-8443(2007)6[129ibltap]20co2

Alfaro-Shigueto JMangel JCBernedoFDuttonPHSeminoffJAampGodleyB J (2011) Small-scale fisheriesofPeruAmajorsinkformarineturtles inthePacificJournal of Applied Ecology481432ndash1440httpsdoiorg101111j1365-2664201102040x

Alfaro-ShiguetoJMangelJCPajueloMDuttonPHSeminoffJ A amp Godley B J (2010) Where small can have a large im-pact Structure and characterization of small-scale fisheries inPeru Fisheries Research 106 8ndash17 httpsdoiorg101016jfishres201006004

Andraka SMugM HallM PonsM Pacheco L ParralesM hellipOrtega D (2013) Circle hooks Developing better fishing prac-ticesintheartisanallonglinefisheriesoftheEasternPacificOceanBiological Conservation 160 214ndash224 httpsdoiorg101016jbiocon201301019

ApostolopoulouEampAdamsWM(2017)BiodiversityoffsettingandconservationReframingnaturetosaveitOryx5123ndash31httpsdoiorg101017S0030605315000782

BaacuteezJCRealRGarciacutea-SotoCJoseacuteMMaciacuteasDampCamintildeasJA(2007)Loggerheadturtleby-catchdependsondistancetothecoastindependentoffishingeffortImplicationsforconservationandfish-eries management Marine Ecology Progress Series 338 249ndash256httpsdoiorg101017S0030605315000782

BBOP (2012) Standard on biodiversity offsets Business and biodiversity offsets programmeWashingtonDCForestTrends

Bishop J (2006) Standardizing fishery-dependent catch and ef-fort data in complex fisheries with technology change Reviews in Fish Biology and Fisheries 16 21ndash38 httpsdoiorg101007s11160-006-0004-9

BoyceJ(1996)AneconomicanalysisofthefisheriesbycatchproblemJournal of Environmental Economics and Management31 314ndash336httpsdoiorg101006jeem19960047

BugoniLManciniPLMonteiroDSNascimentoLampNevesTS(2008)SeabirdbycatchintheBrazilianpelagiclonglinefisheryandareviewofcaptureratesinthesouthwesternAtlanticOceanEndangered Species Research5137ndash147httpsdoiorg103354esr00115

emspensp emsp | emsp13MILNER- GULLAND Et AL

BullJWampBrownlieS(2017)Thetransitionfromnonetlosstoanetgainof biodiversity is far from trivialOryx51 53ndash59 httpsdoiorg101017S0030605315000861

BullJWBryantCBakerJampMilner-GullandEJ(2015December28)Developing measuring and communicating the outcomes of cor-porate biodiversity strategies [pdfdocument]RetrievedfromhttpwwwwildbusinessorgBull_etal_2015_WBLpdf

BullJWGordonAWatsonJEampMaronM(2016)Seekingcon-vergenceonthekeyconceptsinlsquononetlossrsquopolicyJournal of Applied Ecology531686ndash1693httpsdoiorg1011111365-266412726

BullJWHardyMJMoilanenAampGordonA (2015)Categoriesof flexibility in biodiversity offsetting and their implications forconservation Biological Conservation 192 522ndash532 httpsdoiorg101016jbiocon201508003

Bull JW Lloyd S P amp StrangeN (2017) Implementation gap be-tween the theory and practice of biodiversity offset multipliersConservation Lettershttpsdoiorg101111conl12335

Bull JW SuttleKBGordonA SinghN JampMilner-Gulland EJ(2013)BiodiversityoffsetsintheoryandpracticeOryx47369ndash380httpsdoiorg101017S003060531200172X

CampbellLMampCornwellML(2008)Humandimensionsofbycatchreduction technology Current assumptions and directions for fu-tureresearchEndangered Species Research5325ndash334httpsdoiorg103354esr00172

Caswell H Brault S Read A J amp Smith T D (1998) Harborporpoise and fisheries An uncertainty analysis of inciden-tal mortality Ecological Applications 8 1226ndash1238 httpsdoiorg1018901051-0761(1998)008[1226hpafau]20co2

ClementsTJohnANielsenKAnDTanSampMilner-GullandEJ (2010)Payments forbiodiversityconservation in thecontextofweak institutions Comparison of three programs from CambodiaEcological Economics 69 1283ndash1291 httpsdoiorg101016jecolecon200911010

CoxTLewisonRŽydelisRCrowderLSafinaCampReadA(2007)ComparingeffectivenessofexperimentalandimplementedbycatchreductionmeasuresTheidealandtherealConservation Biology211155ndash1164httpsdoiorg101111j1523-1739200700772x

CrollDADewarHDulvyNKFernandoDFrancisMPGalvaacuten-Magantildea F hellip Newton K M (2016) Vulnerabilities and fisher-ies impactsTheuncertain futureofmanta anddevil raysAquatic Conservation Marine and Freshwater Ecosystems 26 562ndash575httpsdoiorg101002aqc2591

Damalas D amp Vassilopoulou V (2013) Slack regulation com-pliance in the Mediterranean fisheries A paradigm from theGreek Aegean Sea demersal trawl fishery modelling discardogives Fisheries Management and Ecology 20 21ndash33 httpsdoiorg101111j1365-2400201200860x

DuttonDLDuttonPHChaloupkaMampBoulonRH(2005)IncreaseofaCaribbeanleatherbackturtleDermochelys coriaceanestingpop-ulation linked to long-termnestprotectionBiological Conservation126186ndash194httpsdoiorg101016jbiocon200505013

DuttonPJosephJSquiresDampWilliamsM(2011)Bellagioblue-print foractiononseaturtlesChapter2 InPDuttonDSquiresampM Ahmed (Eds) Conservation of pacific sea turtles (pp 15ndash36)HonoluluHIUniversityofHawaiiPress

DuttonPampSquiresD (2008)AholisticstrategyforPacificseatur-tlerecoveryOcean Development and International Law39200ndash222httpsdoiorg10108000908320802013685

FAO (2011 January 5) International guidelines on bycatch manage-ment and reduction of discards Rome Italy Food and AgricultureOrganisation [pdf document] Retrieved from httpwwwfaoorgdocrephelliptba0022t00pdf

Finkelstein M Bakker V Doak D F Sullivan B Lewison RSatterthwaite W H hellip Henry R W (2008) Evaluating the po-tential effectiveness of compensatory mitigation strategies for

marinebycatchPLoS ONE3 e2480httpsdoiorg101371jour-nalpone0002480

FowlerSJ(2016January5)Draft best practice mitigation guidelines for sharks and rays taken in purse- seine and long-line fisheries Convention on Migratory Species[pdfdocument]RetrievedfromhttpwwwcmsintsitesdefaultfilesdocumentCMS_Sharks_CWG1_Doc_3_2pdf

FrancisMP(2014)Survival and depth distribution of spinetail devilrays (Mobula japanica) released from purse-seine catches NIWA ClientReportNoWLG2014-2WellingtonNewZealandDepartmentofConservation

Fulton E A Smith A D Smith D C amp van Putten I E (2011)Human behaviour The key source of uncertainty in fish-eries management Fish and Fisheries 12 2ndash17 httpsdoiorg101111j1467-2979201000371x

GardnerTAHaseABrownlieSEkstromJMPilgrimJDSavyCEhellipTenKateK(2013)BiodiversityoffsetsandthechallengeofachievingnonetlossConservation Biology271254ndash1264httpsdoiorg101111cobi12118

GjertsenHHallMampSquiresD(2010)IncentivestoaddressbycatchInRAllenJJosephampDSquires(Eds)Conservation and manage-ment of transnational tuna fisheries (pp225ndash250)Ames IAWiley-Blackwellhttpsdoiorg1010029780813820262ch14

Gjertsen H Squires D Dutton P amp Eguchi T (2014) Cost-effectivenessofalternativeconservationstrategieswithapplicationtothePacificLeatherbackTurtleConservation Biology28140ndash149httpsdoiorg101111cobi12239

GodinACCarlson JKampBurgenerV (2012)Theeffectofcirclehooks on shark catchability and at-vessel mortality rates in long-lines fisheriesBulletin of Marine Science88 469ndash483 httpsdoiorg105343bms20111054

GrimmDBarkhornIFestaDBonzonKBoomhowerJHovlandV amp Blau J (2012) Assessing catch sharesrsquo effects evidencefrom Federal United States and associated British Columbianfisheries Marine Policy 36 644ndash657 httpsdoiorg101016jmarpol201110014

HallMA(1996)OnbycatchesReviews in Fish Biology and Fisheries6319ndash352httpsdoiorg101007BF00122585

HallMAAlversonDLampMetuzalsKI(2000)By-catchProblemsand solutions Marine Pollution Bulletin 41 204ndash219 httpsdoiorg101016S0025-326X(00)00111-9

HallMANakanoHClarke S Thomas SMolloy J PeckhamSHhellipHallSJ (2007)Workingwithfisherstoreduceby-catchesIn S J Kenelly (Ed)By-catch reduction in the worldrsquos fisheries (pp235ndash288) Dordrecht The Netherlands Springer httpsdoiorg101007978-1-4020-6078-6_8

HallM amp RomanM (2013)Bycatch and non-tuna catch in the tropi-cal tuna purse seine fisheries of the worldFisheriesandAquacultureTechnicalPaper568RomeItalyFAO

HallMASwimmerYampPargaM(2012)NoldquosilverbulletsrdquobutplentyofoptionsWorkingwiththeeasternpacificartisanalfisherstore-duceseaturtlemortalityinfisheriesInJASeminoffampBWallace(Eds)Sea turtles of the eastern pacific Advances in research and con-servation(pp136ndash153)TucsonAZUniversityofArizonaPress

HamnerRMWadePOremusMStanleyMBrownPConstantineR amp Baker C S (2014) Critically low abundance and limits tohuman-relatedmortalityfortheMauirsquosdolphinEndangered Species Research2687ndash92httpsdoiorg103354esr00621

HatchSA(2003)Statisticalpowerfordetectingtrendswithapplica-tions to seabird monitoringBiological Conservation 111 317ndash329httpsdoiorg101016S0006-3207(02)00301-4

HeppellSSCrowderLBampCrouseDT(1996)Modelstoevaluateheadstartingasamanagementtoolforlong-livedturtlesEcological Applications6556ndash565httpsdoiorg1023072269391

HoughPampRobertsonM(2009)MitigationunderSection404oftheCleanWater ActWhere it comes from what it meansWetlands

14emsp |emsp emspensp MILNER- GULLAND Et AL

Ecology and Management 17 15ndash33 httpsdoiorg101007s11273-008-9093-7

IATTC(2015)Resolution on the conservation of mobulid rays caught in as-sociation with fisheries in the IATTC convention area Inter-AmericanTropical TunaCommission89thAnnualMeetingResolutionC-15-04LaJollaCAInter-AmericanTropicalTunaCommission

IFC(2012)Performance standard 6 Biodiversity conservation and sustain-able management of natural resources January 1 2012WashingtonDCInternationalFinanceCorporation

Innes J Pascoe S Wilcox C Jennings S amp Paredes S (2015)MitigatingundesirableimpactsinthemarineenvironmentAreviewofmarket-basedmanagementmeasuresFrontiers in Marine Science276httpsdoiorg103389fmars201500076

JanniseCSquiresDSeminoffJampDuttonP (2010)Conservationinvestments andmitigationTheCaliforniadrift gillnet fishery andpacificseaturtles InRQGraftonRHilbornDSquiresMTaitampMJWilliams(Eds)Handbook of marine fisheries conservation and management(pp231ndash240)OxfordUKOxfordUniversityPress

Jones E amp FrancisM (2012)Protected rays ndash Occurrence and devel-opment of mitigation methods in the New Zealand tuna purse seine fishery Auckland New Zealand National Institute of Water andAtmosphericResearch

KormosRKormosCFHumleTLanjouwARainerHVicturineR hellipWilliamson E A (2014) Great apes and biodiversity offsetprojectsinAfricaThecasefornationaloffsetstrategiesPLoS ONE9(11)e111671httpsdoiorg101371journalpone0111671

KotchenMJ (2013)Voluntaryand information-basedapproachestoenvironmentalmanagementApubliceconomicsperspectiveReview of Environmental Economics and Policy 7(2) 276ndash295 httpsdoiorg101093reepret012

Kyriazi Z LejanoRMaes FampDegraer S (2015)Bargaining a netgaincompensationagreementbetweenamarinerenewableenergydeveloperandamarineprotectedareamanagerMarine Policy6040ndash48httpsdoiorg101016jmarpol201506005

LentRampSquiresD(2017)ReducingmarinemammalbycatchinglobalfisheriesAneconomicsapproachDeep Sea Research Part II Topical Studies in Oceanography 140 268ndash277 httpsdoiorg101016jdsr2201703005

Lewison R L Crowder L B Read A J amp Freeman S A (2004)Understanding impactsof fisheriesbycatchonmarinemegafaunaTrends in Ecology amp Evolution19598ndash604httpsdoiorg101016jtree200409004

MannC (2015)StrategiesforsustainablepolicydesignConstructiveassessmentofbiodiversityoffsetsandbankingEcosystem Services16266ndash274httpsdoiorg101016jecoser201507001

Marine Stewardship Council (2014 June 21) MSC fisheries certifica-tion requirements v20 [pdf doc] httpswwwmscorgdocumentsscheme-documentsfisheries-certification-scheme-documentsfisheries-certification-requirements-version-20

MaronM IvesCDKujalaHBullJWMaseykFJBekessyShellip Possingham H P (2016) Taming a wicked problem Resolvingcontroversies inbiodiversityoffsettingBioScience66(6)489ndash498httpsdoiorg101093bioscibiw038

MaxwellSLMilner-GullandEJJonesJPKnightATBunnefeldNNunoAhellipRhodesJR(2015)BeingsmartaboutSMARTenvi-ronmentaltargetsScience3471075ndash1076httpsdoiorg101126scienceaaa1451

Moilanen A Van Teeffelen A J Ben-Haim Y amp Ferrier S (2009)Howmuch compensation is enoughA framework for incorporat-inguncertaintyandtimediscountingwhencalculatingoffsetratiosfor impactedhabitatRestoration Ecology17 470ndash478 httpsdoiorg101111j1526-100X200800382x

MorarNToadvineTampBohannanBJ(2015)Biodiversityattwenty-fiveyearsRevolutionorredherringEthics Policy amp Environment1816ndash29httpsdoiorg1010802155008520151018380

OrphanidesCDampPalkaDL(2013)Analysisofharborporpoisegill-netbycatchcomplianceandenforcement trends in theUSnorth-western Atlantic January 1999 to May 2010 Endangered Species Research20251ndash269httpsdoiorg103354esr00499

Pascoe S Innes J Holland D Finas M Theacutebaud O TownsendR hellip Hutton T (2010) Use of incentive-based managementsystems to limit bycatch and discarding International Review of Environmental and Resource Economics 4 123ndash161 httpsdoiorg10156110100000032

PhalanBHayesG Brooks SMarshDHoward PCostelloeBhellip Whitaker S (2017) Avoiding impacts on biodiversity throughstrengthening the first stage of the mitigation hierarchy Oryxhttpsdoiorg101017S0030605316001034

Queacutetier F Regnery B amp Levrel H (2014) No net loss of biodiver-sity or paper offsets A critical review of the French no net losspolicy Environmental Science amp Policy 38 120ndash131 httpsdoiorg101016jenvsci201311009

RadzioTASmolinskyJAampRoosenburgWM(2013)Lowuseofre-quiredterrapinbycatchreductiondevicesinarecreationalcrabpotfisheryHerpetological Conservation and Biology8222ndash227

RaineyHJPollardEHBDutsonGEkstromJMLivingstoneSRTempleHJampPilgrimJD(2015)AreviewofcorporategoalsofnonetlossandnetpositiveimpactonbiodiversityOryx49232ndash238httpsdoiorg101017S0030605313001476

Rausser G C Hamilton S F Kovach M amp Stifter R (2009)UnintendedconsequencesThe spillovereffectsof commonprop-ertyregulationsMarine Policy3324ndash39httpsdoiorg101016jmarpol200803020

Rice J (2014) Evolution of international commitments for fisheriessustainability ICES Journal of Marine Science Journal du Conseil71157ndash165httpsdoiorg101093icesjmsfst078

RichardYampAbrahamER(2013)ApplicationofPotentialBiologicalRemoval methods to seabird populations New Zealand AquaticEnvironmentandBiodiversityReport108

RodeJGoacutemez-BaggethunEampKrauseT(2015)Motivationcrowd-ingbyeconomic incentives inconservationpolicyAreviewoftheempiricalevidenceEcological Economics117270ndash282httpsdoiorg101016jecolecon201411019

RogersAA(2013)SocialwelfareandmarinereservesIswillingnesstopayforconservationdependentonmanagementprocessAdiscretechoiceexperimentoftheNingalooMarineParkinAustraliaCanadian Journal of Agricultural EconomicsRevue Canadienne Drsquoagroeconomie61217ndash238httpsdoiorg101111cjag12008

Rosenberg A A amp McLeod K L (2005) Implementing ecosystem-basedapproachestomanagementfortheconservationofecosystemservicesMarine Ecology Progress Series300 270ndash274 httpsdoiorg103354meps300270

Segerson K (2010) Can voluntary programs reduce sea turtle by-catch Insights from the literature in environmental economics InRQGraftonRHilbornDSquiresMTaitampMJWilliams(Eds)Handbook of marine fisheries conservation and management(pp618ndash629)OxfordUKOxfordUniversityPress

Serafy JECookeS JDiazGAGraves JEHallMShivjiMampSwimmerY(2012)CirclehooksincommercialrecreationalandartisanalfisheriesResearchstatusandneedsforimprovedconser-vation and management Bulletin of Marine Science 88 371ndash391httpsdoiorg105343bms20121038

ShiodeDHu F ShigaM Yokota K amp Tokai T (2005)Midwaterfloatsystemforstandardizinghookdepthsontunalonglinestore-duce sea turtleby-catchFisheries Science71 1182ndash1184httpsdoiorg101111j1444-2906200501080x

Sims M Cox T amp Lewison R (2008) Modeling spatial patternsin fisheries bycatch Improving bycatch maps to aid fisheriesmanagement Ecological Applications 18 649ndash661 httpsdoiorg10189007-06851

emspensp emsp | emsp15MILNER- GULLAND Et AL

Squires D amp Garcia SM (2014) Ecosystem-level impacts of fisheries bycatch on marine megafauna Biodiversity conservation through miti-gation policy economic instruments and technical changeReportofthe IUCN-CEM-FEGScientificworkshopGland Switzerland 7ndash10October2013GlandSwitzerlandIUCN

SquiresDampGarciaSM(inpress)Fisheries bycatch in marine ecosys-tems Policy economic instruments and technical change ChichesterUKJWileyampSons

SwimmerYArauzRMcCrackenMMcNaughtonLBallesteroJMusylMhellipBrillR(2006)DivingbehavioranddelayedmortalityofoliveridleyseaturtlesLepidochelys olivaceaaftertheirreleasefromlongline fishing gearMarine Ecology Progress Series323 253ndash261httpsdoiorg103354meps323253

TolottiMTFilmalterJDBachPTravassosPSeretBampDagornL(2015)BanningisnotenoughThecomplexitiesofoceanicsharkmanagementbytunaregional fisheriesmanagementorganizationsGlobal Ecology and Conservation 4 1ndash7 httpsdoiorg101016jgecco201505003

Tuck G N Polacheck T amp Bulman C M (2003) Spatio-temporaltrendsoflonglinefishingeffortintheSouthernOceanandimplica-tionsforseabirdbycatchBiological Conservation1141ndash27httpsdoiorg101016S0006-3207(02)00378-6

UNEP-WCMC(2016)Marine no net loss A feasibility assessment of imple-menting no net loss of biodiversity in the seaCambridgeUKUnitedNationsEnvironmentProgramme

Vaissiegravere A-C Levrel H Pioch S amp Carlier A (2014) Biodiversityoffsets for offshore wind farm projects The current situation inEurope Marine Policy 48 172ndash183 httpsdoiorg101016jmarpol201403023

Wallace B P Heppell S S Lewison R L Kelez S amp CrowderL B (2008) Impacts of fisheries bycatch on loggerhead tur-tles worldwide inferred from reproductive value analy-ses Journal of Applied Ecology 45 1076ndash1085 httpsdoiorg101111j1365-2664200801507x

Wanless R M Ryan P G Altwegg R Angel A Cooper JCuthbert R amp Hilton G M (2009) From both sides Dire de-mographic consequences of carnivorous mice and longlining for

the critically endangered Tristan albatrosses on Gough IslandBiological Conservation 142 1710ndash1718 httpsdoiorg101016jbiocon200903008

WardP LawrenceEDarbyshireRampHindmarshS (2008) Large-scale experiment shows that nylon leaders reduce shark bycatchandbenefitpelagiclonglinefishersFisheries Research90100ndash108httpsdoiorg101016jfishres200709034

WardTampPhillipsB(2010)SeafoodecolabelingInRQGraftonRHilbornDSquiresMTaitampMJWilliams(Eds)Handbook of ma-rine fisheries conservation and management (pp 608ndash617) OxfordUKOxfordUniversityPress

WilcoxCampDonlanCJ (2007)Compensatorymitigationasasolu-tion to fisheries bycatch-biodiversity conservation conflictsFrontiers in Ecology and the Environment 5 325ndash331 httpsdoiorg1018901540-9295(2007)5[325cmaast]20co2

WilcoxCampDonlanCJ (2009)NeedforaclearandfairevaluationofbiodiversityoffsetsforfisheriesbycatchConservation Biology23770ndash772httpsdoiorg101111j1523-1739200901173x

Wolf SHartlBCarrollCNeelMCampGreenwaldDN (2015)Beyond PVAWhy recovery under the Endangered Species Act ismorethanpopulationviabilityBioScience65200ndash207httpsdoiorg101093bioscibiu218

ZedlerJBampCallawayJC (1999)TrackingwetlandrestorationDomitigation sites follow desired trajectories Restoration Ecology 769ndash73httpsdoiorg101046j1526-100X199907108x

Žydelis R Wallace B P Gilman E L amp Werner T B (2009)Conservation of marine megafauna through minimization of fish-eries bycatch Conservation Biology 23 608ndash616 httpsdoiorg101111j1523-1739200901172x

How to cite this articleMilner-GullandEJGarciaSArlidgeW etalTranslatingtheterrestrialmitigationhierarchytomarinemegafaunaby-catchFish Fish 2018001ndash15 httpsdoiorg101111faf12273

Page 7: Translating the terrestrial mitigation hierarchy to marine ......of marine megafauna by-catch in fisheries, going from defining an overarching goal with an associated quantitative

emspensp emsp | emsp7MILNER- GULLAND Et AL

themitigationhierarchy In theabsenceofhighqualitypopulationdatawithwhichtoparameterizeamodelaPBR-basedapproachisbeingusedtosetatargetby-catchlevel intermsofnumberof in-dividualsofeachoftheturtlespeciescaughtinthefisheryExpertopinionfromfishersandProdelphinusstaffsupplementedbydatafromalong-runningby-catchobserverprogrammeoperatingoutoftheport(Alfaro-Shiguetoetal2011)givesthepotentialreductioninturtleby-catchnumbersasaresultofagivenmitigationapproachInterviews and focus groups with fishers provide understandingof their preferences for different by-catchmitigation approachesbarriers and constraints to implementation and potential partici-pationindifferentincentiveschemesthiscanbesupplementedbyDiscreteChoiceExperimentsprovidingempiricalestimatesforpref-erencesforcombinationsofby-catchreductionmeasures(cfRogers2013)Thisfieldresearchproducesashort-listoffeasiblemitigationmeasuresateachstageinthemitigationhierarchyforcostingandtesting(egspecificareasortimesforfisheryclosureunderavoid-ancecombinationsofhooktypesandnetmodificationundermini-mizationtraininginturtlehandlingandreleaseforremediationandimprovingby-catchperformanceofothergeartypesintheareaforoffsetting)Thisenablestheanalysisoftheeffectivenessandcostof various combinations of by-catch reduction strategies framedwithinthefourstepsofthemitigationhierarchy(avoidminimizere-mediateoffset)withacleartargetby-catchreductiongoalinmind

4emsp |emspCOMPARING KE Y DEBATES BET WEEN TERRESTRIAL NNL AND BY- C ATCH MITIGATION

41emsp|emspThe hierarchical nature of mitigation

Terrestrial situationsareusuallyviewedas requiringastricthierar-chywithavoidanceminimizationandremediationtakingprecedenceoveroffsetsPartofthereasonforthishierarchymaybesocietalval-uesandexpectationsbut also it is a reflectionof reversibility anduncertaintyTheterrestrialmitigationhierarchywassetuptoaddresshabitatdestructioncausedbydevelopmentwhich iseffectively ir-reversiblehenceavoidanceisstrictlypreferredfromaconservationperspective Inpractice avoidancehasbeenaneglected step andmuchofthedisquietaboutbiodiversityoffsettinghasbeenbecauseofthetendencytopaylipservicetoavoidanceandfocusinsteadonoffsetswhich thenmay be implemented on paper only (HoughampRobertson2009Phalanetal2017)EvenwithperfectenforcementandcompliancewithmeasuresfurtherdownthemitigationhierarchythestrictavoidanceofhabitatlossismorecertaintolimitimpactthanreducinglossesinthecourseofapotentiallydamagingactionwhichismorecertainthanrestoringdamageafterthefactorcompensatingforitwithactionselsewhereOfteninterrestrialsystemsmultipliersareusedattheoffsetstagetoreflectthisuncertaintyrequiringthatanadditionalamountofequivalentlandisprotectedinanoffsetoverandabovetheamountthatislostduringthedevelopment(withtheratiooflandoffsettolanddestroyedinthe10sto100sdependingonthecircumstancesMoilanenVanTeeffelenBen-HaimampFerrierFr

amew

ork

step

Cas

e- st

udy

Alb

atro

sses

lon

glin

esTu

rtle

slo

nglin

esRa

ysp

urse

sei

nes

Oce

anic

whi

tetip

slo

nglin

es

Major

uncertainties

Lackofspecies-levelidentificationof

by-catchlackofunderstandingof

compliance

Lackofecologicalknowledgeofturtle

populationtrendsampdistribution

Potentialforsignificantadditional

by-catchfromcoastalgillnetfishery

Impactofcatchonmobulid

survivalPredictorsof

mobuliddistributions

Lackofobserversorreportingsoverylimited

understandingofby-catchlevelsspatio-

temporalencounterhotspotspost-release

survivalcompliance

Keyobstacle

Compliancewithexistingrulesmustbe

improved

Fundingforalternativestofishingata

largeenoughscaleLongtimelagand

uncertaintyinoffseteffectiveness

Limitedknowledgeofmobulid

distributionsmakes

avoidancedifficult

Lackofmonitoringlimitsoptions

Overallassessment

Existingmeasuresforimprovingimplementa-

tionofminimizationstepalreadyexistbut

needincentivizingoffsettingcouldprovide

short-termgainstocomplementthese

Targetedfundingcouldfacilitateimprove-

mentsthroughoutthehierarchyBest

approachmaydifferbyspecies(particu-

larlyleatherbacksvsothers)

Focusonremediationstepis

currentlythemainoption

avai

labl

e

Somepotentialforminimizationthrough

deepsettingbutchallengingtochange

behaviourinthisfisheryelectronic

monitoringsystemswouldhelp

Keyreferences

BugoniManciniMonteiroNascimentoamp

Neves(2008)Wanlessetal(2009)

Alfaro-ShiguetoDuttonampMangel(2007)

Halletal(2012)Andrakaetal(2013)

JonesampFrancis(2012)Hallamp

Roman(2013)Crolletal

(2016)Fowler(2016)

Tolottietal(2015)

Ticksindicatethepotentialforactionatdifferentstepsofthehierarchybasedonfeasibilitycurrentknowledgeandimpactonmortality(

=highpotential

=somepotential

=limitedpotential

ndash=nopotential)TextinbracketsgivessuggestedmeasuresateachlevelofthehierarchytheseareillustrativeratherthandefinitiveTheinformationforthecase-studiesisbasedontheexpertknowledge

oftheauthorsthroughtheirinvolvementinmanagementoftheby-catchissueinthesefisheriesRFMOregionalfisheriesmanagementorganizationPBRpotentialbiologicalremoval

TABLE 3emsp(Continued)

8emsp |emsp emspensp MILNER- GULLAND Et AL

2009)Bycontrastinfisheriessettingstherehavebeensuggestionsthatdependingonthelegalenvironmentitmaybemoreappropriateforoffsetstobeusedaspartofaleast-costconservationapproachalongsidemoretraditionalmitigationmethodsratherthanasthelaststep inamitigationhierarchy (DuttonJosephSquiresampWilliams2011DuttonampSquires2008WilcoxampDonlan2007)

42emsp|emspOut- of- kind offsets

Out-of-kind offsets are those which do not act to increase theimpact-affectedbiodiversityIntermsofourconceptualframeworktheyareoffsetswhichdonotacttoincreasethepopulationgrowthrateoftheby-catch-affectedfocalpopulation(Equation1)Forex-ampleonesuggestedbenefitof raising funds foroffsetting fromaby-catchtaxonfishersisthattheproceedsfromsuchataxcanfinanceoffsetselsewherewithintherangeoftheby-catch-affectedpopulation (Dutton amp Squires 2008) Although not a true offsetunderamitigationhierarchyfundsfromtheCaliforniadriftgillnetindustry in 2002 financed sea turtle nesting site conservation inBajaCaliforniaforcompensatorymitigationofseaturtleby-catch(Jannise Squires Seminoff amp Dutton 2010) In terrestrial (andmarine)systems itcanbemorechallengingtodefinethe impact-affected biodiversity because impact is rarely as clearly linkedtoagivenspeciesandstockas it is forby-catchBecauseofthisthelocationandbiodiversitytargetofconservationactionsfallingundertheldquooffsetrdquoheadinghassometimesbeenlooselyrelatedtotheactual impactBest-practicestandardsstatethatoffsetsmustbeimplementedasclosetothedamagingactivitiesaspossibleandfocusonbiodiversityassimilaraspossibletothatwhichhasbeenimpacted (BBOP 2012) However there have also been calls forldquoout-of-kindrdquooffsetsthatgivemoreconservationbang-for-buckbyfocussingonthreatenedspeciesorrarehabitatsorareasinneedofconservation rather than the impactedareasor specieswhichmay be considered less ldquovaluablerdquo for conservation (Bull Hardyetal2015)Thishasledtosubstantialdebateastotheappropri-atelimitsonthegeographicscaleandbiodiversityfocusforoffset-ting(egApostolopoulouampAdams2017)Italsodrawsattentiontothesubjectiveanduser-definednatureof theword ldquobiodiversityrdquo(Morar ToadvineampBohannan 2015) As it is impossible fully tooperationalizetheconceptimplementersofthemitigationhierar-chyhavelatitudetointerpretbiodiversityaccordingtoforexampleeaseofmeasurement perceived societal valueormitigation cost(Maron etal 2016) In our casewe take a narrow focus on theby-caughtspecies itself this is in linewithmuchof the literatureon by-catch but notwith the broader discourses on ecosystem-basedapproachestomarinemanagementandecosystemservices(RosenbergampMcLeod2005)Thesediscoursessuggest theneedforamorefunctionalecosystem-basedapproachtononetlossofbiodiversitythishasyettotranspireeitherinthemarineorintheterrestrialliteraturepossiblybecausesubstantialchallengesinde-finingimpact-affectedbiodiversitytheninevitablyensue

Asmarinemegafauna stocks are often transboundary andmi-gratorydefiningtheappropriatespatialunit foroffsettingmaybe

achallengebecause themosteffective location foranoffsetmayormaynotbewithintheareaofinfluenceofagivenfisheryClearlyandpreciselydefining the spatial unitwithinwhich themitigationhierarchywill be implemented during theprocess of defining theoverallgoal(suchasNNL)isvitalThisunitshouldreflectthescaleoverwhichanactionwillaffectλToffsetswhicharewithinthedis-tributionofthefocalstockoftheby-caughtspecies(asdefinedforEquation1)arenotout-of-kindHoweverchallengesemergewhenthe appropriate spatial unit for offsetting activities is different totheappropriatespatialunitforotherelementsofthemitigationhi-erarchywhicharelikelytobedefinedinsteadbyjurisdictionalareaor target fish stock distribution Inmany fisheries the species af-fectedbyby-catchmaynotbewellenoughknownandoffsetsmayaccordinglyneedtobebroadlytargetedtobenefitanypotentiallyaffectedspeciesTrueout-of-kindoffsetswouldincludefundingtheconservationofunaffectedspeciesorstocksofhabitatsnotusedbythefocalstockorcontributionstoaconservationfundwithoutaclearcommitmentthatthefundsaretobespentonincreasingλT for thefocalby-caughtstockTheseareunlikelytoformpartofbest-practiceguidanceforby-catchoffsets

43emsp|emspResearch as an offset

Arelatedareaofactivecontroversyformarineby-catchiswhetherresearchor informationgatheringshouldbeseenasavalidoffsetmechanism The rationale is that this research could be used toreduceuncertaintypromote innovationand thereby improveout-comes for by-caught species albeit indirectly An offset could beusedto incentivizebetterdatacollectionfor instanceusingaby-catchlevytopayfortaggingortoputby-catchobserversorelec-tronicmonitoringsystemsonboatsThismightbeapreludetolatermitigation or avoidance activities once more is known about thebiological settingWhether research activities could appropriatelybeconsideredaspartofanldquooffsetrdquoiscontroversialmdashinsomecasesan indirectbenefit to theby-caught stockmightbe clearly appar-ent(egtheoceanicwhitetip(Carcharinus longimanusCarcharinidae)case-studyinTable3)whileinothercasesusinginvestmentinre-searchasanoffsetcouldbeseenasacaseofmoralhazardpoten-tially compromising scientistsrsquo independence and having at best ahighlyindirectrelationshiptoNNLoftheby-caughtspeciesAnotherviewisthatreducinguncertaintyisacoreresponsibilityofoperatingafisherywhichthereforeshouldbebornebythemanagementau-thorityorfishingbusinessesInterrestrialsystemsthesedilemmasalsoexistbutthesentimentismuchmoreclearlyexpressedthatre-searchactivitiesarenotappropriateoffsets(BullGordonWatsonampMaron2016)

44emsp|emspIncentivizing implementation of mitigation measures

Thefactorsthatdrivedecision-makingaboutmegafaunaby-catchreduction (by skippers companies fishery managers policymak-ers and other stakeholders) include legal obligations tominimize

emspensp emsp | emsp9MILNER- GULLAND Et AL

by-catch at the national or international levels (eg FAO 2011Rice 2014) the availability and quality of technical fixes associ-atedcosts tofishers limitsonaccesstoseafoodmarketsaswellassocietalpressuresHowevermuchresearchonby-catchreduc-tion focuses on identifying and implementing technicalmeasuresto reduceBPUE rather thanon the social andeconomicbarriersto implementation (Campbell amp Cornwell 2008) Technologicalinnovation to improve BPUE needs to be appropriately incentiv-izedwitheffortsmadetoensurethatsuchmeasuresareascost-effective as possible for fishers (Gjertsen Hall amp Squires 2010Lent amp Squires 2017) However it often happens that even ap-parently suitable by-catchmeasures are notwidely implemented(eg Damalas amp Vassilopoulou 2013 Orphanides amp Palka 2013RadzioSmolinskyampRoosenburg2013)Inthesecasesthedegreeofnon-implementationandthereasonsbehinditneedstobeun-derstoodsoitcanbeaddressed(Coxetal2007)Thesetypesofconsiderationarealsonotwellresearchedintheterrestrialoffset-tingliteraturebecausecomplianceispoorlymonitored(BullSuttleGordonSinghampMilner-Gulland2013)andthereislittlesupportfor researchon thebarriers to implementationofamitigationhi-erarchyandhowtosupportdeveloperstoaddressthesebarriers(BullBryantBakerampMilner-Gulland2015)Thesocialimpactsofimplementingabiodiversitymitigationhierarchyonresourceusersarementioned inguidance (egBBOP2012)buthowtomeasureandaccountforthemisverypoorlyunderstoodThefewstudiesin-vestigatingdeliveryofpromisedoffsetmeasuresinterrestrialsys-temssuggestaverypoorrecord(QueacutetierRegneryampLevrel2014)Therefore the social side of implementing the mitigation hierar-chyand incentivizingcompliance isanarea thatneedsmore andmoreactiveresearchwithinboththeterrestrialandmarinerealms(FultonSmithSmithampvanPutten2011)Thisisparticularlytruewhentheburdenof implementingmitigationapproaches isbornebyrelativelysmall-scaleproducersratherthangovernmentsormul-tinationals(egthepelagiclonglinefisheriesinTable3)

45emsp|emspSocietal limits

Foraspeciesathighriskofextinctioncompleteavoidanceofby-catchmightbethemostdesirablepolicyfrombothamanagementagency and societal perspective In addition with emblematic orhighlythreatenedmarinemegafaunaitmaybeviewedbymembersof the public asmorallywrong to kill any individuals even ifmiti-gationisinplace(egMauirsquosdolphinHamneretal2014) leadingtopressureongovernmentstoreflectthisethicalconcerninregu-lationsThesedilemmasecho the issueof thresholds in terrestrialoffsetswhichrecognizesthattherearesomecriticalareasinwhichdevelopmentisnotsocietallyappropriateregardlessofthepoten-tialformitigationandotherareasinwhichthemitigationhierarchycan be appropriately applied (Bull etal 2013) Examples of loca-tionswhereathresholdapproach isseenasappropriate interres-trial systems include the habitat of highly endangered species orecosystemswhich are limited in extent and irreplaceable (such asoldgrowthforest) In terrestrialsystems therefore themitigation

hierarchyisseenasmostappropriateforapplicationinmorecom-monanddegradedhabitatssuchasfarmlandSimilarlyinfisheriestheremaybesomesituationsinwhichthestockssubjecttoby-catchare so precious or threatened that no level of threat from fishingcanbecontemplatedandotherswherefishingsubjecttoNNLandthemitigationhierarchyisasociallyacceptableapproachInsitua-tions inwhich trade-offs between conservation and developmentareseenasnecessaryoracceptablebywidersocietyasociallicencetooperatemaybegainedthroughadoptingoffsetsintheabsenceofregulationForexampleinsub-SaharanAfricaseverallargedevel-opmentprojectsareattemptingtooffsettheirimpactsongreatapesandtheirhabitats(Kormosetal2014)Aby-catchequivalentmightbe fishing companies voluntarily donating funds for turtle nestingbeachrestorationintheirareaofoperationinadditiontocomply-ingwithregulatoryby-catchmitigationmeasuresThesemeasuresmayimprovetheimageofthecompanywiththegeneralpublicbuttoavoidaccusationsofldquogreenwashingrdquotheireffectivenessneedstobeproperlyscrutinized(Bulletal2016)Transparentlyembeddingthesetypesofactionswithinamitigationhierarchysuchasweareproposing and critically evaluating their contribution to increasingthepopulationgrowthrate(asperEquation1)wouldbeonewaytopromptsuchscrutiny

46emsp|emspUncertainty

The nature of the uncertainties surrounding biology and enforce-ment in themarine setting raisesquestions about theorderingofsteps in themitigationhierarchy inaway that isdissimilar to ter-restrialsystemswherethehierarchyofuncertaintiesmaybecleareranduncertaintyisgenerallylowerForexampleitmaybethattheimpactonoverallpopulationgrowthrateofanoffsetmeasurelikeeradicating invasivespecies fromaseabirdnestinghabitat isbothless uncertain and more cost-effective than avoidance measuressuchasclosingareaswhichmayormaynotbefrequentedbyadultseabirds in a given time-periodGenerally though itmightbe as-sumedthatmeasureswhichtargetlifestagessubjecttohighlevelsofnaturalmortalityorwithinwhichindividualcontributiontoover-allpopulationgrowthrateislow(egheadstartingjuvenileturtles)maybelesseffectiveinachievingNNLthanmeasureswhichtargetreproductivelymatureadultfemales(suchaslivereleasesHeppellCrowderampCrouse1996)Howeverbeforeimplementinganoffsetthataimstoimprovethesurvivalofonelifestageinordertocom-pensatefortheby-catchmortalityofanotherarobustassessmentoftheconsequences(withassociateduncertainties)shouldbecar-ried out through detailed population modelling based on strongempiricalstudies(cfWallaceHeppellLewisonKelezampCrowder2008)Interrestrialsystemstherequirementsequentiallytoapplythemitigationhierarchyisbroadlyunchallengedbutactuallysimilararguments apply For example habitat restoration sits above off-settinginthehierarchyandyetitisalong-termuncertainprocesswhichmayinsomecircumstancesbemuchlesspreferabletoanoff-setusingawell-establishedapproachwhichishighlylikelytoleadtoconservationgains

10emsp |emsp emspensp MILNER- GULLAND Et AL

47emsp|emspTemporal considerations

Thetimingofoffsetsinrelationtootherelementsofthemitigationhierarchyhasbeenthesubjectofdebatewithintheterrestriallitera-tureThemainsuggestionforaddressingthetemporarylossofbio-diversitywhileoffsetscometofruitionhasbeenadoptingmitigationbankingwherebyoffsetsareimplementedinadvanceofpotentiallydamagingactivitiesprovidingbiodiversitycreditswhichcanbeusedtocompensateforlaterlossesThisbothremovesanelementofun-certaintyfromtheoffsetimplementationandreducesthetimelagbetweenlossandgain(Mann2015)Withrespecttomarinemega-faunaby-catchflexibilityintimingprovidesadditionalscopeforcostreduction and benefit enhancementwhichmay not be present intraditionalhabitat-basedterrestrialoffsetsForexampletemporarymeasuressuchasashort-termby-catchtaxtofundanoffsetmaybeusedifmitigationoravoidancemethodstaketimetocomeonlineorifatemporarynudgeisenoughtocausebehaviouralchangeThismightbethecaseifapolicywasneededtoinducefisherstotakeupnewgeartoavoidthecostofanoffsetorifconcernsaboutsafetyoryieldreductionsduringthetransitiontonewgearcouldbeallayedbyatemporarysubsidyforearlyadoptersorapaidparticipatorymoni-toringprogrammeto informwider implementation(egthemobu-lidandsharkcase-studiesinTable3)Justasforhabitatrestoration(ZedlerampCallaway 1999) by-catchoffset strategieswhich targetjuvenilestagesof long-livedspecies (eg turtleheadstartingor in-vasive removal fromseabirdnesting islands)may takemanyyearsfor their effects to become apparent in an increase in populationgrowthratesAdditionaluncertaintyisintroducedbythedifficultyinmonitoringpopulationsofmanyby-catch species (eg seabirdsHatch2003)leadingtouncertainestimatesoftheimpactofoffsetactivitiesonpopulationgrowth(seecase-studiesinTable3)Theseproblemsarenot insuperablehoweverpositivetrendshavebeenreportedinturtlepopulationsoverdecadesasaresultofnestpro-tection(egDuttonDuttonChaloupkaampBoulon2005)

5emsp |emspUSING INCENTIVES TO REDUCE BY- C ATCH

Manyoftheexamplesandprinciplesdiscussedaboveeitherimplic-itlyorexplicitlyrelatetotheeconomicsocialinstitutionalormoralincentivesoperatingondifferentactorsinsideandoutsidethefish-erywhichcanbepositiveornegativeWenowturntoadiscussionofhowincentivescanbeusedtoreduceby-catchwithinourframe-workIncentivescanbeputinplacetochangefisherbehaviourwithrespecttoanyoftheelementsoftheframework (avoidminimizeremediateandoffsetTable3)Althoughdiscussedintheliteraturemostof these incentive approaches are yet tobe implemented inthe realworldparticularly forby-catchThereforeuntil empiricalevidenceoftheireffectivenessisavailablethesesuggestionscomewithacaveat

Financial costsofby-catchmitigationactions canarise for in-stancefromlostcatchcapitalinvestmentsinnewgearormitigation

equipmentor the lossofaccesstoafisheryCostsmayalsoarisefromthedeploymentofby-catchobserversortrainingintheuseofnewgearThesecostscanbepaidbyfishingcompaniesorindivid-ualsorbygovernmentsNGOsorseafoodconsumersWhetherornotcompensationforcostsincurredbyfishersisseenasappropri-atedependsonwhetherby-catchreductionisseenasasocialgoodthatfishersareproviding(inwhichcasetheyshouldbecompensatedforit)orasputtingrighttheharmthattheyaredoingtobiodiver-sitywhilegeneratingtheirownprivategain(ineconomiclanguagewhetherby-catchisviewedasanunpricedexternalityinwhichcasetheyshouldpay)Italsodependsonwhethereconomichardshipwillensueacaseforcompensationofby-catchreductioncostsincurredbypeopledependenton fishing for their livelihoodsmaybemoresympatheticallyreceivedbyotheractorsthanacasemadebyalargemultinationalfishingcompany

Ifby-catchisseenasanunpricedexternalityitmightbesociallyoptimaltotaxfishersfortheirby-catchsothatthisexternalityisin-ternalizedThisplacesanexplicitpriceuponby-catch(Boyce1996Pascoeetal2010SquiresampGarcia2014)Theby-catchprice islikely to be incorporated into the price of the target species andtherebybecomespartofthetargetspeciescostThispricecouldbeset differently for different demographic classesof theby-caughtspecies depending on the impact the loss of an individualwouldhaveonthepopulationAllelsebeingequalputtingapriceonby-catchmeans that theseafoodproduct that is the targetcatchbe-comesmoreexpensiveandconsumershave topaymore for theirseafoodreducingdemandTheninprincipleeveryfirminthesup-plychaineveryvesselandeveryconsumerhaveanincentivetore-duceby-catchuntileacheconomicactorrsquosmarginalcostofby-catchreductionequals thecommonpriceofby-catch that theyall faceOffsetsareonewaytopriceandinternalizetheby-catchexternalitycostIfanoffsettingactioniscostlytoimplementandmustbepaidforwith each unit of by-catch it implicitly prices the residual by-catch In this circumstance the effect from a financial standpointisthesameasaby-catchtaxwiththe levelsetbasedonthecostoftheoffsetVariousinstitutionalstructurestosupportthischargeperunitofby-catcharepossiblewithdifferentimplicationsintermsofthedistributionofcostsandbenefitsForexampleaninsuranceschemecouldbepaidintobyfishersthatpaysoutintheeventofaby-catcheventtherebyspreadingthecostofunavoidablerareby-catcheventsOratradablepermitschemecouldoperatesuchthatfisherswhoexperienceaby-catcheventcanbuyapermitwiththecostvaryingdependingondemandforpermits (henceprovidingavessel-levelincentivetoinnovatetoreduceby-catch)

If there isdemandforconservation inan internationalmarketthen price premiums and market access (through eco-labellingsupply chain certification other food sustainability campaignsWardampPhillips2010)orboycottsactingasstrategicthreatsfromconsumers (Kotchen 2013 Segerson 2010) could act as positiveornegativeeconomic leversonthe fisheryprovidingan incentivefor fishers to reduce their by-catch voluntarily (as has been sug-gested for the Brazilianmahi-mahi fishery Table3) For exampletheMarine StewardshipCouncil now includesby-catchmitigation

emspensp emsp | emsp11MILNER- GULLAND Et AL

intheircertificationprocess(MSC2014)Demand-ledleversmaybemoreorlessapplicableatdifferentlevelsinthehierarchyforexam-pleavoidancemayberelativelyhardtoevidencewhileoffsettingmaybelesseasytoselltoaconsumerthanminimizationorreme-diationConcerns about the unintended consequences of positiveincentives (particularlyfordirectsubsidiesratherthanconditionalincentives)maydeterminewhethertheyareanappropriateinstru-mentinagivencaseForexampletheymaybeinappropriateifthereisariskthattheadditionalmoneyisreinvestedinincreasedfishingcapacityor iftheremaybeconsumptionproductionorconserva-tionleakages(transferoftheproblemsomewhereelse)whetheratthe vessel fishery or trans-national levelHigh transactions costsmayalsolimitthebenefitsofincentivesschemes

Otherchangeswhichmayneedtobeincentivizedforsuccessfulimplementationofby-catchreductionpoliciesmaybelessamenabletofinancialmeasuresatleastpartlybecauseitislessclearhowtoassign financial value to theactionsor to thebenefits and losseswhichtheyproduceForexampleperceivedreductionsinsafetyforfishingcrews(fromweightedlonglinesfor instance)arecoststhatmaybehardtovaluefinanciallyOtherprerequisitesfor long-termsustainable behaviour change such as changes in social norms sothatfishingcommunitiesseeby-catchreductionasappropriatebe-haviourortechnicalskillacquisitionsothattheycanusenewmeth-odsmaybeincentivizedbycarefullydesignedinterventionsworkingwithfishers(Halletal2007)Conservationpoliciesbasedoneco-nomic incentives (extrinsicmotivation) are not always superior tothosebasedupon intrinsicmotivation Infact incentive-basedby-catch reduction policy instruments could even be counterproduc-tivebyreducingtheeffectivenessofintrinsicmotivationdependingupon the situation (although the empirical evidence on this topicisweak RodeGoacutemez-BaggethunampKrause 2015) If the changerequiredforby-catchreductiontoworkmeetscultural resistancethenparticipatory researchmightbeespeciallyeffective inbreak-ingdownbarriersbetweenthosewhowantby-catchreductiontotakeplaceandthosewhoactuallyhavetoimplementit(thefishers)ForexampleinAustraliathegovernment-fundedbodyOceanwatchfacilitatesengagementbetweencommunities thefishing industryseafood suppliers and government to improve knowledge sharing(wwwoceanwatchorgau)Innovationiscrucialinfisheriesandfish-ersareaccustomedtoadoptingnewtechnologyorprocessespo-tentiallymakingan incentivizedparticipatory researchprogrammeespeciallyfruitful

Sometimes the most efficient way to solve problems is a so-cial instrumentoran institutionalchange inplaceoforaswellasan economic instrument For example supporting developmentof fisherorganizations rather than instituting a vessel-level taxorsubsidy might provide the impetus needed to change behaviourInstitutingcatchshares(individualtransferablequotas)mayprovideanenablingenvironmentforby-catchreductionforexamplebypro-motingmoreeffectivemonitoring(Grimmetal2012)Experiencein terrestrial system produces similar insights incentive-basedschemeswhichalsobuildcommunitycohesionandsupportthede-velopment or strengthening of localmanagement institutions are

more effective in the longer run than direct economic incentives(Clementsetal2010)

6emsp |emspCONCLUSIONS

The framework we present here is novel It draws upon and ex-tends the frameworks for conceptualizing by-catch developed byHall (1996) and Hall Alverson andMetuzals (2000) It amalgam-atesHallrsquos frameworkwith themitigationhierarchyasused in theEnvironmental Impact Assessment literature (BBOP 2012) Thesuggestions about goals metric andmitigation actions are drawnfromtheempiricalby-catchliteratureandtheissueswediscussin-tegratetheconcernsoftheextensiveterrestrialandnascentmarineoffsetting literature with the by-catch literature The frameworkmakesclear thatanearlycrucial step is toclarify thegoalofanyby-catch reduction policyOverarching goals like those issued bytheConventiononBiologicalDiversity(egAichiTarget11that10ofmarinehabitatshouldbeunderprotectionby2020)needtobetranslatedintooperationaltermswithineachfisheryCurrentlyleg-islatedoragreedby-catch reductiongoals tend tobe less specificthantheycouldbeandthisleadstoproblemsininterpretingthesegoals inordertoplanaby-catchmitigationstrategy(seethecase-studies inTable3 for examples) This ambiguity is tobe expectedwithinnegotiatedtargetsbutitisachallengenonetheless(Maxwelletal2015)Usingacommonunitofby-catch impactsuchastheΔλTwhichweuseherewouldbehelpfulbothinclarifyingexpecta-tionsandevaluatingtheeffectivenessofelementsofthemitigationhierarchy

Once the by-catch goal is known options for implementingavoidanceminimizationremediationandoffsetscanbeclarified(asinTable2)Howeveroutsideof the interconnectedbiologyof theecosystemby-catch isembeddedwithinsocialandeconomicsys-temsDifferentunitsofanalysismaybeneededatdifferent levelsofthehierarchytocopewiththechallengesofincompleteoverlapbetween jurisdictional units fisheries target stocks and by-catchstocksJurisdictionalissuesareimportantandcomplexpotentiallyimpeding implementationFleets interact raisingtheriskofpolicyleakageforexampleifpeopleshifttootherfisheriesgearorliveli-hoodsThereforethescaleatwhicheachelementofthemitigationhierarchyisimplementedislikelytovarywithincentivestomitigateoftenbeingbest appliedat thevessel level focussedon reducingindividualmortalitywhileoffsettingisimplementedatthescaleoftheby-catchspeciesrsquostockWithtransboundaryspeciesunilateralconservationinonejurisdictioncreatesthepotentialforproductiontrade and conservation leakages For example a conserving Statecouldimplementtheavoidancestepandshutdownordramaticallycurtailitsownproductionofswordfishtoreduceseaturtleby-catchbuttheknock-oneffectmaybemoreimportationofswordfishfromfleetswithhigherseaturtleby-catch(RausserHamiltonKovachampStifter2009)

Translatingtheframeworkfromaspeciestoanecosystemlevelwill require consideration of the potential interactions between

12emsp |emsp emspensp MILNER- GULLAND Et AL

by-catchmitigationapproachestargetedatdifferentspecies(Serafyetal 2012) Actions to mitigate by-catch for one group of spe-cies can increase or decrease it for others and so a system-wideapproach isneededForexample changing fromJ-hooks tocirclehookstoreducemortalityofturtlesmaydecreaseorincreasesharkmortality(Andrakaetal2013GodinCarlsonampBurgener2012)In terrestrial systems similar interactions arise and value judge-mentsaremade(whetherexplicitlyorimplicitly)astowhatlossandgain of ldquobiodiversityrdquo translates to in operational terms andwhatelementsofbiodiversitymattermosttoimplementers

Uncertainty is high in ocean ecosystems creating both chal-lengesandopportunitiesinapplyingtheconceptofNNLthroughamitigationhierarchythatincludesoffsettingInparticularformarinemegafaunathereishighuncertaintyintheprocesseslinkinganyel-ementofthemitigationhierarchythroughtochangesinpopulationgrowthrateFurthermore impactscanbelong-termhardtomea-sureandspatiallydiffuseanduncertaintyisnotpredictablyspreadthroughthehierarchyThiscreatesadifferentsetofchallengestothosefacedinterrestrialsystemswhereatleastforsometypesofenvironmentalimpactthelinksbetweenactionandimpactarerel-ativelydirectandmeasurableanduncertaintygenerally increasesthroughthemitigationhierarchy (fromavoidthroughminimizere-mediatetooffset)

By-catch reduction measures have had significant successesoverthelastdecadesasaresultofsubstantialinvestmentoftimeand funding by researchers management authorities conserva-tionorganizationsandfishers(Coxetal2007)Howeverthissuc-cessisnotuniversalJustasforanyfisheriesmanagementissueapoorregulatoryregimelimitedcomplianceandlackofinforma-tionhampereffortstoreduceby-catchInsomeplaceshighlevelsofby-catch limitedoptions formitigationandweakgovernance(leadingtopoorenforcement)cancombinetomaketheby-catchproblemintractableOurframeworkwillnotsolvetheseproblemsHowever itbrings together the full rangeofapproaches forby-catchmitigationinastructuredandsystematicwaywhichrequiresatargettobeexpressedagainstwhichoutcomescanbeevaluatedByexposingareasofuncertaintyanddatadeficiencyitcouldchal-lengescientistsandmanagerstoobtainthedatarequiredproperlytoevaluate theeffectivenessofmitigationmeasuresThis couldthensupportandencourageclearerdecision-makingandprioriti-zationofactionsOurframeworkdemonstratesthattheprincipleof implementing thegoalofnonet loss throughamitigationhi-erarchy isasapplicable tomarinemegafaunaby-catchas to ter-restrial systems where it is already widely used in challengingdata-poorcircumstances

There isuntappedpotential forcost-effectiveby-catchmitiga-tionwhichcouldberealizedwiththeadoptionofthisframeworkandwithconsiderationofnewapproachestoincentivizingby-catchmitigationwithinthestepsofthehierarchyApplyingittoafewcase-studiesinpracticewilldemonstrateempiricallywhereandhowthepotentialforimprovedeffectivenesscouldbestberealizedExistinglegalframeworksoftenprecludeapproacheswhichimplicitlyorex-plicitly permit by-catch including the use of economic incentives

ornewapproachessuchasoffsetsHoweverinthiscontextofdy-namicuncertaintythedividendsofthinkingmorecreativelyaboutby-catchmitigationcouldbehigh

ACKNOWLEDG EMENTS

EJMG acknowledges the Pew Charitable Foundation for its sup-port of thiswork This article originated at a 2013workshop co-organized by NOAA-Fisheries and IUCN-CEEM-FEG entitledldquoMultidisciplinaryWorkshoptoAddressEcosystem-LevelImpactsofFisheriesBycatchonMarineMegafaunaBiodiversityConservationthrough Mitigation Policy Economic Instruments and TechnicalChangerdquo We thank the reviewers for their insightful commentswhichmuchimprovedthemanuscript

ORCID

E J Milner-Gulland httporcidorg0000-0003-0324-2710

R E FE R E N C E S

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Alfaro-Shigueto JMangel JCBernedoFDuttonPHSeminoffJAampGodleyB J (2011) Small-scale fisheriesofPeruAmajorsinkformarineturtles inthePacificJournal of Applied Ecology481432ndash1440httpsdoiorg101111j1365-2664201102040x

Alfaro-ShiguetoJMangelJCPajueloMDuttonPHSeminoffJ A amp Godley B J (2010) Where small can have a large im-pact Structure and characterization of small-scale fisheries inPeru Fisheries Research 106 8ndash17 httpsdoiorg101016jfishres201006004

Andraka SMugM HallM PonsM Pacheco L ParralesM hellipOrtega D (2013) Circle hooks Developing better fishing prac-ticesintheartisanallonglinefisheriesoftheEasternPacificOceanBiological Conservation 160 214ndash224 httpsdoiorg101016jbiocon201301019

ApostolopoulouEampAdamsWM(2017)BiodiversityoffsettingandconservationReframingnaturetosaveitOryx5123ndash31httpsdoiorg101017S0030605315000782

BaacuteezJCRealRGarciacutea-SotoCJoseacuteMMaciacuteasDampCamintildeasJA(2007)Loggerheadturtleby-catchdependsondistancetothecoastindependentoffishingeffortImplicationsforconservationandfish-eries management Marine Ecology Progress Series 338 249ndash256httpsdoiorg101017S0030605315000782

BBOP (2012) Standard on biodiversity offsets Business and biodiversity offsets programmeWashingtonDCForestTrends

Bishop J (2006) Standardizing fishery-dependent catch and ef-fort data in complex fisheries with technology change Reviews in Fish Biology and Fisheries 16 21ndash38 httpsdoiorg101007s11160-006-0004-9

BoyceJ(1996)AneconomicanalysisofthefisheriesbycatchproblemJournal of Environmental Economics and Management31 314ndash336httpsdoiorg101006jeem19960047

BugoniLManciniPLMonteiroDSNascimentoLampNevesTS(2008)SeabirdbycatchintheBrazilianpelagiclonglinefisheryandareviewofcaptureratesinthesouthwesternAtlanticOceanEndangered Species Research5137ndash147httpsdoiorg103354esr00115

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BullJWampBrownlieS(2017)Thetransitionfromnonetlosstoanetgainof biodiversity is far from trivialOryx51 53ndash59 httpsdoiorg101017S0030605315000861

BullJWBryantCBakerJampMilner-GullandEJ(2015December28)Developing measuring and communicating the outcomes of cor-porate biodiversity strategies [pdfdocument]RetrievedfromhttpwwwwildbusinessorgBull_etal_2015_WBLpdf

BullJWGordonAWatsonJEampMaronM(2016)Seekingcon-vergenceonthekeyconceptsinlsquononetlossrsquopolicyJournal of Applied Ecology531686ndash1693httpsdoiorg1011111365-266412726

BullJWHardyMJMoilanenAampGordonA (2015)Categoriesof flexibility in biodiversity offsetting and their implications forconservation Biological Conservation 192 522ndash532 httpsdoiorg101016jbiocon201508003

Bull JW Lloyd S P amp StrangeN (2017) Implementation gap be-tween the theory and practice of biodiversity offset multipliersConservation Lettershttpsdoiorg101111conl12335

Bull JW SuttleKBGordonA SinghN JampMilner-Gulland EJ(2013)BiodiversityoffsetsintheoryandpracticeOryx47369ndash380httpsdoiorg101017S003060531200172X

CampbellLMampCornwellML(2008)Humandimensionsofbycatchreduction technology Current assumptions and directions for fu-tureresearchEndangered Species Research5325ndash334httpsdoiorg103354esr00172

Caswell H Brault S Read A J amp Smith T D (1998) Harborporpoise and fisheries An uncertainty analysis of inciden-tal mortality Ecological Applications 8 1226ndash1238 httpsdoiorg1018901051-0761(1998)008[1226hpafau]20co2

ClementsTJohnANielsenKAnDTanSampMilner-GullandEJ (2010)Payments forbiodiversityconservation in thecontextofweak institutions Comparison of three programs from CambodiaEcological Economics 69 1283ndash1291 httpsdoiorg101016jecolecon200911010

CoxTLewisonRŽydelisRCrowderLSafinaCampReadA(2007)ComparingeffectivenessofexperimentalandimplementedbycatchreductionmeasuresTheidealandtherealConservation Biology211155ndash1164httpsdoiorg101111j1523-1739200700772x

CrollDADewarHDulvyNKFernandoDFrancisMPGalvaacuten-Magantildea F hellip Newton K M (2016) Vulnerabilities and fisher-ies impactsTheuncertain futureofmanta anddevil raysAquatic Conservation Marine and Freshwater Ecosystems 26 562ndash575httpsdoiorg101002aqc2591

Damalas D amp Vassilopoulou V (2013) Slack regulation com-pliance in the Mediterranean fisheries A paradigm from theGreek Aegean Sea demersal trawl fishery modelling discardogives Fisheries Management and Ecology 20 21ndash33 httpsdoiorg101111j1365-2400201200860x

DuttonDLDuttonPHChaloupkaMampBoulonRH(2005)IncreaseofaCaribbeanleatherbackturtleDermochelys coriaceanestingpop-ulation linked to long-termnestprotectionBiological Conservation126186ndash194httpsdoiorg101016jbiocon200505013

DuttonPJosephJSquiresDampWilliamsM(2011)Bellagioblue-print foractiononseaturtlesChapter2 InPDuttonDSquiresampM Ahmed (Eds) Conservation of pacific sea turtles (pp 15ndash36)HonoluluHIUniversityofHawaiiPress

DuttonPampSquiresD (2008)AholisticstrategyforPacificseatur-tlerecoveryOcean Development and International Law39200ndash222httpsdoiorg10108000908320802013685

FAO (2011 January 5) International guidelines on bycatch manage-ment and reduction of discards Rome Italy Food and AgricultureOrganisation [pdf document] Retrieved from httpwwwfaoorgdocrephelliptba0022t00pdf

Finkelstein M Bakker V Doak D F Sullivan B Lewison RSatterthwaite W H hellip Henry R W (2008) Evaluating the po-tential effectiveness of compensatory mitigation strategies for

marinebycatchPLoS ONE3 e2480httpsdoiorg101371jour-nalpone0002480

FowlerSJ(2016January5)Draft best practice mitigation guidelines for sharks and rays taken in purse- seine and long-line fisheries Convention on Migratory Species[pdfdocument]RetrievedfromhttpwwwcmsintsitesdefaultfilesdocumentCMS_Sharks_CWG1_Doc_3_2pdf

FrancisMP(2014)Survival and depth distribution of spinetail devilrays (Mobula japanica) released from purse-seine catches NIWA ClientReportNoWLG2014-2WellingtonNewZealandDepartmentofConservation

Fulton E A Smith A D Smith D C amp van Putten I E (2011)Human behaviour The key source of uncertainty in fish-eries management Fish and Fisheries 12 2ndash17 httpsdoiorg101111j1467-2979201000371x

GardnerTAHaseABrownlieSEkstromJMPilgrimJDSavyCEhellipTenKateK(2013)BiodiversityoffsetsandthechallengeofachievingnonetlossConservation Biology271254ndash1264httpsdoiorg101111cobi12118

GjertsenHHallMampSquiresD(2010)IncentivestoaddressbycatchInRAllenJJosephampDSquires(Eds)Conservation and manage-ment of transnational tuna fisheries (pp225ndash250)Ames IAWiley-Blackwellhttpsdoiorg1010029780813820262ch14

Gjertsen H Squires D Dutton P amp Eguchi T (2014) Cost-effectivenessofalternativeconservationstrategieswithapplicationtothePacificLeatherbackTurtleConservation Biology28140ndash149httpsdoiorg101111cobi12239

GodinACCarlson JKampBurgenerV (2012)Theeffectofcirclehooks on shark catchability and at-vessel mortality rates in long-lines fisheriesBulletin of Marine Science88 469ndash483 httpsdoiorg105343bms20111054

GrimmDBarkhornIFestaDBonzonKBoomhowerJHovlandV amp Blau J (2012) Assessing catch sharesrsquo effects evidencefrom Federal United States and associated British Columbianfisheries Marine Policy 36 644ndash657 httpsdoiorg101016jmarpol201110014

HallMA(1996)OnbycatchesReviews in Fish Biology and Fisheries6319ndash352httpsdoiorg101007BF00122585

HallMAAlversonDLampMetuzalsKI(2000)By-catchProblemsand solutions Marine Pollution Bulletin 41 204ndash219 httpsdoiorg101016S0025-326X(00)00111-9

HallMANakanoHClarke S Thomas SMolloy J PeckhamSHhellipHallSJ (2007)Workingwithfisherstoreduceby-catchesIn S J Kenelly (Ed)By-catch reduction in the worldrsquos fisheries (pp235ndash288) Dordrecht The Netherlands Springer httpsdoiorg101007978-1-4020-6078-6_8

HallM amp RomanM (2013)Bycatch and non-tuna catch in the tropi-cal tuna purse seine fisheries of the worldFisheriesandAquacultureTechnicalPaper568RomeItalyFAO

HallMASwimmerYampPargaM(2012)NoldquosilverbulletsrdquobutplentyofoptionsWorkingwiththeeasternpacificartisanalfisherstore-duceseaturtlemortalityinfisheriesInJASeminoffampBWallace(Eds)Sea turtles of the eastern pacific Advances in research and con-servation(pp136ndash153)TucsonAZUniversityofArizonaPress

HamnerRMWadePOremusMStanleyMBrownPConstantineR amp Baker C S (2014) Critically low abundance and limits tohuman-relatedmortalityfortheMauirsquosdolphinEndangered Species Research2687ndash92httpsdoiorg103354esr00621

HatchSA(2003)Statisticalpowerfordetectingtrendswithapplica-tions to seabird monitoringBiological Conservation 111 317ndash329httpsdoiorg101016S0006-3207(02)00301-4

HeppellSSCrowderLBampCrouseDT(1996)Modelstoevaluateheadstartingasamanagementtoolforlong-livedturtlesEcological Applications6556ndash565httpsdoiorg1023072269391

HoughPampRobertsonM(2009)MitigationunderSection404oftheCleanWater ActWhere it comes from what it meansWetlands

14emsp |emsp emspensp MILNER- GULLAND Et AL

Ecology and Management 17 15ndash33 httpsdoiorg101007s11273-008-9093-7

IATTC(2015)Resolution on the conservation of mobulid rays caught in as-sociation with fisheries in the IATTC convention area Inter-AmericanTropical TunaCommission89thAnnualMeetingResolutionC-15-04LaJollaCAInter-AmericanTropicalTunaCommission

IFC(2012)Performance standard 6 Biodiversity conservation and sustain-able management of natural resources January 1 2012WashingtonDCInternationalFinanceCorporation

Innes J Pascoe S Wilcox C Jennings S amp Paredes S (2015)MitigatingundesirableimpactsinthemarineenvironmentAreviewofmarket-basedmanagementmeasuresFrontiers in Marine Science276httpsdoiorg103389fmars201500076

JanniseCSquiresDSeminoffJampDuttonP (2010)Conservationinvestments andmitigationTheCaliforniadrift gillnet fishery andpacificseaturtles InRQGraftonRHilbornDSquiresMTaitampMJWilliams(Eds)Handbook of marine fisheries conservation and management(pp231ndash240)OxfordUKOxfordUniversityPress

Jones E amp FrancisM (2012)Protected rays ndash Occurrence and devel-opment of mitigation methods in the New Zealand tuna purse seine fishery Auckland New Zealand National Institute of Water andAtmosphericResearch

KormosRKormosCFHumleTLanjouwARainerHVicturineR hellipWilliamson E A (2014) Great apes and biodiversity offsetprojectsinAfricaThecasefornationaloffsetstrategiesPLoS ONE9(11)e111671httpsdoiorg101371journalpone0111671

KotchenMJ (2013)Voluntaryand information-basedapproachestoenvironmentalmanagementApubliceconomicsperspectiveReview of Environmental Economics and Policy 7(2) 276ndash295 httpsdoiorg101093reepret012

Kyriazi Z LejanoRMaes FampDegraer S (2015)Bargaining a netgaincompensationagreementbetweenamarinerenewableenergydeveloperandamarineprotectedareamanagerMarine Policy6040ndash48httpsdoiorg101016jmarpol201506005

LentRampSquiresD(2017)ReducingmarinemammalbycatchinglobalfisheriesAneconomicsapproachDeep Sea Research Part II Topical Studies in Oceanography 140 268ndash277 httpsdoiorg101016jdsr2201703005

Lewison R L Crowder L B Read A J amp Freeman S A (2004)Understanding impactsof fisheriesbycatchonmarinemegafaunaTrends in Ecology amp Evolution19598ndash604httpsdoiorg101016jtree200409004

MannC (2015)StrategiesforsustainablepolicydesignConstructiveassessmentofbiodiversityoffsetsandbankingEcosystem Services16266ndash274httpsdoiorg101016jecoser201507001

Marine Stewardship Council (2014 June 21) MSC fisheries certifica-tion requirements v20 [pdf doc] httpswwwmscorgdocumentsscheme-documentsfisheries-certification-scheme-documentsfisheries-certification-requirements-version-20

MaronM IvesCDKujalaHBullJWMaseykFJBekessyShellip Possingham H P (2016) Taming a wicked problem Resolvingcontroversies inbiodiversityoffsettingBioScience66(6)489ndash498httpsdoiorg101093bioscibiw038

MaxwellSLMilner-GullandEJJonesJPKnightATBunnefeldNNunoAhellipRhodesJR(2015)BeingsmartaboutSMARTenvi-ronmentaltargetsScience3471075ndash1076httpsdoiorg101126scienceaaa1451

Moilanen A Van Teeffelen A J Ben-Haim Y amp Ferrier S (2009)Howmuch compensation is enoughA framework for incorporat-inguncertaintyandtimediscountingwhencalculatingoffsetratiosfor impactedhabitatRestoration Ecology17 470ndash478 httpsdoiorg101111j1526-100X200800382x

MorarNToadvineTampBohannanBJ(2015)Biodiversityattwenty-fiveyearsRevolutionorredherringEthics Policy amp Environment1816ndash29httpsdoiorg1010802155008520151018380

OrphanidesCDampPalkaDL(2013)Analysisofharborporpoisegill-netbycatchcomplianceandenforcement trends in theUSnorth-western Atlantic January 1999 to May 2010 Endangered Species Research20251ndash269httpsdoiorg103354esr00499

Pascoe S Innes J Holland D Finas M Theacutebaud O TownsendR hellip Hutton T (2010) Use of incentive-based managementsystems to limit bycatch and discarding International Review of Environmental and Resource Economics 4 123ndash161 httpsdoiorg10156110100000032

PhalanBHayesG Brooks SMarshDHoward PCostelloeBhellip Whitaker S (2017) Avoiding impacts on biodiversity throughstrengthening the first stage of the mitigation hierarchy Oryxhttpsdoiorg101017S0030605316001034

Queacutetier F Regnery B amp Levrel H (2014) No net loss of biodiver-sity or paper offsets A critical review of the French no net losspolicy Environmental Science amp Policy 38 120ndash131 httpsdoiorg101016jenvsci201311009

RadzioTASmolinskyJAampRoosenburgWM(2013)Lowuseofre-quiredterrapinbycatchreductiondevicesinarecreationalcrabpotfisheryHerpetological Conservation and Biology8222ndash227

RaineyHJPollardEHBDutsonGEkstromJMLivingstoneSRTempleHJampPilgrimJD(2015)AreviewofcorporategoalsofnonetlossandnetpositiveimpactonbiodiversityOryx49232ndash238httpsdoiorg101017S0030605313001476

Rausser G C Hamilton S F Kovach M amp Stifter R (2009)UnintendedconsequencesThe spillovereffectsof commonprop-ertyregulationsMarine Policy3324ndash39httpsdoiorg101016jmarpol200803020

Rice J (2014) Evolution of international commitments for fisheriessustainability ICES Journal of Marine Science Journal du Conseil71157ndash165httpsdoiorg101093icesjmsfst078

RichardYampAbrahamER(2013)ApplicationofPotentialBiologicalRemoval methods to seabird populations New Zealand AquaticEnvironmentandBiodiversityReport108

RodeJGoacutemez-BaggethunEampKrauseT(2015)Motivationcrowd-ingbyeconomic incentives inconservationpolicyAreviewoftheempiricalevidenceEcological Economics117270ndash282httpsdoiorg101016jecolecon201411019

RogersAA(2013)SocialwelfareandmarinereservesIswillingnesstopayforconservationdependentonmanagementprocessAdiscretechoiceexperimentoftheNingalooMarineParkinAustraliaCanadian Journal of Agricultural EconomicsRevue Canadienne Drsquoagroeconomie61217ndash238httpsdoiorg101111cjag12008

Rosenberg A A amp McLeod K L (2005) Implementing ecosystem-basedapproachestomanagementfortheconservationofecosystemservicesMarine Ecology Progress Series300 270ndash274 httpsdoiorg103354meps300270

Segerson K (2010) Can voluntary programs reduce sea turtle by-catch Insights from the literature in environmental economics InRQGraftonRHilbornDSquiresMTaitampMJWilliams(Eds)Handbook of marine fisheries conservation and management(pp618ndash629)OxfordUKOxfordUniversityPress

Serafy JECookeS JDiazGAGraves JEHallMShivjiMampSwimmerY(2012)CirclehooksincommercialrecreationalandartisanalfisheriesResearchstatusandneedsforimprovedconser-vation and management Bulletin of Marine Science 88 371ndash391httpsdoiorg105343bms20121038

ShiodeDHu F ShigaM Yokota K amp Tokai T (2005)Midwaterfloatsystemforstandardizinghookdepthsontunalonglinestore-duce sea turtleby-catchFisheries Science71 1182ndash1184httpsdoiorg101111j1444-2906200501080x

Sims M Cox T amp Lewison R (2008) Modeling spatial patternsin fisheries bycatch Improving bycatch maps to aid fisheriesmanagement Ecological Applications 18 649ndash661 httpsdoiorg10189007-06851

emspensp emsp | emsp15MILNER- GULLAND Et AL

Squires D amp Garcia SM (2014) Ecosystem-level impacts of fisheries bycatch on marine megafauna Biodiversity conservation through miti-gation policy economic instruments and technical changeReportofthe IUCN-CEM-FEGScientificworkshopGland Switzerland 7ndash10October2013GlandSwitzerlandIUCN

SquiresDampGarciaSM(inpress)Fisheries bycatch in marine ecosys-tems Policy economic instruments and technical change ChichesterUKJWileyampSons

SwimmerYArauzRMcCrackenMMcNaughtonLBallesteroJMusylMhellipBrillR(2006)DivingbehavioranddelayedmortalityofoliveridleyseaturtlesLepidochelys olivaceaaftertheirreleasefromlongline fishing gearMarine Ecology Progress Series323 253ndash261httpsdoiorg103354meps323253

TolottiMTFilmalterJDBachPTravassosPSeretBampDagornL(2015)BanningisnotenoughThecomplexitiesofoceanicsharkmanagementbytunaregional fisheriesmanagementorganizationsGlobal Ecology and Conservation 4 1ndash7 httpsdoiorg101016jgecco201505003

Tuck G N Polacheck T amp Bulman C M (2003) Spatio-temporaltrendsoflonglinefishingeffortintheSouthernOceanandimplica-tionsforseabirdbycatchBiological Conservation1141ndash27httpsdoiorg101016S0006-3207(02)00378-6

UNEP-WCMC(2016)Marine no net loss A feasibility assessment of imple-menting no net loss of biodiversity in the seaCambridgeUKUnitedNationsEnvironmentProgramme

Vaissiegravere A-C Levrel H Pioch S amp Carlier A (2014) Biodiversityoffsets for offshore wind farm projects The current situation inEurope Marine Policy 48 172ndash183 httpsdoiorg101016jmarpol201403023

Wallace B P Heppell S S Lewison R L Kelez S amp CrowderL B (2008) Impacts of fisheries bycatch on loggerhead tur-tles worldwide inferred from reproductive value analy-ses Journal of Applied Ecology 45 1076ndash1085 httpsdoiorg101111j1365-2664200801507x

Wanless R M Ryan P G Altwegg R Angel A Cooper JCuthbert R amp Hilton G M (2009) From both sides Dire de-mographic consequences of carnivorous mice and longlining for

the critically endangered Tristan albatrosses on Gough IslandBiological Conservation 142 1710ndash1718 httpsdoiorg101016jbiocon200903008

WardP LawrenceEDarbyshireRampHindmarshS (2008) Large-scale experiment shows that nylon leaders reduce shark bycatchandbenefitpelagiclonglinefishersFisheries Research90100ndash108httpsdoiorg101016jfishres200709034

WardTampPhillipsB(2010)SeafoodecolabelingInRQGraftonRHilbornDSquiresMTaitampMJWilliams(Eds)Handbook of ma-rine fisheries conservation and management (pp 608ndash617) OxfordUKOxfordUniversityPress

WilcoxCampDonlanCJ (2007)Compensatorymitigationasasolu-tion to fisheries bycatch-biodiversity conservation conflictsFrontiers in Ecology and the Environment 5 325ndash331 httpsdoiorg1018901540-9295(2007)5[325cmaast]20co2

WilcoxCampDonlanCJ (2009)NeedforaclearandfairevaluationofbiodiversityoffsetsforfisheriesbycatchConservation Biology23770ndash772httpsdoiorg101111j1523-1739200901173x

Wolf SHartlBCarrollCNeelMCampGreenwaldDN (2015)Beyond PVAWhy recovery under the Endangered Species Act ismorethanpopulationviabilityBioScience65200ndash207httpsdoiorg101093bioscibiu218

ZedlerJBampCallawayJC (1999)TrackingwetlandrestorationDomitigation sites follow desired trajectories Restoration Ecology 769ndash73httpsdoiorg101046j1526-100X199907108x

Žydelis R Wallace B P Gilman E L amp Werner T B (2009)Conservation of marine megafauna through minimization of fish-eries bycatch Conservation Biology 23 608ndash616 httpsdoiorg101111j1523-1739200901172x

How to cite this articleMilner-GullandEJGarciaSArlidgeW etalTranslatingtheterrestrialmitigationhierarchytomarinemegafaunaby-catchFish Fish 2018001ndash15 httpsdoiorg101111faf12273

Page 8: Translating the terrestrial mitigation hierarchy to marine ......of marine megafauna by-catch in fisheries, going from defining an overarching goal with an associated quantitative

8emsp |emsp emspensp MILNER- GULLAND Et AL

2009)Bycontrastinfisheriessettingstherehavebeensuggestionsthatdependingonthelegalenvironmentitmaybemoreappropriateforoffsetstobeusedaspartofaleast-costconservationapproachalongsidemoretraditionalmitigationmethodsratherthanasthelaststep inamitigationhierarchy (DuttonJosephSquiresampWilliams2011DuttonampSquires2008WilcoxampDonlan2007)

42emsp|emspOut- of- kind offsets

Out-of-kind offsets are those which do not act to increase theimpact-affectedbiodiversityIntermsofourconceptualframeworktheyareoffsetswhichdonotacttoincreasethepopulationgrowthrateoftheby-catch-affectedfocalpopulation(Equation1)Forex-ampleonesuggestedbenefitof raising funds foroffsetting fromaby-catchtaxonfishersisthattheproceedsfromsuchataxcanfinanceoffsetselsewherewithintherangeoftheby-catch-affectedpopulation (Dutton amp Squires 2008) Although not a true offsetunderamitigationhierarchyfundsfromtheCaliforniadriftgillnetindustry in 2002 financed sea turtle nesting site conservation inBajaCaliforniaforcompensatorymitigationofseaturtleby-catch(Jannise Squires Seminoff amp Dutton 2010) In terrestrial (andmarine)systems itcanbemorechallengingtodefinethe impact-affected biodiversity because impact is rarely as clearly linkedtoagivenspeciesandstockas it is forby-catchBecauseofthisthelocationandbiodiversitytargetofconservationactionsfallingundertheldquooffsetrdquoheadinghassometimesbeenlooselyrelatedtotheactual impactBest-practicestandardsstatethatoffsetsmustbeimplementedasclosetothedamagingactivitiesaspossibleandfocusonbiodiversityassimilaraspossibletothatwhichhasbeenimpacted (BBOP 2012) However there have also been calls forldquoout-of-kindrdquooffsetsthatgivemoreconservationbang-for-buckbyfocussingonthreatenedspeciesorrarehabitatsorareasinneedofconservation rather than the impactedareasor specieswhichmay be considered less ldquovaluablerdquo for conservation (Bull Hardyetal2015)Thishasledtosubstantialdebateastotheappropri-atelimitsonthegeographicscaleandbiodiversityfocusforoffset-ting(egApostolopoulouampAdams2017)Italsodrawsattentiontothesubjectiveanduser-definednatureof theword ldquobiodiversityrdquo(Morar ToadvineampBohannan 2015) As it is impossible fully tooperationalizetheconceptimplementersofthemitigationhierar-chyhavelatitudetointerpretbiodiversityaccordingtoforexampleeaseofmeasurement perceived societal valueormitigation cost(Maron etal 2016) In our casewe take a narrow focus on theby-caughtspecies itself this is in linewithmuchof the literatureon by-catch but notwith the broader discourses on ecosystem-basedapproachestomarinemanagementandecosystemservices(RosenbergampMcLeod2005)Thesediscoursessuggest theneedforamorefunctionalecosystem-basedapproachtononetlossofbiodiversitythishasyettotranspireeitherinthemarineorintheterrestrialliteraturepossiblybecausesubstantialchallengesinde-finingimpact-affectedbiodiversitytheninevitablyensue

Asmarinemegafauna stocks are often transboundary andmi-gratorydefiningtheappropriatespatialunit foroffsettingmaybe

achallengebecause themosteffective location foranoffsetmayormaynotbewithintheareaofinfluenceofagivenfisheryClearlyandpreciselydefining the spatial unitwithinwhich themitigationhierarchywill be implemented during theprocess of defining theoverallgoal(suchasNNL)isvitalThisunitshouldreflectthescaleoverwhichanactionwillaffectλToffsetswhicharewithinthedis-tributionofthefocalstockoftheby-caughtspecies(asdefinedforEquation1)arenotout-of-kindHoweverchallengesemergewhenthe appropriate spatial unit for offsetting activities is different totheappropriatespatialunitforotherelementsofthemitigationhi-erarchywhicharelikelytobedefinedinsteadbyjurisdictionalareaor target fish stock distribution Inmany fisheries the species af-fectedbyby-catchmaynotbewellenoughknownandoffsetsmayaccordinglyneedtobebroadlytargetedtobenefitanypotentiallyaffectedspeciesTrueout-of-kindoffsetswouldincludefundingtheconservationofunaffectedspeciesorstocksofhabitatsnotusedbythefocalstockorcontributionstoaconservationfundwithoutaclearcommitmentthatthefundsaretobespentonincreasingλT for thefocalby-caughtstockTheseareunlikelytoformpartofbest-practiceguidanceforby-catchoffsets

43emsp|emspResearch as an offset

Arelatedareaofactivecontroversyformarineby-catchiswhetherresearchor informationgatheringshouldbeseenasavalidoffsetmechanism The rationale is that this research could be used toreduceuncertaintypromote innovationand thereby improveout-comes for by-caught species albeit indirectly An offset could beusedto incentivizebetterdatacollectionfor instanceusingaby-catchlevytopayfortaggingortoputby-catchobserversorelec-tronicmonitoringsystemsonboatsThismightbeapreludetolatermitigation or avoidance activities once more is known about thebiological settingWhether research activities could appropriatelybeconsideredaspartofanldquooffsetrdquoiscontroversialmdashinsomecasesan indirectbenefit to theby-caught stockmightbe clearly appar-ent(egtheoceanicwhitetip(Carcharinus longimanusCarcharinidae)case-studyinTable3)whileinothercasesusinginvestmentinre-searchasanoffsetcouldbeseenasacaseofmoralhazardpoten-tially compromising scientistsrsquo independence and having at best ahighlyindirectrelationshiptoNNLoftheby-caughtspeciesAnotherviewisthatreducinguncertaintyisacoreresponsibilityofoperatingafisherywhichthereforeshouldbebornebythemanagementau-thorityorfishingbusinessesInterrestrialsystemsthesedilemmasalsoexistbutthesentimentismuchmoreclearlyexpressedthatre-searchactivitiesarenotappropriateoffsets(BullGordonWatsonampMaron2016)

44emsp|emspIncentivizing implementation of mitigation measures

Thefactorsthatdrivedecision-makingaboutmegafaunaby-catchreduction (by skippers companies fishery managers policymak-ers and other stakeholders) include legal obligations tominimize

emspensp emsp | emsp9MILNER- GULLAND Et AL

by-catch at the national or international levels (eg FAO 2011Rice 2014) the availability and quality of technical fixes associ-atedcosts tofishers limitsonaccesstoseafoodmarketsaswellassocietalpressuresHowevermuchresearchonby-catchreduc-tion focuses on identifying and implementing technicalmeasuresto reduceBPUE rather thanon the social andeconomicbarriersto implementation (Campbell amp Cornwell 2008) Technologicalinnovation to improve BPUE needs to be appropriately incentiv-izedwitheffortsmadetoensurethatsuchmeasuresareascost-effective as possible for fishers (Gjertsen Hall amp Squires 2010Lent amp Squires 2017) However it often happens that even ap-parently suitable by-catchmeasures are notwidely implemented(eg Damalas amp Vassilopoulou 2013 Orphanides amp Palka 2013RadzioSmolinskyampRoosenburg2013)Inthesecasesthedegreeofnon-implementationandthereasonsbehinditneedstobeun-derstoodsoitcanbeaddressed(Coxetal2007)Thesetypesofconsiderationarealsonotwellresearchedintheterrestrialoffset-tingliteraturebecausecomplianceispoorlymonitored(BullSuttleGordonSinghampMilner-Gulland2013)andthereislittlesupportfor researchon thebarriers to implementationofamitigationhi-erarchyandhowtosupportdeveloperstoaddressthesebarriers(BullBryantBakerampMilner-Gulland2015)Thesocialimpactsofimplementingabiodiversitymitigationhierarchyonresourceusersarementioned inguidance (egBBOP2012)buthowtomeasureandaccountforthemisverypoorlyunderstoodThefewstudiesin-vestigatingdeliveryofpromisedoffsetmeasuresinterrestrialsys-temssuggestaverypoorrecord(QueacutetierRegneryampLevrel2014)Therefore the social side of implementing the mitigation hierar-chyand incentivizingcompliance isanarea thatneedsmore andmoreactiveresearchwithinboththeterrestrialandmarinerealms(FultonSmithSmithampvanPutten2011)Thisisparticularlytruewhentheburdenof implementingmitigationapproaches isbornebyrelativelysmall-scaleproducersratherthangovernmentsormul-tinationals(egthepelagiclonglinefisheriesinTable3)

45emsp|emspSocietal limits

Foraspeciesathighriskofextinctioncompleteavoidanceofby-catchmightbethemostdesirablepolicyfrombothamanagementagency and societal perspective In addition with emblematic orhighlythreatenedmarinemegafaunaitmaybeviewedbymembersof the public asmorallywrong to kill any individuals even ifmiti-gationisinplace(egMauirsquosdolphinHamneretal2014) leadingtopressureongovernmentstoreflectthisethicalconcerninregu-lationsThesedilemmasecho the issueof thresholds in terrestrialoffsetswhichrecognizesthattherearesomecriticalareasinwhichdevelopmentisnotsocietallyappropriateregardlessofthepoten-tialformitigationandotherareasinwhichthemitigationhierarchycan be appropriately applied (Bull etal 2013) Examples of loca-tionswhereathresholdapproach isseenasappropriate interres-trial systems include the habitat of highly endangered species orecosystemswhich are limited in extent and irreplaceable (such asoldgrowthforest) In terrestrialsystems therefore themitigation

hierarchyisseenasmostappropriateforapplicationinmorecom-monanddegradedhabitatssuchasfarmlandSimilarlyinfisheriestheremaybesomesituationsinwhichthestockssubjecttoby-catchare so precious or threatened that no level of threat from fishingcanbecontemplatedandotherswherefishingsubjecttoNNLandthemitigationhierarchyisasociallyacceptableapproachInsitua-tions inwhich trade-offs between conservation and developmentareseenasnecessaryoracceptablebywidersocietyasociallicencetooperatemaybegainedthroughadoptingoffsetsintheabsenceofregulationForexampleinsub-SaharanAfricaseverallargedevel-opmentprojectsareattemptingtooffsettheirimpactsongreatapesandtheirhabitats(Kormosetal2014)Aby-catchequivalentmightbe fishing companies voluntarily donating funds for turtle nestingbeachrestorationintheirareaofoperationinadditiontocomply-ingwithregulatoryby-catchmitigationmeasuresThesemeasuresmayimprovetheimageofthecompanywiththegeneralpublicbuttoavoidaccusationsofldquogreenwashingrdquotheireffectivenessneedstobeproperlyscrutinized(Bulletal2016)Transparentlyembeddingthesetypesofactionswithinamitigationhierarchysuchasweareproposing and critically evaluating their contribution to increasingthepopulationgrowthrate(asperEquation1)wouldbeonewaytopromptsuchscrutiny

46emsp|emspUncertainty

The nature of the uncertainties surrounding biology and enforce-ment in themarine setting raisesquestions about theorderingofsteps in themitigationhierarchy inaway that isdissimilar to ter-restrialsystemswherethehierarchyofuncertaintiesmaybecleareranduncertaintyisgenerallylowerForexampleitmaybethattheimpactonoverallpopulationgrowthrateofanoffsetmeasurelikeeradicating invasivespecies fromaseabirdnestinghabitat isbothless uncertain and more cost-effective than avoidance measuressuchasclosingareaswhichmayormaynotbefrequentedbyadultseabirds in a given time-periodGenerally though itmightbe as-sumedthatmeasureswhichtargetlifestagessubjecttohighlevelsofnaturalmortalityorwithinwhichindividualcontributiontoover-allpopulationgrowthrateislow(egheadstartingjuvenileturtles)maybelesseffectiveinachievingNNLthanmeasureswhichtargetreproductivelymatureadultfemales(suchaslivereleasesHeppellCrowderampCrouse1996)Howeverbeforeimplementinganoffsetthataimstoimprovethesurvivalofonelifestageinordertocom-pensatefortheby-catchmortalityofanotherarobustassessmentoftheconsequences(withassociateduncertainties)shouldbecar-ried out through detailed population modelling based on strongempiricalstudies(cfWallaceHeppellLewisonKelezampCrowder2008)Interrestrialsystemstherequirementsequentiallytoapplythemitigationhierarchyisbroadlyunchallengedbutactuallysimilararguments apply For example habitat restoration sits above off-settinginthehierarchyandyetitisalong-termuncertainprocesswhichmayinsomecircumstancesbemuchlesspreferabletoanoff-setusingawell-establishedapproachwhichishighlylikelytoleadtoconservationgains

10emsp |emsp emspensp MILNER- GULLAND Et AL

47emsp|emspTemporal considerations

Thetimingofoffsetsinrelationtootherelementsofthemitigationhierarchyhasbeenthesubjectofdebatewithintheterrestriallitera-tureThemainsuggestionforaddressingthetemporarylossofbio-diversitywhileoffsetscometofruitionhasbeenadoptingmitigationbankingwherebyoffsetsareimplementedinadvanceofpotentiallydamagingactivitiesprovidingbiodiversitycreditswhichcanbeusedtocompensateforlaterlossesThisbothremovesanelementofun-certaintyfromtheoffsetimplementationandreducesthetimelagbetweenlossandgain(Mann2015)Withrespecttomarinemega-faunaby-catchflexibilityintimingprovidesadditionalscopeforcostreduction and benefit enhancementwhichmay not be present intraditionalhabitat-basedterrestrialoffsetsForexampletemporarymeasuressuchasashort-termby-catchtaxtofundanoffsetmaybeusedifmitigationoravoidancemethodstaketimetocomeonlineorifatemporarynudgeisenoughtocausebehaviouralchangeThismightbethecaseifapolicywasneededtoinducefisherstotakeupnewgeartoavoidthecostofanoffsetorifconcernsaboutsafetyoryieldreductionsduringthetransitiontonewgearcouldbeallayedbyatemporarysubsidyforearlyadoptersorapaidparticipatorymoni-toringprogrammeto informwider implementation(egthemobu-lidandsharkcase-studiesinTable3)Justasforhabitatrestoration(ZedlerampCallaway 1999) by-catchoffset strategieswhich targetjuvenilestagesof long-livedspecies (eg turtleheadstartingor in-vasive removal fromseabirdnesting islands)may takemanyyearsfor their effects to become apparent in an increase in populationgrowthratesAdditionaluncertaintyisintroducedbythedifficultyinmonitoringpopulationsofmanyby-catch species (eg seabirdsHatch2003)leadingtouncertainestimatesoftheimpactofoffsetactivitiesonpopulationgrowth(seecase-studiesinTable3)Theseproblemsarenot insuperablehoweverpositivetrendshavebeenreportedinturtlepopulationsoverdecadesasaresultofnestpro-tection(egDuttonDuttonChaloupkaampBoulon2005)

5emsp |emspUSING INCENTIVES TO REDUCE BY- C ATCH

Manyoftheexamplesandprinciplesdiscussedaboveeitherimplic-itlyorexplicitlyrelatetotheeconomicsocialinstitutionalormoralincentivesoperatingondifferentactorsinsideandoutsidethefish-erywhichcanbepositiveornegativeWenowturntoadiscussionofhowincentivescanbeusedtoreduceby-catchwithinourframe-workIncentivescanbeputinplacetochangefisherbehaviourwithrespecttoanyoftheelementsoftheframework (avoidminimizeremediateandoffsetTable3)Althoughdiscussedintheliteraturemostof these incentive approaches are yet tobe implemented inthe realworldparticularly forby-catchThereforeuntil empiricalevidenceoftheireffectivenessisavailablethesesuggestionscomewithacaveat

Financial costsofby-catchmitigationactions canarise for in-stancefromlostcatchcapitalinvestmentsinnewgearormitigation

equipmentor the lossofaccesstoafisheryCostsmayalsoarisefromthedeploymentofby-catchobserversortrainingintheuseofnewgearThesecostscanbepaidbyfishingcompaniesorindivid-ualsorbygovernmentsNGOsorseafoodconsumersWhetherornotcompensationforcostsincurredbyfishersisseenasappropri-atedependsonwhetherby-catchreductionisseenasasocialgoodthatfishersareproviding(inwhichcasetheyshouldbecompensatedforit)orasputtingrighttheharmthattheyaredoingtobiodiver-sitywhilegeneratingtheirownprivategain(ineconomiclanguagewhetherby-catchisviewedasanunpricedexternalityinwhichcasetheyshouldpay)Italsodependsonwhethereconomichardshipwillensueacaseforcompensationofby-catchreductioncostsincurredbypeopledependenton fishing for their livelihoodsmaybemoresympatheticallyreceivedbyotheractorsthanacasemadebyalargemultinationalfishingcompany

Ifby-catchisseenasanunpricedexternalityitmightbesociallyoptimaltotaxfishersfortheirby-catchsothatthisexternalityisin-ternalizedThisplacesanexplicitpriceuponby-catch(Boyce1996Pascoeetal2010SquiresampGarcia2014)Theby-catchprice islikely to be incorporated into the price of the target species andtherebybecomespartofthetargetspeciescostThispricecouldbeset differently for different demographic classesof theby-caughtspecies depending on the impact the loss of an individualwouldhaveonthepopulationAllelsebeingequalputtingapriceonby-catchmeans that theseafoodproduct that is the targetcatchbe-comesmoreexpensiveandconsumershave topaymore for theirseafoodreducingdemandTheninprincipleeveryfirminthesup-plychaineveryvesselandeveryconsumerhaveanincentivetore-duceby-catchuntileacheconomicactorrsquosmarginalcostofby-catchreductionequals thecommonpriceofby-catch that theyall faceOffsetsareonewaytopriceandinternalizetheby-catchexternalitycostIfanoffsettingactioniscostlytoimplementandmustbepaidforwith each unit of by-catch it implicitly prices the residual by-catch In this circumstance the effect from a financial standpointisthesameasaby-catchtaxwiththe levelsetbasedonthecostoftheoffsetVariousinstitutionalstructurestosupportthischargeperunitofby-catcharepossiblewithdifferentimplicationsintermsofthedistributionofcostsandbenefitsForexampleaninsuranceschemecouldbepaidintobyfishersthatpaysoutintheeventofaby-catcheventtherebyspreadingthecostofunavoidablerareby-catcheventsOratradablepermitschemecouldoperatesuchthatfisherswhoexperienceaby-catcheventcanbuyapermitwiththecostvaryingdependingondemandforpermits (henceprovidingavessel-levelincentivetoinnovatetoreduceby-catch)

If there isdemandforconservation inan internationalmarketthen price premiums and market access (through eco-labellingsupply chain certification other food sustainability campaignsWardampPhillips2010)orboycottsactingasstrategicthreatsfromconsumers (Kotchen 2013 Segerson 2010) could act as positiveornegativeeconomic leversonthe fisheryprovidingan incentivefor fishers to reduce their by-catch voluntarily (as has been sug-gested for the Brazilianmahi-mahi fishery Table3) For exampletheMarine StewardshipCouncil now includesby-catchmitigation

emspensp emsp | emsp11MILNER- GULLAND Et AL

intheircertificationprocess(MSC2014)Demand-ledleversmaybemoreorlessapplicableatdifferentlevelsinthehierarchyforexam-pleavoidancemayberelativelyhardtoevidencewhileoffsettingmaybelesseasytoselltoaconsumerthanminimizationorreme-diationConcerns about the unintended consequences of positiveincentives (particularlyfordirectsubsidiesratherthanconditionalincentives)maydeterminewhethertheyareanappropriateinstru-mentinagivencaseForexampletheymaybeinappropriateifthereisariskthattheadditionalmoneyisreinvestedinincreasedfishingcapacityor iftheremaybeconsumptionproductionorconserva-tionleakages(transferoftheproblemsomewhereelse)whetheratthe vessel fishery or trans-national levelHigh transactions costsmayalsolimitthebenefitsofincentivesschemes

Otherchangeswhichmayneedtobeincentivizedforsuccessfulimplementationofby-catchreductionpoliciesmaybelessamenabletofinancialmeasuresatleastpartlybecauseitislessclearhowtoassign financial value to theactionsor to thebenefits and losseswhichtheyproduceForexampleperceivedreductionsinsafetyforfishingcrews(fromweightedlonglinesfor instance)arecoststhatmaybehardtovaluefinanciallyOtherprerequisitesfor long-termsustainable behaviour change such as changes in social norms sothatfishingcommunitiesseeby-catchreductionasappropriatebe-haviourortechnicalskillacquisitionsothattheycanusenewmeth-odsmaybeincentivizedbycarefullydesignedinterventionsworkingwithfishers(Halletal2007)Conservationpoliciesbasedoneco-nomic incentives (extrinsicmotivation) are not always superior tothosebasedupon intrinsicmotivation Infact incentive-basedby-catch reduction policy instruments could even be counterproduc-tivebyreducingtheeffectivenessofintrinsicmotivationdependingupon the situation (although the empirical evidence on this topicisweak RodeGoacutemez-BaggethunampKrause 2015) If the changerequiredforby-catchreductiontoworkmeetscultural resistancethenparticipatory researchmightbeespeciallyeffective inbreak-ingdownbarriersbetweenthosewhowantby-catchreductiontotakeplaceandthosewhoactuallyhavetoimplementit(thefishers)ForexampleinAustraliathegovernment-fundedbodyOceanwatchfacilitatesengagementbetweencommunities thefishing industryseafood suppliers and government to improve knowledge sharing(wwwoceanwatchorgau)Innovationiscrucialinfisheriesandfish-ersareaccustomedtoadoptingnewtechnologyorprocessespo-tentiallymakingan incentivizedparticipatory researchprogrammeespeciallyfruitful

Sometimes the most efficient way to solve problems is a so-cial instrumentoran institutionalchange inplaceoforaswellasan economic instrument For example supporting developmentof fisherorganizations rather than instituting a vessel-level taxorsubsidy might provide the impetus needed to change behaviourInstitutingcatchshares(individualtransferablequotas)mayprovideanenablingenvironmentforby-catchreductionforexamplebypro-motingmoreeffectivemonitoring(Grimmetal2012)Experiencein terrestrial system produces similar insights incentive-basedschemeswhichalsobuildcommunitycohesionandsupportthede-velopment or strengthening of localmanagement institutions are

more effective in the longer run than direct economic incentives(Clementsetal2010)

6emsp |emspCONCLUSIONS

The framework we present here is novel It draws upon and ex-tends the frameworks for conceptualizing by-catch developed byHall (1996) and Hall Alverson andMetuzals (2000) It amalgam-atesHallrsquos frameworkwith themitigationhierarchyasused in theEnvironmental Impact Assessment literature (BBOP 2012) Thesuggestions about goals metric andmitigation actions are drawnfromtheempiricalby-catchliteratureandtheissueswediscussin-tegratetheconcernsoftheextensiveterrestrialandnascentmarineoffsetting literature with the by-catch literature The frameworkmakesclear thatanearlycrucial step is toclarify thegoalofanyby-catch reduction policyOverarching goals like those issued bytheConventiononBiologicalDiversity(egAichiTarget11that10ofmarinehabitatshouldbeunderprotectionby2020)needtobetranslatedintooperationaltermswithineachfisheryCurrentlyleg-islatedoragreedby-catch reductiongoals tend tobe less specificthantheycouldbeandthisleadstoproblemsininterpretingthesegoals inordertoplanaby-catchmitigationstrategy(seethecase-studies inTable3 for examples) This ambiguity is tobe expectedwithinnegotiatedtargetsbutitisachallengenonetheless(Maxwelletal2015)Usingacommonunitofby-catch impactsuchastheΔλTwhichweuseherewouldbehelpfulbothinclarifyingexpecta-tionsandevaluatingtheeffectivenessofelementsofthemitigationhierarchy

Once the by-catch goal is known options for implementingavoidanceminimizationremediationandoffsetscanbeclarified(asinTable2)Howeveroutsideof the interconnectedbiologyof theecosystemby-catch isembeddedwithinsocialandeconomicsys-temsDifferentunitsofanalysismaybeneededatdifferent levelsofthehierarchytocopewiththechallengesofincompleteoverlapbetween jurisdictional units fisheries target stocks and by-catchstocksJurisdictionalissuesareimportantandcomplexpotentiallyimpeding implementationFleets interact raisingtheriskofpolicyleakageforexampleifpeopleshifttootherfisheriesgearorliveli-hoodsThereforethescaleatwhicheachelementofthemitigationhierarchyisimplementedislikelytovarywithincentivestomitigateoftenbeingbest appliedat thevessel level focussedon reducingindividualmortalitywhileoffsettingisimplementedatthescaleoftheby-catchspeciesrsquostockWithtransboundaryspeciesunilateralconservationinonejurisdictioncreatesthepotentialforproductiontrade and conservation leakages For example a conserving Statecouldimplementtheavoidancestepandshutdownordramaticallycurtailitsownproductionofswordfishtoreduceseaturtleby-catchbuttheknock-oneffectmaybemoreimportationofswordfishfromfleetswithhigherseaturtleby-catch(RausserHamiltonKovachampStifter2009)

Translatingtheframeworkfromaspeciestoanecosystemlevelwill require consideration of the potential interactions between

12emsp |emsp emspensp MILNER- GULLAND Et AL

by-catchmitigationapproachestargetedatdifferentspecies(Serafyetal 2012) Actions to mitigate by-catch for one group of spe-cies can increase or decrease it for others and so a system-wideapproach isneededForexample changing fromJ-hooks tocirclehookstoreducemortalityofturtlesmaydecreaseorincreasesharkmortality(Andrakaetal2013GodinCarlsonampBurgener2012)In terrestrial systems similar interactions arise and value judge-mentsaremade(whetherexplicitlyorimplicitly)astowhatlossandgain of ldquobiodiversityrdquo translates to in operational terms andwhatelementsofbiodiversitymattermosttoimplementers

Uncertainty is high in ocean ecosystems creating both chal-lengesandopportunitiesinapplyingtheconceptofNNLthroughamitigationhierarchythatincludesoffsettingInparticularformarinemegafaunathereishighuncertaintyintheprocesseslinkinganyel-ementofthemitigationhierarchythroughtochangesinpopulationgrowthrateFurthermore impactscanbelong-termhardtomea-sureandspatiallydiffuseanduncertaintyisnotpredictablyspreadthroughthehierarchyThiscreatesadifferentsetofchallengestothosefacedinterrestrialsystemswhereatleastforsometypesofenvironmentalimpactthelinksbetweenactionandimpactarerel-ativelydirectandmeasurableanduncertaintygenerally increasesthroughthemitigationhierarchy (fromavoidthroughminimizere-mediatetooffset)

By-catch reduction measures have had significant successesoverthelastdecadesasaresultofsubstantialinvestmentoftimeand funding by researchers management authorities conserva-tionorganizationsandfishers(Coxetal2007)Howeverthissuc-cessisnotuniversalJustasforanyfisheriesmanagementissueapoorregulatoryregimelimitedcomplianceandlackofinforma-tionhampereffortstoreduceby-catchInsomeplaceshighlevelsofby-catch limitedoptions formitigationandweakgovernance(leadingtopoorenforcement)cancombinetomaketheby-catchproblemintractableOurframeworkwillnotsolvetheseproblemsHowever itbrings together the full rangeofapproaches forby-catchmitigationinastructuredandsystematicwaywhichrequiresatargettobeexpressedagainstwhichoutcomescanbeevaluatedByexposingareasofuncertaintyanddatadeficiencyitcouldchal-lengescientistsandmanagerstoobtainthedatarequiredproperlytoevaluate theeffectivenessofmitigationmeasuresThis couldthensupportandencourageclearerdecision-makingandprioriti-zationofactionsOurframeworkdemonstratesthattheprincipleof implementing thegoalofnonet loss throughamitigationhi-erarchy isasapplicable tomarinemegafaunaby-catchas to ter-restrial systems where it is already widely used in challengingdata-poorcircumstances

There isuntappedpotential forcost-effectiveby-catchmitiga-tionwhichcouldberealizedwiththeadoptionofthisframeworkandwithconsiderationofnewapproachestoincentivizingby-catchmitigationwithinthestepsofthehierarchyApplyingittoafewcase-studiesinpracticewilldemonstrateempiricallywhereandhowthepotentialforimprovedeffectivenesscouldbestberealizedExistinglegalframeworksoftenprecludeapproacheswhichimplicitlyorex-plicitly permit by-catch including the use of economic incentives

ornewapproachessuchasoffsetsHoweverinthiscontextofdy-namicuncertaintythedividendsofthinkingmorecreativelyaboutby-catchmitigationcouldbehigh

ACKNOWLEDG EMENTS

EJMG acknowledges the Pew Charitable Foundation for its sup-port of thiswork This article originated at a 2013workshop co-organized by NOAA-Fisheries and IUCN-CEEM-FEG entitledldquoMultidisciplinaryWorkshoptoAddressEcosystem-LevelImpactsofFisheriesBycatchonMarineMegafaunaBiodiversityConservationthrough Mitigation Policy Economic Instruments and TechnicalChangerdquo We thank the reviewers for their insightful commentswhichmuchimprovedthemanuscript

ORCID

E J Milner-Gulland httporcidorg0000-0003-0324-2710

R E FE R E N C E S

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Alfaro-Shigueto JMangel JCBernedoFDuttonPHSeminoffJAampGodleyB J (2011) Small-scale fisheriesofPeruAmajorsinkformarineturtles inthePacificJournal of Applied Ecology481432ndash1440httpsdoiorg101111j1365-2664201102040x

Alfaro-ShiguetoJMangelJCPajueloMDuttonPHSeminoffJ A amp Godley B J (2010) Where small can have a large im-pact Structure and characterization of small-scale fisheries inPeru Fisheries Research 106 8ndash17 httpsdoiorg101016jfishres201006004

Andraka SMugM HallM PonsM Pacheco L ParralesM hellipOrtega D (2013) Circle hooks Developing better fishing prac-ticesintheartisanallonglinefisheriesoftheEasternPacificOceanBiological Conservation 160 214ndash224 httpsdoiorg101016jbiocon201301019

ApostolopoulouEampAdamsWM(2017)BiodiversityoffsettingandconservationReframingnaturetosaveitOryx5123ndash31httpsdoiorg101017S0030605315000782

BaacuteezJCRealRGarciacutea-SotoCJoseacuteMMaciacuteasDampCamintildeasJA(2007)Loggerheadturtleby-catchdependsondistancetothecoastindependentoffishingeffortImplicationsforconservationandfish-eries management Marine Ecology Progress Series 338 249ndash256httpsdoiorg101017S0030605315000782

BBOP (2012) Standard on biodiversity offsets Business and biodiversity offsets programmeWashingtonDCForestTrends

Bishop J (2006) Standardizing fishery-dependent catch and ef-fort data in complex fisheries with technology change Reviews in Fish Biology and Fisheries 16 21ndash38 httpsdoiorg101007s11160-006-0004-9

BoyceJ(1996)AneconomicanalysisofthefisheriesbycatchproblemJournal of Environmental Economics and Management31 314ndash336httpsdoiorg101006jeem19960047

BugoniLManciniPLMonteiroDSNascimentoLampNevesTS(2008)SeabirdbycatchintheBrazilianpelagiclonglinefisheryandareviewofcaptureratesinthesouthwesternAtlanticOceanEndangered Species Research5137ndash147httpsdoiorg103354esr00115

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BullJWampBrownlieS(2017)Thetransitionfromnonetlosstoanetgainof biodiversity is far from trivialOryx51 53ndash59 httpsdoiorg101017S0030605315000861

BullJWBryantCBakerJampMilner-GullandEJ(2015December28)Developing measuring and communicating the outcomes of cor-porate biodiversity strategies [pdfdocument]RetrievedfromhttpwwwwildbusinessorgBull_etal_2015_WBLpdf

BullJWGordonAWatsonJEampMaronM(2016)Seekingcon-vergenceonthekeyconceptsinlsquononetlossrsquopolicyJournal of Applied Ecology531686ndash1693httpsdoiorg1011111365-266412726

BullJWHardyMJMoilanenAampGordonA (2015)Categoriesof flexibility in biodiversity offsetting and their implications forconservation Biological Conservation 192 522ndash532 httpsdoiorg101016jbiocon201508003

Bull JW Lloyd S P amp StrangeN (2017) Implementation gap be-tween the theory and practice of biodiversity offset multipliersConservation Lettershttpsdoiorg101111conl12335

Bull JW SuttleKBGordonA SinghN JampMilner-Gulland EJ(2013)BiodiversityoffsetsintheoryandpracticeOryx47369ndash380httpsdoiorg101017S003060531200172X

CampbellLMampCornwellML(2008)Humandimensionsofbycatchreduction technology Current assumptions and directions for fu-tureresearchEndangered Species Research5325ndash334httpsdoiorg103354esr00172

Caswell H Brault S Read A J amp Smith T D (1998) Harborporpoise and fisheries An uncertainty analysis of inciden-tal mortality Ecological Applications 8 1226ndash1238 httpsdoiorg1018901051-0761(1998)008[1226hpafau]20co2

ClementsTJohnANielsenKAnDTanSampMilner-GullandEJ (2010)Payments forbiodiversityconservation in thecontextofweak institutions Comparison of three programs from CambodiaEcological Economics 69 1283ndash1291 httpsdoiorg101016jecolecon200911010

CoxTLewisonRŽydelisRCrowderLSafinaCampReadA(2007)ComparingeffectivenessofexperimentalandimplementedbycatchreductionmeasuresTheidealandtherealConservation Biology211155ndash1164httpsdoiorg101111j1523-1739200700772x

CrollDADewarHDulvyNKFernandoDFrancisMPGalvaacuten-Magantildea F hellip Newton K M (2016) Vulnerabilities and fisher-ies impactsTheuncertain futureofmanta anddevil raysAquatic Conservation Marine and Freshwater Ecosystems 26 562ndash575httpsdoiorg101002aqc2591

Damalas D amp Vassilopoulou V (2013) Slack regulation com-pliance in the Mediterranean fisheries A paradigm from theGreek Aegean Sea demersal trawl fishery modelling discardogives Fisheries Management and Ecology 20 21ndash33 httpsdoiorg101111j1365-2400201200860x

DuttonDLDuttonPHChaloupkaMampBoulonRH(2005)IncreaseofaCaribbeanleatherbackturtleDermochelys coriaceanestingpop-ulation linked to long-termnestprotectionBiological Conservation126186ndash194httpsdoiorg101016jbiocon200505013

DuttonPJosephJSquiresDampWilliamsM(2011)Bellagioblue-print foractiononseaturtlesChapter2 InPDuttonDSquiresampM Ahmed (Eds) Conservation of pacific sea turtles (pp 15ndash36)HonoluluHIUniversityofHawaiiPress

DuttonPampSquiresD (2008)AholisticstrategyforPacificseatur-tlerecoveryOcean Development and International Law39200ndash222httpsdoiorg10108000908320802013685

FAO (2011 January 5) International guidelines on bycatch manage-ment and reduction of discards Rome Italy Food and AgricultureOrganisation [pdf document] Retrieved from httpwwwfaoorgdocrephelliptba0022t00pdf

Finkelstein M Bakker V Doak D F Sullivan B Lewison RSatterthwaite W H hellip Henry R W (2008) Evaluating the po-tential effectiveness of compensatory mitigation strategies for

marinebycatchPLoS ONE3 e2480httpsdoiorg101371jour-nalpone0002480

FowlerSJ(2016January5)Draft best practice mitigation guidelines for sharks and rays taken in purse- seine and long-line fisheries Convention on Migratory Species[pdfdocument]RetrievedfromhttpwwwcmsintsitesdefaultfilesdocumentCMS_Sharks_CWG1_Doc_3_2pdf

FrancisMP(2014)Survival and depth distribution of spinetail devilrays (Mobula japanica) released from purse-seine catches NIWA ClientReportNoWLG2014-2WellingtonNewZealandDepartmentofConservation

Fulton E A Smith A D Smith D C amp van Putten I E (2011)Human behaviour The key source of uncertainty in fish-eries management Fish and Fisheries 12 2ndash17 httpsdoiorg101111j1467-2979201000371x

GardnerTAHaseABrownlieSEkstromJMPilgrimJDSavyCEhellipTenKateK(2013)BiodiversityoffsetsandthechallengeofachievingnonetlossConservation Biology271254ndash1264httpsdoiorg101111cobi12118

GjertsenHHallMampSquiresD(2010)IncentivestoaddressbycatchInRAllenJJosephampDSquires(Eds)Conservation and manage-ment of transnational tuna fisheries (pp225ndash250)Ames IAWiley-Blackwellhttpsdoiorg1010029780813820262ch14

Gjertsen H Squires D Dutton P amp Eguchi T (2014) Cost-effectivenessofalternativeconservationstrategieswithapplicationtothePacificLeatherbackTurtleConservation Biology28140ndash149httpsdoiorg101111cobi12239

GodinACCarlson JKampBurgenerV (2012)Theeffectofcirclehooks on shark catchability and at-vessel mortality rates in long-lines fisheriesBulletin of Marine Science88 469ndash483 httpsdoiorg105343bms20111054

GrimmDBarkhornIFestaDBonzonKBoomhowerJHovlandV amp Blau J (2012) Assessing catch sharesrsquo effects evidencefrom Federal United States and associated British Columbianfisheries Marine Policy 36 644ndash657 httpsdoiorg101016jmarpol201110014

HallMA(1996)OnbycatchesReviews in Fish Biology and Fisheries6319ndash352httpsdoiorg101007BF00122585

HallMAAlversonDLampMetuzalsKI(2000)By-catchProblemsand solutions Marine Pollution Bulletin 41 204ndash219 httpsdoiorg101016S0025-326X(00)00111-9

HallMANakanoHClarke S Thomas SMolloy J PeckhamSHhellipHallSJ (2007)Workingwithfisherstoreduceby-catchesIn S J Kenelly (Ed)By-catch reduction in the worldrsquos fisheries (pp235ndash288) Dordrecht The Netherlands Springer httpsdoiorg101007978-1-4020-6078-6_8

HallM amp RomanM (2013)Bycatch and non-tuna catch in the tropi-cal tuna purse seine fisheries of the worldFisheriesandAquacultureTechnicalPaper568RomeItalyFAO

HallMASwimmerYampPargaM(2012)NoldquosilverbulletsrdquobutplentyofoptionsWorkingwiththeeasternpacificartisanalfisherstore-duceseaturtlemortalityinfisheriesInJASeminoffampBWallace(Eds)Sea turtles of the eastern pacific Advances in research and con-servation(pp136ndash153)TucsonAZUniversityofArizonaPress

HamnerRMWadePOremusMStanleyMBrownPConstantineR amp Baker C S (2014) Critically low abundance and limits tohuman-relatedmortalityfortheMauirsquosdolphinEndangered Species Research2687ndash92httpsdoiorg103354esr00621

HatchSA(2003)Statisticalpowerfordetectingtrendswithapplica-tions to seabird monitoringBiological Conservation 111 317ndash329httpsdoiorg101016S0006-3207(02)00301-4

HeppellSSCrowderLBampCrouseDT(1996)Modelstoevaluateheadstartingasamanagementtoolforlong-livedturtlesEcological Applications6556ndash565httpsdoiorg1023072269391

HoughPampRobertsonM(2009)MitigationunderSection404oftheCleanWater ActWhere it comes from what it meansWetlands

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Ecology and Management 17 15ndash33 httpsdoiorg101007s11273-008-9093-7

IATTC(2015)Resolution on the conservation of mobulid rays caught in as-sociation with fisheries in the IATTC convention area Inter-AmericanTropical TunaCommission89thAnnualMeetingResolutionC-15-04LaJollaCAInter-AmericanTropicalTunaCommission

IFC(2012)Performance standard 6 Biodiversity conservation and sustain-able management of natural resources January 1 2012WashingtonDCInternationalFinanceCorporation

Innes J Pascoe S Wilcox C Jennings S amp Paredes S (2015)MitigatingundesirableimpactsinthemarineenvironmentAreviewofmarket-basedmanagementmeasuresFrontiers in Marine Science276httpsdoiorg103389fmars201500076

JanniseCSquiresDSeminoffJampDuttonP (2010)Conservationinvestments andmitigationTheCaliforniadrift gillnet fishery andpacificseaturtles InRQGraftonRHilbornDSquiresMTaitampMJWilliams(Eds)Handbook of marine fisheries conservation and management(pp231ndash240)OxfordUKOxfordUniversityPress

Jones E amp FrancisM (2012)Protected rays ndash Occurrence and devel-opment of mitigation methods in the New Zealand tuna purse seine fishery Auckland New Zealand National Institute of Water andAtmosphericResearch

KormosRKormosCFHumleTLanjouwARainerHVicturineR hellipWilliamson E A (2014) Great apes and biodiversity offsetprojectsinAfricaThecasefornationaloffsetstrategiesPLoS ONE9(11)e111671httpsdoiorg101371journalpone0111671

KotchenMJ (2013)Voluntaryand information-basedapproachestoenvironmentalmanagementApubliceconomicsperspectiveReview of Environmental Economics and Policy 7(2) 276ndash295 httpsdoiorg101093reepret012

Kyriazi Z LejanoRMaes FampDegraer S (2015)Bargaining a netgaincompensationagreementbetweenamarinerenewableenergydeveloperandamarineprotectedareamanagerMarine Policy6040ndash48httpsdoiorg101016jmarpol201506005

LentRampSquiresD(2017)ReducingmarinemammalbycatchinglobalfisheriesAneconomicsapproachDeep Sea Research Part II Topical Studies in Oceanography 140 268ndash277 httpsdoiorg101016jdsr2201703005

Lewison R L Crowder L B Read A J amp Freeman S A (2004)Understanding impactsof fisheriesbycatchonmarinemegafaunaTrends in Ecology amp Evolution19598ndash604httpsdoiorg101016jtree200409004

MannC (2015)StrategiesforsustainablepolicydesignConstructiveassessmentofbiodiversityoffsetsandbankingEcosystem Services16266ndash274httpsdoiorg101016jecoser201507001

Marine Stewardship Council (2014 June 21) MSC fisheries certifica-tion requirements v20 [pdf doc] httpswwwmscorgdocumentsscheme-documentsfisheries-certification-scheme-documentsfisheries-certification-requirements-version-20

MaronM IvesCDKujalaHBullJWMaseykFJBekessyShellip Possingham H P (2016) Taming a wicked problem Resolvingcontroversies inbiodiversityoffsettingBioScience66(6)489ndash498httpsdoiorg101093bioscibiw038

MaxwellSLMilner-GullandEJJonesJPKnightATBunnefeldNNunoAhellipRhodesJR(2015)BeingsmartaboutSMARTenvi-ronmentaltargetsScience3471075ndash1076httpsdoiorg101126scienceaaa1451

Moilanen A Van Teeffelen A J Ben-Haim Y amp Ferrier S (2009)Howmuch compensation is enoughA framework for incorporat-inguncertaintyandtimediscountingwhencalculatingoffsetratiosfor impactedhabitatRestoration Ecology17 470ndash478 httpsdoiorg101111j1526-100X200800382x

MorarNToadvineTampBohannanBJ(2015)Biodiversityattwenty-fiveyearsRevolutionorredherringEthics Policy amp Environment1816ndash29httpsdoiorg1010802155008520151018380

OrphanidesCDampPalkaDL(2013)Analysisofharborporpoisegill-netbycatchcomplianceandenforcement trends in theUSnorth-western Atlantic January 1999 to May 2010 Endangered Species Research20251ndash269httpsdoiorg103354esr00499

Pascoe S Innes J Holland D Finas M Theacutebaud O TownsendR hellip Hutton T (2010) Use of incentive-based managementsystems to limit bycatch and discarding International Review of Environmental and Resource Economics 4 123ndash161 httpsdoiorg10156110100000032

PhalanBHayesG Brooks SMarshDHoward PCostelloeBhellip Whitaker S (2017) Avoiding impacts on biodiversity throughstrengthening the first stage of the mitigation hierarchy Oryxhttpsdoiorg101017S0030605316001034

Queacutetier F Regnery B amp Levrel H (2014) No net loss of biodiver-sity or paper offsets A critical review of the French no net losspolicy Environmental Science amp Policy 38 120ndash131 httpsdoiorg101016jenvsci201311009

RadzioTASmolinskyJAampRoosenburgWM(2013)Lowuseofre-quiredterrapinbycatchreductiondevicesinarecreationalcrabpotfisheryHerpetological Conservation and Biology8222ndash227

RaineyHJPollardEHBDutsonGEkstromJMLivingstoneSRTempleHJampPilgrimJD(2015)AreviewofcorporategoalsofnonetlossandnetpositiveimpactonbiodiversityOryx49232ndash238httpsdoiorg101017S0030605313001476

Rausser G C Hamilton S F Kovach M amp Stifter R (2009)UnintendedconsequencesThe spillovereffectsof commonprop-ertyregulationsMarine Policy3324ndash39httpsdoiorg101016jmarpol200803020

Rice J (2014) Evolution of international commitments for fisheriessustainability ICES Journal of Marine Science Journal du Conseil71157ndash165httpsdoiorg101093icesjmsfst078

RichardYampAbrahamER(2013)ApplicationofPotentialBiologicalRemoval methods to seabird populations New Zealand AquaticEnvironmentandBiodiversityReport108

RodeJGoacutemez-BaggethunEampKrauseT(2015)Motivationcrowd-ingbyeconomic incentives inconservationpolicyAreviewoftheempiricalevidenceEcological Economics117270ndash282httpsdoiorg101016jecolecon201411019

RogersAA(2013)SocialwelfareandmarinereservesIswillingnesstopayforconservationdependentonmanagementprocessAdiscretechoiceexperimentoftheNingalooMarineParkinAustraliaCanadian Journal of Agricultural EconomicsRevue Canadienne Drsquoagroeconomie61217ndash238httpsdoiorg101111cjag12008

Rosenberg A A amp McLeod K L (2005) Implementing ecosystem-basedapproachestomanagementfortheconservationofecosystemservicesMarine Ecology Progress Series300 270ndash274 httpsdoiorg103354meps300270

Segerson K (2010) Can voluntary programs reduce sea turtle by-catch Insights from the literature in environmental economics InRQGraftonRHilbornDSquiresMTaitampMJWilliams(Eds)Handbook of marine fisheries conservation and management(pp618ndash629)OxfordUKOxfordUniversityPress

Serafy JECookeS JDiazGAGraves JEHallMShivjiMampSwimmerY(2012)CirclehooksincommercialrecreationalandartisanalfisheriesResearchstatusandneedsforimprovedconser-vation and management Bulletin of Marine Science 88 371ndash391httpsdoiorg105343bms20121038

ShiodeDHu F ShigaM Yokota K amp Tokai T (2005)Midwaterfloatsystemforstandardizinghookdepthsontunalonglinestore-duce sea turtleby-catchFisheries Science71 1182ndash1184httpsdoiorg101111j1444-2906200501080x

Sims M Cox T amp Lewison R (2008) Modeling spatial patternsin fisheries bycatch Improving bycatch maps to aid fisheriesmanagement Ecological Applications 18 649ndash661 httpsdoiorg10189007-06851

emspensp emsp | emsp15MILNER- GULLAND Et AL

Squires D amp Garcia SM (2014) Ecosystem-level impacts of fisheries bycatch on marine megafauna Biodiversity conservation through miti-gation policy economic instruments and technical changeReportofthe IUCN-CEM-FEGScientificworkshopGland Switzerland 7ndash10October2013GlandSwitzerlandIUCN

SquiresDampGarciaSM(inpress)Fisheries bycatch in marine ecosys-tems Policy economic instruments and technical change ChichesterUKJWileyampSons

SwimmerYArauzRMcCrackenMMcNaughtonLBallesteroJMusylMhellipBrillR(2006)DivingbehavioranddelayedmortalityofoliveridleyseaturtlesLepidochelys olivaceaaftertheirreleasefromlongline fishing gearMarine Ecology Progress Series323 253ndash261httpsdoiorg103354meps323253

TolottiMTFilmalterJDBachPTravassosPSeretBampDagornL(2015)BanningisnotenoughThecomplexitiesofoceanicsharkmanagementbytunaregional fisheriesmanagementorganizationsGlobal Ecology and Conservation 4 1ndash7 httpsdoiorg101016jgecco201505003

Tuck G N Polacheck T amp Bulman C M (2003) Spatio-temporaltrendsoflonglinefishingeffortintheSouthernOceanandimplica-tionsforseabirdbycatchBiological Conservation1141ndash27httpsdoiorg101016S0006-3207(02)00378-6

UNEP-WCMC(2016)Marine no net loss A feasibility assessment of imple-menting no net loss of biodiversity in the seaCambridgeUKUnitedNationsEnvironmentProgramme

Vaissiegravere A-C Levrel H Pioch S amp Carlier A (2014) Biodiversityoffsets for offshore wind farm projects The current situation inEurope Marine Policy 48 172ndash183 httpsdoiorg101016jmarpol201403023

Wallace B P Heppell S S Lewison R L Kelez S amp CrowderL B (2008) Impacts of fisheries bycatch on loggerhead tur-tles worldwide inferred from reproductive value analy-ses Journal of Applied Ecology 45 1076ndash1085 httpsdoiorg101111j1365-2664200801507x

Wanless R M Ryan P G Altwegg R Angel A Cooper JCuthbert R amp Hilton G M (2009) From both sides Dire de-mographic consequences of carnivorous mice and longlining for

the critically endangered Tristan albatrosses on Gough IslandBiological Conservation 142 1710ndash1718 httpsdoiorg101016jbiocon200903008

WardP LawrenceEDarbyshireRampHindmarshS (2008) Large-scale experiment shows that nylon leaders reduce shark bycatchandbenefitpelagiclonglinefishersFisheries Research90100ndash108httpsdoiorg101016jfishres200709034

WardTampPhillipsB(2010)SeafoodecolabelingInRQGraftonRHilbornDSquiresMTaitampMJWilliams(Eds)Handbook of ma-rine fisheries conservation and management (pp 608ndash617) OxfordUKOxfordUniversityPress

WilcoxCampDonlanCJ (2007)Compensatorymitigationasasolu-tion to fisheries bycatch-biodiversity conservation conflictsFrontiers in Ecology and the Environment 5 325ndash331 httpsdoiorg1018901540-9295(2007)5[325cmaast]20co2

WilcoxCampDonlanCJ (2009)NeedforaclearandfairevaluationofbiodiversityoffsetsforfisheriesbycatchConservation Biology23770ndash772httpsdoiorg101111j1523-1739200901173x

Wolf SHartlBCarrollCNeelMCampGreenwaldDN (2015)Beyond PVAWhy recovery under the Endangered Species Act ismorethanpopulationviabilityBioScience65200ndash207httpsdoiorg101093bioscibiu218

ZedlerJBampCallawayJC (1999)TrackingwetlandrestorationDomitigation sites follow desired trajectories Restoration Ecology 769ndash73httpsdoiorg101046j1526-100X199907108x

Žydelis R Wallace B P Gilman E L amp Werner T B (2009)Conservation of marine megafauna through minimization of fish-eries bycatch Conservation Biology 23 608ndash616 httpsdoiorg101111j1523-1739200901172x

How to cite this articleMilner-GullandEJGarciaSArlidgeW etalTranslatingtheterrestrialmitigationhierarchytomarinemegafaunaby-catchFish Fish 2018001ndash15 httpsdoiorg101111faf12273

Page 9: Translating the terrestrial mitigation hierarchy to marine ......of marine megafauna by-catch in fisheries, going from defining an overarching goal with an associated quantitative

emspensp emsp | emsp9MILNER- GULLAND Et AL

by-catch at the national or international levels (eg FAO 2011Rice 2014) the availability and quality of technical fixes associ-atedcosts tofishers limitsonaccesstoseafoodmarketsaswellassocietalpressuresHowevermuchresearchonby-catchreduc-tion focuses on identifying and implementing technicalmeasuresto reduceBPUE rather thanon the social andeconomicbarriersto implementation (Campbell amp Cornwell 2008) Technologicalinnovation to improve BPUE needs to be appropriately incentiv-izedwitheffortsmadetoensurethatsuchmeasuresareascost-effective as possible for fishers (Gjertsen Hall amp Squires 2010Lent amp Squires 2017) However it often happens that even ap-parently suitable by-catchmeasures are notwidely implemented(eg Damalas amp Vassilopoulou 2013 Orphanides amp Palka 2013RadzioSmolinskyampRoosenburg2013)Inthesecasesthedegreeofnon-implementationandthereasonsbehinditneedstobeun-derstoodsoitcanbeaddressed(Coxetal2007)Thesetypesofconsiderationarealsonotwellresearchedintheterrestrialoffset-tingliteraturebecausecomplianceispoorlymonitored(BullSuttleGordonSinghampMilner-Gulland2013)andthereislittlesupportfor researchon thebarriers to implementationofamitigationhi-erarchyandhowtosupportdeveloperstoaddressthesebarriers(BullBryantBakerampMilner-Gulland2015)Thesocialimpactsofimplementingabiodiversitymitigationhierarchyonresourceusersarementioned inguidance (egBBOP2012)buthowtomeasureandaccountforthemisverypoorlyunderstoodThefewstudiesin-vestigatingdeliveryofpromisedoffsetmeasuresinterrestrialsys-temssuggestaverypoorrecord(QueacutetierRegneryampLevrel2014)Therefore the social side of implementing the mitigation hierar-chyand incentivizingcompliance isanarea thatneedsmore andmoreactiveresearchwithinboththeterrestrialandmarinerealms(FultonSmithSmithampvanPutten2011)Thisisparticularlytruewhentheburdenof implementingmitigationapproaches isbornebyrelativelysmall-scaleproducersratherthangovernmentsormul-tinationals(egthepelagiclonglinefisheriesinTable3)

45emsp|emspSocietal limits

Foraspeciesathighriskofextinctioncompleteavoidanceofby-catchmightbethemostdesirablepolicyfrombothamanagementagency and societal perspective In addition with emblematic orhighlythreatenedmarinemegafaunaitmaybeviewedbymembersof the public asmorallywrong to kill any individuals even ifmiti-gationisinplace(egMauirsquosdolphinHamneretal2014) leadingtopressureongovernmentstoreflectthisethicalconcerninregu-lationsThesedilemmasecho the issueof thresholds in terrestrialoffsetswhichrecognizesthattherearesomecriticalareasinwhichdevelopmentisnotsocietallyappropriateregardlessofthepoten-tialformitigationandotherareasinwhichthemitigationhierarchycan be appropriately applied (Bull etal 2013) Examples of loca-tionswhereathresholdapproach isseenasappropriate interres-trial systems include the habitat of highly endangered species orecosystemswhich are limited in extent and irreplaceable (such asoldgrowthforest) In terrestrialsystems therefore themitigation

hierarchyisseenasmostappropriateforapplicationinmorecom-monanddegradedhabitatssuchasfarmlandSimilarlyinfisheriestheremaybesomesituationsinwhichthestockssubjecttoby-catchare so precious or threatened that no level of threat from fishingcanbecontemplatedandotherswherefishingsubjecttoNNLandthemitigationhierarchyisasociallyacceptableapproachInsitua-tions inwhich trade-offs between conservation and developmentareseenasnecessaryoracceptablebywidersocietyasociallicencetooperatemaybegainedthroughadoptingoffsetsintheabsenceofregulationForexampleinsub-SaharanAfricaseverallargedevel-opmentprojectsareattemptingtooffsettheirimpactsongreatapesandtheirhabitats(Kormosetal2014)Aby-catchequivalentmightbe fishing companies voluntarily donating funds for turtle nestingbeachrestorationintheirareaofoperationinadditiontocomply-ingwithregulatoryby-catchmitigationmeasuresThesemeasuresmayimprovetheimageofthecompanywiththegeneralpublicbuttoavoidaccusationsofldquogreenwashingrdquotheireffectivenessneedstobeproperlyscrutinized(Bulletal2016)Transparentlyembeddingthesetypesofactionswithinamitigationhierarchysuchasweareproposing and critically evaluating their contribution to increasingthepopulationgrowthrate(asperEquation1)wouldbeonewaytopromptsuchscrutiny

46emsp|emspUncertainty

The nature of the uncertainties surrounding biology and enforce-ment in themarine setting raisesquestions about theorderingofsteps in themitigationhierarchy inaway that isdissimilar to ter-restrialsystemswherethehierarchyofuncertaintiesmaybecleareranduncertaintyisgenerallylowerForexampleitmaybethattheimpactonoverallpopulationgrowthrateofanoffsetmeasurelikeeradicating invasivespecies fromaseabirdnestinghabitat isbothless uncertain and more cost-effective than avoidance measuressuchasclosingareaswhichmayormaynotbefrequentedbyadultseabirds in a given time-periodGenerally though itmightbe as-sumedthatmeasureswhichtargetlifestagessubjecttohighlevelsofnaturalmortalityorwithinwhichindividualcontributiontoover-allpopulationgrowthrateislow(egheadstartingjuvenileturtles)maybelesseffectiveinachievingNNLthanmeasureswhichtargetreproductivelymatureadultfemales(suchaslivereleasesHeppellCrowderampCrouse1996)Howeverbeforeimplementinganoffsetthataimstoimprovethesurvivalofonelifestageinordertocom-pensatefortheby-catchmortalityofanotherarobustassessmentoftheconsequences(withassociateduncertainties)shouldbecar-ried out through detailed population modelling based on strongempiricalstudies(cfWallaceHeppellLewisonKelezampCrowder2008)Interrestrialsystemstherequirementsequentiallytoapplythemitigationhierarchyisbroadlyunchallengedbutactuallysimilararguments apply For example habitat restoration sits above off-settinginthehierarchyandyetitisalong-termuncertainprocesswhichmayinsomecircumstancesbemuchlesspreferabletoanoff-setusingawell-establishedapproachwhichishighlylikelytoleadtoconservationgains

10emsp |emsp emspensp MILNER- GULLAND Et AL

47emsp|emspTemporal considerations

Thetimingofoffsetsinrelationtootherelementsofthemitigationhierarchyhasbeenthesubjectofdebatewithintheterrestriallitera-tureThemainsuggestionforaddressingthetemporarylossofbio-diversitywhileoffsetscometofruitionhasbeenadoptingmitigationbankingwherebyoffsetsareimplementedinadvanceofpotentiallydamagingactivitiesprovidingbiodiversitycreditswhichcanbeusedtocompensateforlaterlossesThisbothremovesanelementofun-certaintyfromtheoffsetimplementationandreducesthetimelagbetweenlossandgain(Mann2015)Withrespecttomarinemega-faunaby-catchflexibilityintimingprovidesadditionalscopeforcostreduction and benefit enhancementwhichmay not be present intraditionalhabitat-basedterrestrialoffsetsForexampletemporarymeasuressuchasashort-termby-catchtaxtofundanoffsetmaybeusedifmitigationoravoidancemethodstaketimetocomeonlineorifatemporarynudgeisenoughtocausebehaviouralchangeThismightbethecaseifapolicywasneededtoinducefisherstotakeupnewgeartoavoidthecostofanoffsetorifconcernsaboutsafetyoryieldreductionsduringthetransitiontonewgearcouldbeallayedbyatemporarysubsidyforearlyadoptersorapaidparticipatorymoni-toringprogrammeto informwider implementation(egthemobu-lidandsharkcase-studiesinTable3)Justasforhabitatrestoration(ZedlerampCallaway 1999) by-catchoffset strategieswhich targetjuvenilestagesof long-livedspecies (eg turtleheadstartingor in-vasive removal fromseabirdnesting islands)may takemanyyearsfor their effects to become apparent in an increase in populationgrowthratesAdditionaluncertaintyisintroducedbythedifficultyinmonitoringpopulationsofmanyby-catch species (eg seabirdsHatch2003)leadingtouncertainestimatesoftheimpactofoffsetactivitiesonpopulationgrowth(seecase-studiesinTable3)Theseproblemsarenot insuperablehoweverpositivetrendshavebeenreportedinturtlepopulationsoverdecadesasaresultofnestpro-tection(egDuttonDuttonChaloupkaampBoulon2005)

5emsp |emspUSING INCENTIVES TO REDUCE BY- C ATCH

Manyoftheexamplesandprinciplesdiscussedaboveeitherimplic-itlyorexplicitlyrelatetotheeconomicsocialinstitutionalormoralincentivesoperatingondifferentactorsinsideandoutsidethefish-erywhichcanbepositiveornegativeWenowturntoadiscussionofhowincentivescanbeusedtoreduceby-catchwithinourframe-workIncentivescanbeputinplacetochangefisherbehaviourwithrespecttoanyoftheelementsoftheframework (avoidminimizeremediateandoffsetTable3)Althoughdiscussedintheliteraturemostof these incentive approaches are yet tobe implemented inthe realworldparticularly forby-catchThereforeuntil empiricalevidenceoftheireffectivenessisavailablethesesuggestionscomewithacaveat

Financial costsofby-catchmitigationactions canarise for in-stancefromlostcatchcapitalinvestmentsinnewgearormitigation

equipmentor the lossofaccesstoafisheryCostsmayalsoarisefromthedeploymentofby-catchobserversortrainingintheuseofnewgearThesecostscanbepaidbyfishingcompaniesorindivid-ualsorbygovernmentsNGOsorseafoodconsumersWhetherornotcompensationforcostsincurredbyfishersisseenasappropri-atedependsonwhetherby-catchreductionisseenasasocialgoodthatfishersareproviding(inwhichcasetheyshouldbecompensatedforit)orasputtingrighttheharmthattheyaredoingtobiodiver-sitywhilegeneratingtheirownprivategain(ineconomiclanguagewhetherby-catchisviewedasanunpricedexternalityinwhichcasetheyshouldpay)Italsodependsonwhethereconomichardshipwillensueacaseforcompensationofby-catchreductioncostsincurredbypeopledependenton fishing for their livelihoodsmaybemoresympatheticallyreceivedbyotheractorsthanacasemadebyalargemultinationalfishingcompany

Ifby-catchisseenasanunpricedexternalityitmightbesociallyoptimaltotaxfishersfortheirby-catchsothatthisexternalityisin-ternalizedThisplacesanexplicitpriceuponby-catch(Boyce1996Pascoeetal2010SquiresampGarcia2014)Theby-catchprice islikely to be incorporated into the price of the target species andtherebybecomespartofthetargetspeciescostThispricecouldbeset differently for different demographic classesof theby-caughtspecies depending on the impact the loss of an individualwouldhaveonthepopulationAllelsebeingequalputtingapriceonby-catchmeans that theseafoodproduct that is the targetcatchbe-comesmoreexpensiveandconsumershave topaymore for theirseafoodreducingdemandTheninprincipleeveryfirminthesup-plychaineveryvesselandeveryconsumerhaveanincentivetore-duceby-catchuntileacheconomicactorrsquosmarginalcostofby-catchreductionequals thecommonpriceofby-catch that theyall faceOffsetsareonewaytopriceandinternalizetheby-catchexternalitycostIfanoffsettingactioniscostlytoimplementandmustbepaidforwith each unit of by-catch it implicitly prices the residual by-catch In this circumstance the effect from a financial standpointisthesameasaby-catchtaxwiththe levelsetbasedonthecostoftheoffsetVariousinstitutionalstructurestosupportthischargeperunitofby-catcharepossiblewithdifferentimplicationsintermsofthedistributionofcostsandbenefitsForexampleaninsuranceschemecouldbepaidintobyfishersthatpaysoutintheeventofaby-catcheventtherebyspreadingthecostofunavoidablerareby-catcheventsOratradablepermitschemecouldoperatesuchthatfisherswhoexperienceaby-catcheventcanbuyapermitwiththecostvaryingdependingondemandforpermits (henceprovidingavessel-levelincentivetoinnovatetoreduceby-catch)

If there isdemandforconservation inan internationalmarketthen price premiums and market access (through eco-labellingsupply chain certification other food sustainability campaignsWardampPhillips2010)orboycottsactingasstrategicthreatsfromconsumers (Kotchen 2013 Segerson 2010) could act as positiveornegativeeconomic leversonthe fisheryprovidingan incentivefor fishers to reduce their by-catch voluntarily (as has been sug-gested for the Brazilianmahi-mahi fishery Table3) For exampletheMarine StewardshipCouncil now includesby-catchmitigation

emspensp emsp | emsp11MILNER- GULLAND Et AL

intheircertificationprocess(MSC2014)Demand-ledleversmaybemoreorlessapplicableatdifferentlevelsinthehierarchyforexam-pleavoidancemayberelativelyhardtoevidencewhileoffsettingmaybelesseasytoselltoaconsumerthanminimizationorreme-diationConcerns about the unintended consequences of positiveincentives (particularlyfordirectsubsidiesratherthanconditionalincentives)maydeterminewhethertheyareanappropriateinstru-mentinagivencaseForexampletheymaybeinappropriateifthereisariskthattheadditionalmoneyisreinvestedinincreasedfishingcapacityor iftheremaybeconsumptionproductionorconserva-tionleakages(transferoftheproblemsomewhereelse)whetheratthe vessel fishery or trans-national levelHigh transactions costsmayalsolimitthebenefitsofincentivesschemes

Otherchangeswhichmayneedtobeincentivizedforsuccessfulimplementationofby-catchreductionpoliciesmaybelessamenabletofinancialmeasuresatleastpartlybecauseitislessclearhowtoassign financial value to theactionsor to thebenefits and losseswhichtheyproduceForexampleperceivedreductionsinsafetyforfishingcrews(fromweightedlonglinesfor instance)arecoststhatmaybehardtovaluefinanciallyOtherprerequisitesfor long-termsustainable behaviour change such as changes in social norms sothatfishingcommunitiesseeby-catchreductionasappropriatebe-haviourortechnicalskillacquisitionsothattheycanusenewmeth-odsmaybeincentivizedbycarefullydesignedinterventionsworkingwithfishers(Halletal2007)Conservationpoliciesbasedoneco-nomic incentives (extrinsicmotivation) are not always superior tothosebasedupon intrinsicmotivation Infact incentive-basedby-catch reduction policy instruments could even be counterproduc-tivebyreducingtheeffectivenessofintrinsicmotivationdependingupon the situation (although the empirical evidence on this topicisweak RodeGoacutemez-BaggethunampKrause 2015) If the changerequiredforby-catchreductiontoworkmeetscultural resistancethenparticipatory researchmightbeespeciallyeffective inbreak-ingdownbarriersbetweenthosewhowantby-catchreductiontotakeplaceandthosewhoactuallyhavetoimplementit(thefishers)ForexampleinAustraliathegovernment-fundedbodyOceanwatchfacilitatesengagementbetweencommunities thefishing industryseafood suppliers and government to improve knowledge sharing(wwwoceanwatchorgau)Innovationiscrucialinfisheriesandfish-ersareaccustomedtoadoptingnewtechnologyorprocessespo-tentiallymakingan incentivizedparticipatory researchprogrammeespeciallyfruitful

Sometimes the most efficient way to solve problems is a so-cial instrumentoran institutionalchange inplaceoforaswellasan economic instrument For example supporting developmentof fisherorganizations rather than instituting a vessel-level taxorsubsidy might provide the impetus needed to change behaviourInstitutingcatchshares(individualtransferablequotas)mayprovideanenablingenvironmentforby-catchreductionforexamplebypro-motingmoreeffectivemonitoring(Grimmetal2012)Experiencein terrestrial system produces similar insights incentive-basedschemeswhichalsobuildcommunitycohesionandsupportthede-velopment or strengthening of localmanagement institutions are

more effective in the longer run than direct economic incentives(Clementsetal2010)

6emsp |emspCONCLUSIONS

The framework we present here is novel It draws upon and ex-tends the frameworks for conceptualizing by-catch developed byHall (1996) and Hall Alverson andMetuzals (2000) It amalgam-atesHallrsquos frameworkwith themitigationhierarchyasused in theEnvironmental Impact Assessment literature (BBOP 2012) Thesuggestions about goals metric andmitigation actions are drawnfromtheempiricalby-catchliteratureandtheissueswediscussin-tegratetheconcernsoftheextensiveterrestrialandnascentmarineoffsetting literature with the by-catch literature The frameworkmakesclear thatanearlycrucial step is toclarify thegoalofanyby-catch reduction policyOverarching goals like those issued bytheConventiononBiologicalDiversity(egAichiTarget11that10ofmarinehabitatshouldbeunderprotectionby2020)needtobetranslatedintooperationaltermswithineachfisheryCurrentlyleg-islatedoragreedby-catch reductiongoals tend tobe less specificthantheycouldbeandthisleadstoproblemsininterpretingthesegoals inordertoplanaby-catchmitigationstrategy(seethecase-studies inTable3 for examples) This ambiguity is tobe expectedwithinnegotiatedtargetsbutitisachallengenonetheless(Maxwelletal2015)Usingacommonunitofby-catch impactsuchastheΔλTwhichweuseherewouldbehelpfulbothinclarifyingexpecta-tionsandevaluatingtheeffectivenessofelementsofthemitigationhierarchy

Once the by-catch goal is known options for implementingavoidanceminimizationremediationandoffsetscanbeclarified(asinTable2)Howeveroutsideof the interconnectedbiologyof theecosystemby-catch isembeddedwithinsocialandeconomicsys-temsDifferentunitsofanalysismaybeneededatdifferent levelsofthehierarchytocopewiththechallengesofincompleteoverlapbetween jurisdictional units fisheries target stocks and by-catchstocksJurisdictionalissuesareimportantandcomplexpotentiallyimpeding implementationFleets interact raisingtheriskofpolicyleakageforexampleifpeopleshifttootherfisheriesgearorliveli-hoodsThereforethescaleatwhicheachelementofthemitigationhierarchyisimplementedislikelytovarywithincentivestomitigateoftenbeingbest appliedat thevessel level focussedon reducingindividualmortalitywhileoffsettingisimplementedatthescaleoftheby-catchspeciesrsquostockWithtransboundaryspeciesunilateralconservationinonejurisdictioncreatesthepotentialforproductiontrade and conservation leakages For example a conserving Statecouldimplementtheavoidancestepandshutdownordramaticallycurtailitsownproductionofswordfishtoreduceseaturtleby-catchbuttheknock-oneffectmaybemoreimportationofswordfishfromfleetswithhigherseaturtleby-catch(RausserHamiltonKovachampStifter2009)

Translatingtheframeworkfromaspeciestoanecosystemlevelwill require consideration of the potential interactions between

12emsp |emsp emspensp MILNER- GULLAND Et AL

by-catchmitigationapproachestargetedatdifferentspecies(Serafyetal 2012) Actions to mitigate by-catch for one group of spe-cies can increase or decrease it for others and so a system-wideapproach isneededForexample changing fromJ-hooks tocirclehookstoreducemortalityofturtlesmaydecreaseorincreasesharkmortality(Andrakaetal2013GodinCarlsonampBurgener2012)In terrestrial systems similar interactions arise and value judge-mentsaremade(whetherexplicitlyorimplicitly)astowhatlossandgain of ldquobiodiversityrdquo translates to in operational terms andwhatelementsofbiodiversitymattermosttoimplementers

Uncertainty is high in ocean ecosystems creating both chal-lengesandopportunitiesinapplyingtheconceptofNNLthroughamitigationhierarchythatincludesoffsettingInparticularformarinemegafaunathereishighuncertaintyintheprocesseslinkinganyel-ementofthemitigationhierarchythroughtochangesinpopulationgrowthrateFurthermore impactscanbelong-termhardtomea-sureandspatiallydiffuseanduncertaintyisnotpredictablyspreadthroughthehierarchyThiscreatesadifferentsetofchallengestothosefacedinterrestrialsystemswhereatleastforsometypesofenvironmentalimpactthelinksbetweenactionandimpactarerel-ativelydirectandmeasurableanduncertaintygenerally increasesthroughthemitigationhierarchy (fromavoidthroughminimizere-mediatetooffset)

By-catch reduction measures have had significant successesoverthelastdecadesasaresultofsubstantialinvestmentoftimeand funding by researchers management authorities conserva-tionorganizationsandfishers(Coxetal2007)Howeverthissuc-cessisnotuniversalJustasforanyfisheriesmanagementissueapoorregulatoryregimelimitedcomplianceandlackofinforma-tionhampereffortstoreduceby-catchInsomeplaceshighlevelsofby-catch limitedoptions formitigationandweakgovernance(leadingtopoorenforcement)cancombinetomaketheby-catchproblemintractableOurframeworkwillnotsolvetheseproblemsHowever itbrings together the full rangeofapproaches forby-catchmitigationinastructuredandsystematicwaywhichrequiresatargettobeexpressedagainstwhichoutcomescanbeevaluatedByexposingareasofuncertaintyanddatadeficiencyitcouldchal-lengescientistsandmanagerstoobtainthedatarequiredproperlytoevaluate theeffectivenessofmitigationmeasuresThis couldthensupportandencourageclearerdecision-makingandprioriti-zationofactionsOurframeworkdemonstratesthattheprincipleof implementing thegoalofnonet loss throughamitigationhi-erarchy isasapplicable tomarinemegafaunaby-catchas to ter-restrial systems where it is already widely used in challengingdata-poorcircumstances

There isuntappedpotential forcost-effectiveby-catchmitiga-tionwhichcouldberealizedwiththeadoptionofthisframeworkandwithconsiderationofnewapproachestoincentivizingby-catchmitigationwithinthestepsofthehierarchyApplyingittoafewcase-studiesinpracticewilldemonstrateempiricallywhereandhowthepotentialforimprovedeffectivenesscouldbestberealizedExistinglegalframeworksoftenprecludeapproacheswhichimplicitlyorex-plicitly permit by-catch including the use of economic incentives

ornewapproachessuchasoffsetsHoweverinthiscontextofdy-namicuncertaintythedividendsofthinkingmorecreativelyaboutby-catchmitigationcouldbehigh

ACKNOWLEDG EMENTS

EJMG acknowledges the Pew Charitable Foundation for its sup-port of thiswork This article originated at a 2013workshop co-organized by NOAA-Fisheries and IUCN-CEEM-FEG entitledldquoMultidisciplinaryWorkshoptoAddressEcosystem-LevelImpactsofFisheriesBycatchonMarineMegafaunaBiodiversityConservationthrough Mitigation Policy Economic Instruments and TechnicalChangerdquo We thank the reviewers for their insightful commentswhichmuchimprovedthemanuscript

ORCID

E J Milner-Gulland httporcidorg0000-0003-0324-2710

R E FE R E N C E S

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Alfaro-Shigueto JMangel JCBernedoFDuttonPHSeminoffJAampGodleyB J (2011) Small-scale fisheriesofPeruAmajorsinkformarineturtles inthePacificJournal of Applied Ecology481432ndash1440httpsdoiorg101111j1365-2664201102040x

Alfaro-ShiguetoJMangelJCPajueloMDuttonPHSeminoffJ A amp Godley B J (2010) Where small can have a large im-pact Structure and characterization of small-scale fisheries inPeru Fisheries Research 106 8ndash17 httpsdoiorg101016jfishres201006004

Andraka SMugM HallM PonsM Pacheco L ParralesM hellipOrtega D (2013) Circle hooks Developing better fishing prac-ticesintheartisanallonglinefisheriesoftheEasternPacificOceanBiological Conservation 160 214ndash224 httpsdoiorg101016jbiocon201301019

ApostolopoulouEampAdamsWM(2017)BiodiversityoffsettingandconservationReframingnaturetosaveitOryx5123ndash31httpsdoiorg101017S0030605315000782

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BBOP (2012) Standard on biodiversity offsets Business and biodiversity offsets programmeWashingtonDCForestTrends

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BoyceJ(1996)AneconomicanalysisofthefisheriesbycatchproblemJournal of Environmental Economics and Management31 314ndash336httpsdoiorg101006jeem19960047

BugoniLManciniPLMonteiroDSNascimentoLampNevesTS(2008)SeabirdbycatchintheBrazilianpelagiclonglinefisheryandareviewofcaptureratesinthesouthwesternAtlanticOceanEndangered Species Research5137ndash147httpsdoiorg103354esr00115

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BullJWampBrownlieS(2017)Thetransitionfromnonetlosstoanetgainof biodiversity is far from trivialOryx51 53ndash59 httpsdoiorg101017S0030605315000861

BullJWBryantCBakerJampMilner-GullandEJ(2015December28)Developing measuring and communicating the outcomes of cor-porate biodiversity strategies [pdfdocument]RetrievedfromhttpwwwwildbusinessorgBull_etal_2015_WBLpdf

BullJWGordonAWatsonJEampMaronM(2016)Seekingcon-vergenceonthekeyconceptsinlsquononetlossrsquopolicyJournal of Applied Ecology531686ndash1693httpsdoiorg1011111365-266412726

BullJWHardyMJMoilanenAampGordonA (2015)Categoriesof flexibility in biodiversity offsetting and their implications forconservation Biological Conservation 192 522ndash532 httpsdoiorg101016jbiocon201508003

Bull JW Lloyd S P amp StrangeN (2017) Implementation gap be-tween the theory and practice of biodiversity offset multipliersConservation Lettershttpsdoiorg101111conl12335

Bull JW SuttleKBGordonA SinghN JampMilner-Gulland EJ(2013)BiodiversityoffsetsintheoryandpracticeOryx47369ndash380httpsdoiorg101017S003060531200172X

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Caswell H Brault S Read A J amp Smith T D (1998) Harborporpoise and fisheries An uncertainty analysis of inciden-tal mortality Ecological Applications 8 1226ndash1238 httpsdoiorg1018901051-0761(1998)008[1226hpafau]20co2

ClementsTJohnANielsenKAnDTanSampMilner-GullandEJ (2010)Payments forbiodiversityconservation in thecontextofweak institutions Comparison of three programs from CambodiaEcological Economics 69 1283ndash1291 httpsdoiorg101016jecolecon200911010

CoxTLewisonRŽydelisRCrowderLSafinaCampReadA(2007)ComparingeffectivenessofexperimentalandimplementedbycatchreductionmeasuresTheidealandtherealConservation Biology211155ndash1164httpsdoiorg101111j1523-1739200700772x

CrollDADewarHDulvyNKFernandoDFrancisMPGalvaacuten-Magantildea F hellip Newton K M (2016) Vulnerabilities and fisher-ies impactsTheuncertain futureofmanta anddevil raysAquatic Conservation Marine and Freshwater Ecosystems 26 562ndash575httpsdoiorg101002aqc2591

Damalas D amp Vassilopoulou V (2013) Slack regulation com-pliance in the Mediterranean fisheries A paradigm from theGreek Aegean Sea demersal trawl fishery modelling discardogives Fisheries Management and Ecology 20 21ndash33 httpsdoiorg101111j1365-2400201200860x

DuttonDLDuttonPHChaloupkaMampBoulonRH(2005)IncreaseofaCaribbeanleatherbackturtleDermochelys coriaceanestingpop-ulation linked to long-termnestprotectionBiological Conservation126186ndash194httpsdoiorg101016jbiocon200505013

DuttonPJosephJSquiresDampWilliamsM(2011)Bellagioblue-print foractiononseaturtlesChapter2 InPDuttonDSquiresampM Ahmed (Eds) Conservation of pacific sea turtles (pp 15ndash36)HonoluluHIUniversityofHawaiiPress

DuttonPampSquiresD (2008)AholisticstrategyforPacificseatur-tlerecoveryOcean Development and International Law39200ndash222httpsdoiorg10108000908320802013685

FAO (2011 January 5) International guidelines on bycatch manage-ment and reduction of discards Rome Italy Food and AgricultureOrganisation [pdf document] Retrieved from httpwwwfaoorgdocrephelliptba0022t00pdf

Finkelstein M Bakker V Doak D F Sullivan B Lewison RSatterthwaite W H hellip Henry R W (2008) Evaluating the po-tential effectiveness of compensatory mitigation strategies for

marinebycatchPLoS ONE3 e2480httpsdoiorg101371jour-nalpone0002480

FowlerSJ(2016January5)Draft best practice mitigation guidelines for sharks and rays taken in purse- seine and long-line fisheries Convention on Migratory Species[pdfdocument]RetrievedfromhttpwwwcmsintsitesdefaultfilesdocumentCMS_Sharks_CWG1_Doc_3_2pdf

FrancisMP(2014)Survival and depth distribution of spinetail devilrays (Mobula japanica) released from purse-seine catches NIWA ClientReportNoWLG2014-2WellingtonNewZealandDepartmentofConservation

Fulton E A Smith A D Smith D C amp van Putten I E (2011)Human behaviour The key source of uncertainty in fish-eries management Fish and Fisheries 12 2ndash17 httpsdoiorg101111j1467-2979201000371x

GardnerTAHaseABrownlieSEkstromJMPilgrimJDSavyCEhellipTenKateK(2013)BiodiversityoffsetsandthechallengeofachievingnonetlossConservation Biology271254ndash1264httpsdoiorg101111cobi12118

GjertsenHHallMampSquiresD(2010)IncentivestoaddressbycatchInRAllenJJosephampDSquires(Eds)Conservation and manage-ment of transnational tuna fisheries (pp225ndash250)Ames IAWiley-Blackwellhttpsdoiorg1010029780813820262ch14

Gjertsen H Squires D Dutton P amp Eguchi T (2014) Cost-effectivenessofalternativeconservationstrategieswithapplicationtothePacificLeatherbackTurtleConservation Biology28140ndash149httpsdoiorg101111cobi12239

GodinACCarlson JKampBurgenerV (2012)Theeffectofcirclehooks on shark catchability and at-vessel mortality rates in long-lines fisheriesBulletin of Marine Science88 469ndash483 httpsdoiorg105343bms20111054

GrimmDBarkhornIFestaDBonzonKBoomhowerJHovlandV amp Blau J (2012) Assessing catch sharesrsquo effects evidencefrom Federal United States and associated British Columbianfisheries Marine Policy 36 644ndash657 httpsdoiorg101016jmarpol201110014

HallMA(1996)OnbycatchesReviews in Fish Biology and Fisheries6319ndash352httpsdoiorg101007BF00122585

HallMAAlversonDLampMetuzalsKI(2000)By-catchProblemsand solutions Marine Pollution Bulletin 41 204ndash219 httpsdoiorg101016S0025-326X(00)00111-9

HallMANakanoHClarke S Thomas SMolloy J PeckhamSHhellipHallSJ (2007)Workingwithfisherstoreduceby-catchesIn S J Kenelly (Ed)By-catch reduction in the worldrsquos fisheries (pp235ndash288) Dordrecht The Netherlands Springer httpsdoiorg101007978-1-4020-6078-6_8

HallM amp RomanM (2013)Bycatch and non-tuna catch in the tropi-cal tuna purse seine fisheries of the worldFisheriesandAquacultureTechnicalPaper568RomeItalyFAO

HallMASwimmerYampPargaM(2012)NoldquosilverbulletsrdquobutplentyofoptionsWorkingwiththeeasternpacificartisanalfisherstore-duceseaturtlemortalityinfisheriesInJASeminoffampBWallace(Eds)Sea turtles of the eastern pacific Advances in research and con-servation(pp136ndash153)TucsonAZUniversityofArizonaPress

HamnerRMWadePOremusMStanleyMBrownPConstantineR amp Baker C S (2014) Critically low abundance and limits tohuman-relatedmortalityfortheMauirsquosdolphinEndangered Species Research2687ndash92httpsdoiorg103354esr00621

HatchSA(2003)Statisticalpowerfordetectingtrendswithapplica-tions to seabird monitoringBiological Conservation 111 317ndash329httpsdoiorg101016S0006-3207(02)00301-4

HeppellSSCrowderLBampCrouseDT(1996)Modelstoevaluateheadstartingasamanagementtoolforlong-livedturtlesEcological Applications6556ndash565httpsdoiorg1023072269391

HoughPampRobertsonM(2009)MitigationunderSection404oftheCleanWater ActWhere it comes from what it meansWetlands

14emsp |emsp emspensp MILNER- GULLAND Et AL

Ecology and Management 17 15ndash33 httpsdoiorg101007s11273-008-9093-7

IATTC(2015)Resolution on the conservation of mobulid rays caught in as-sociation with fisheries in the IATTC convention area Inter-AmericanTropical TunaCommission89thAnnualMeetingResolutionC-15-04LaJollaCAInter-AmericanTropicalTunaCommission

IFC(2012)Performance standard 6 Biodiversity conservation and sustain-able management of natural resources January 1 2012WashingtonDCInternationalFinanceCorporation

Innes J Pascoe S Wilcox C Jennings S amp Paredes S (2015)MitigatingundesirableimpactsinthemarineenvironmentAreviewofmarket-basedmanagementmeasuresFrontiers in Marine Science276httpsdoiorg103389fmars201500076

JanniseCSquiresDSeminoffJampDuttonP (2010)Conservationinvestments andmitigationTheCaliforniadrift gillnet fishery andpacificseaturtles InRQGraftonRHilbornDSquiresMTaitampMJWilliams(Eds)Handbook of marine fisheries conservation and management(pp231ndash240)OxfordUKOxfordUniversityPress

Jones E amp FrancisM (2012)Protected rays ndash Occurrence and devel-opment of mitigation methods in the New Zealand tuna purse seine fishery Auckland New Zealand National Institute of Water andAtmosphericResearch

KormosRKormosCFHumleTLanjouwARainerHVicturineR hellipWilliamson E A (2014) Great apes and biodiversity offsetprojectsinAfricaThecasefornationaloffsetstrategiesPLoS ONE9(11)e111671httpsdoiorg101371journalpone0111671

KotchenMJ (2013)Voluntaryand information-basedapproachestoenvironmentalmanagementApubliceconomicsperspectiveReview of Environmental Economics and Policy 7(2) 276ndash295 httpsdoiorg101093reepret012

Kyriazi Z LejanoRMaes FampDegraer S (2015)Bargaining a netgaincompensationagreementbetweenamarinerenewableenergydeveloperandamarineprotectedareamanagerMarine Policy6040ndash48httpsdoiorg101016jmarpol201506005

LentRampSquiresD(2017)ReducingmarinemammalbycatchinglobalfisheriesAneconomicsapproachDeep Sea Research Part II Topical Studies in Oceanography 140 268ndash277 httpsdoiorg101016jdsr2201703005

Lewison R L Crowder L B Read A J amp Freeman S A (2004)Understanding impactsof fisheriesbycatchonmarinemegafaunaTrends in Ecology amp Evolution19598ndash604httpsdoiorg101016jtree200409004

MannC (2015)StrategiesforsustainablepolicydesignConstructiveassessmentofbiodiversityoffsetsandbankingEcosystem Services16266ndash274httpsdoiorg101016jecoser201507001

Marine Stewardship Council (2014 June 21) MSC fisheries certifica-tion requirements v20 [pdf doc] httpswwwmscorgdocumentsscheme-documentsfisheries-certification-scheme-documentsfisheries-certification-requirements-version-20

MaronM IvesCDKujalaHBullJWMaseykFJBekessyShellip Possingham H P (2016) Taming a wicked problem Resolvingcontroversies inbiodiversityoffsettingBioScience66(6)489ndash498httpsdoiorg101093bioscibiw038

MaxwellSLMilner-GullandEJJonesJPKnightATBunnefeldNNunoAhellipRhodesJR(2015)BeingsmartaboutSMARTenvi-ronmentaltargetsScience3471075ndash1076httpsdoiorg101126scienceaaa1451

Moilanen A Van Teeffelen A J Ben-Haim Y amp Ferrier S (2009)Howmuch compensation is enoughA framework for incorporat-inguncertaintyandtimediscountingwhencalculatingoffsetratiosfor impactedhabitatRestoration Ecology17 470ndash478 httpsdoiorg101111j1526-100X200800382x

MorarNToadvineTampBohannanBJ(2015)Biodiversityattwenty-fiveyearsRevolutionorredherringEthics Policy amp Environment1816ndash29httpsdoiorg1010802155008520151018380

OrphanidesCDampPalkaDL(2013)Analysisofharborporpoisegill-netbycatchcomplianceandenforcement trends in theUSnorth-western Atlantic January 1999 to May 2010 Endangered Species Research20251ndash269httpsdoiorg103354esr00499

Pascoe S Innes J Holland D Finas M Theacutebaud O TownsendR hellip Hutton T (2010) Use of incentive-based managementsystems to limit bycatch and discarding International Review of Environmental and Resource Economics 4 123ndash161 httpsdoiorg10156110100000032

PhalanBHayesG Brooks SMarshDHoward PCostelloeBhellip Whitaker S (2017) Avoiding impacts on biodiversity throughstrengthening the first stage of the mitigation hierarchy Oryxhttpsdoiorg101017S0030605316001034

Queacutetier F Regnery B amp Levrel H (2014) No net loss of biodiver-sity or paper offsets A critical review of the French no net losspolicy Environmental Science amp Policy 38 120ndash131 httpsdoiorg101016jenvsci201311009

RadzioTASmolinskyJAampRoosenburgWM(2013)Lowuseofre-quiredterrapinbycatchreductiondevicesinarecreationalcrabpotfisheryHerpetological Conservation and Biology8222ndash227

RaineyHJPollardEHBDutsonGEkstromJMLivingstoneSRTempleHJampPilgrimJD(2015)AreviewofcorporategoalsofnonetlossandnetpositiveimpactonbiodiversityOryx49232ndash238httpsdoiorg101017S0030605313001476

Rausser G C Hamilton S F Kovach M amp Stifter R (2009)UnintendedconsequencesThe spillovereffectsof commonprop-ertyregulationsMarine Policy3324ndash39httpsdoiorg101016jmarpol200803020

Rice J (2014) Evolution of international commitments for fisheriessustainability ICES Journal of Marine Science Journal du Conseil71157ndash165httpsdoiorg101093icesjmsfst078

RichardYampAbrahamER(2013)ApplicationofPotentialBiologicalRemoval methods to seabird populations New Zealand AquaticEnvironmentandBiodiversityReport108

RodeJGoacutemez-BaggethunEampKrauseT(2015)Motivationcrowd-ingbyeconomic incentives inconservationpolicyAreviewoftheempiricalevidenceEcological Economics117270ndash282httpsdoiorg101016jecolecon201411019

RogersAA(2013)SocialwelfareandmarinereservesIswillingnesstopayforconservationdependentonmanagementprocessAdiscretechoiceexperimentoftheNingalooMarineParkinAustraliaCanadian Journal of Agricultural EconomicsRevue Canadienne Drsquoagroeconomie61217ndash238httpsdoiorg101111cjag12008

Rosenberg A A amp McLeod K L (2005) Implementing ecosystem-basedapproachestomanagementfortheconservationofecosystemservicesMarine Ecology Progress Series300 270ndash274 httpsdoiorg103354meps300270

Segerson K (2010) Can voluntary programs reduce sea turtle by-catch Insights from the literature in environmental economics InRQGraftonRHilbornDSquiresMTaitampMJWilliams(Eds)Handbook of marine fisheries conservation and management(pp618ndash629)OxfordUKOxfordUniversityPress

Serafy JECookeS JDiazGAGraves JEHallMShivjiMampSwimmerY(2012)CirclehooksincommercialrecreationalandartisanalfisheriesResearchstatusandneedsforimprovedconser-vation and management Bulletin of Marine Science 88 371ndash391httpsdoiorg105343bms20121038

ShiodeDHu F ShigaM Yokota K amp Tokai T (2005)Midwaterfloatsystemforstandardizinghookdepthsontunalonglinestore-duce sea turtleby-catchFisheries Science71 1182ndash1184httpsdoiorg101111j1444-2906200501080x

Sims M Cox T amp Lewison R (2008) Modeling spatial patternsin fisheries bycatch Improving bycatch maps to aid fisheriesmanagement Ecological Applications 18 649ndash661 httpsdoiorg10189007-06851

emspensp emsp | emsp15MILNER- GULLAND Et AL

Squires D amp Garcia SM (2014) Ecosystem-level impacts of fisheries bycatch on marine megafauna Biodiversity conservation through miti-gation policy economic instruments and technical changeReportofthe IUCN-CEM-FEGScientificworkshopGland Switzerland 7ndash10October2013GlandSwitzerlandIUCN

SquiresDampGarciaSM(inpress)Fisheries bycatch in marine ecosys-tems Policy economic instruments and technical change ChichesterUKJWileyampSons

SwimmerYArauzRMcCrackenMMcNaughtonLBallesteroJMusylMhellipBrillR(2006)DivingbehavioranddelayedmortalityofoliveridleyseaturtlesLepidochelys olivaceaaftertheirreleasefromlongline fishing gearMarine Ecology Progress Series323 253ndash261httpsdoiorg103354meps323253

TolottiMTFilmalterJDBachPTravassosPSeretBampDagornL(2015)BanningisnotenoughThecomplexitiesofoceanicsharkmanagementbytunaregional fisheriesmanagementorganizationsGlobal Ecology and Conservation 4 1ndash7 httpsdoiorg101016jgecco201505003

Tuck G N Polacheck T amp Bulman C M (2003) Spatio-temporaltrendsoflonglinefishingeffortintheSouthernOceanandimplica-tionsforseabirdbycatchBiological Conservation1141ndash27httpsdoiorg101016S0006-3207(02)00378-6

UNEP-WCMC(2016)Marine no net loss A feasibility assessment of imple-menting no net loss of biodiversity in the seaCambridgeUKUnitedNationsEnvironmentProgramme

Vaissiegravere A-C Levrel H Pioch S amp Carlier A (2014) Biodiversityoffsets for offshore wind farm projects The current situation inEurope Marine Policy 48 172ndash183 httpsdoiorg101016jmarpol201403023

Wallace B P Heppell S S Lewison R L Kelez S amp CrowderL B (2008) Impacts of fisheries bycatch on loggerhead tur-tles worldwide inferred from reproductive value analy-ses Journal of Applied Ecology 45 1076ndash1085 httpsdoiorg101111j1365-2664200801507x

Wanless R M Ryan P G Altwegg R Angel A Cooper JCuthbert R amp Hilton G M (2009) From both sides Dire de-mographic consequences of carnivorous mice and longlining for

the critically endangered Tristan albatrosses on Gough IslandBiological Conservation 142 1710ndash1718 httpsdoiorg101016jbiocon200903008

WardP LawrenceEDarbyshireRampHindmarshS (2008) Large-scale experiment shows that nylon leaders reduce shark bycatchandbenefitpelagiclonglinefishersFisheries Research90100ndash108httpsdoiorg101016jfishres200709034

WardTampPhillipsB(2010)SeafoodecolabelingInRQGraftonRHilbornDSquiresMTaitampMJWilliams(Eds)Handbook of ma-rine fisheries conservation and management (pp 608ndash617) OxfordUKOxfordUniversityPress

WilcoxCampDonlanCJ (2007)Compensatorymitigationasasolu-tion to fisheries bycatch-biodiversity conservation conflictsFrontiers in Ecology and the Environment 5 325ndash331 httpsdoiorg1018901540-9295(2007)5[325cmaast]20co2

WilcoxCampDonlanCJ (2009)NeedforaclearandfairevaluationofbiodiversityoffsetsforfisheriesbycatchConservation Biology23770ndash772httpsdoiorg101111j1523-1739200901173x

Wolf SHartlBCarrollCNeelMCampGreenwaldDN (2015)Beyond PVAWhy recovery under the Endangered Species Act ismorethanpopulationviabilityBioScience65200ndash207httpsdoiorg101093bioscibiu218

ZedlerJBampCallawayJC (1999)TrackingwetlandrestorationDomitigation sites follow desired trajectories Restoration Ecology 769ndash73httpsdoiorg101046j1526-100X199907108x

Žydelis R Wallace B P Gilman E L amp Werner T B (2009)Conservation of marine megafauna through minimization of fish-eries bycatch Conservation Biology 23 608ndash616 httpsdoiorg101111j1523-1739200901172x

How to cite this articleMilner-GullandEJGarciaSArlidgeW etalTranslatingtheterrestrialmitigationhierarchytomarinemegafaunaby-catchFish Fish 2018001ndash15 httpsdoiorg101111faf12273

Page 10: Translating the terrestrial mitigation hierarchy to marine ......of marine megafauna by-catch in fisheries, going from defining an overarching goal with an associated quantitative

10emsp |emsp emspensp MILNER- GULLAND Et AL

47emsp|emspTemporal considerations

Thetimingofoffsetsinrelationtootherelementsofthemitigationhierarchyhasbeenthesubjectofdebatewithintheterrestriallitera-tureThemainsuggestionforaddressingthetemporarylossofbio-diversitywhileoffsetscometofruitionhasbeenadoptingmitigationbankingwherebyoffsetsareimplementedinadvanceofpotentiallydamagingactivitiesprovidingbiodiversitycreditswhichcanbeusedtocompensateforlaterlossesThisbothremovesanelementofun-certaintyfromtheoffsetimplementationandreducesthetimelagbetweenlossandgain(Mann2015)Withrespecttomarinemega-faunaby-catchflexibilityintimingprovidesadditionalscopeforcostreduction and benefit enhancementwhichmay not be present intraditionalhabitat-basedterrestrialoffsetsForexampletemporarymeasuressuchasashort-termby-catchtaxtofundanoffsetmaybeusedifmitigationoravoidancemethodstaketimetocomeonlineorifatemporarynudgeisenoughtocausebehaviouralchangeThismightbethecaseifapolicywasneededtoinducefisherstotakeupnewgeartoavoidthecostofanoffsetorifconcernsaboutsafetyoryieldreductionsduringthetransitiontonewgearcouldbeallayedbyatemporarysubsidyforearlyadoptersorapaidparticipatorymoni-toringprogrammeto informwider implementation(egthemobu-lidandsharkcase-studiesinTable3)Justasforhabitatrestoration(ZedlerampCallaway 1999) by-catchoffset strategieswhich targetjuvenilestagesof long-livedspecies (eg turtleheadstartingor in-vasive removal fromseabirdnesting islands)may takemanyyearsfor their effects to become apparent in an increase in populationgrowthratesAdditionaluncertaintyisintroducedbythedifficultyinmonitoringpopulationsofmanyby-catch species (eg seabirdsHatch2003)leadingtouncertainestimatesoftheimpactofoffsetactivitiesonpopulationgrowth(seecase-studiesinTable3)Theseproblemsarenot insuperablehoweverpositivetrendshavebeenreportedinturtlepopulationsoverdecadesasaresultofnestpro-tection(egDuttonDuttonChaloupkaampBoulon2005)

5emsp |emspUSING INCENTIVES TO REDUCE BY- C ATCH

Manyoftheexamplesandprinciplesdiscussedaboveeitherimplic-itlyorexplicitlyrelatetotheeconomicsocialinstitutionalormoralincentivesoperatingondifferentactorsinsideandoutsidethefish-erywhichcanbepositiveornegativeWenowturntoadiscussionofhowincentivescanbeusedtoreduceby-catchwithinourframe-workIncentivescanbeputinplacetochangefisherbehaviourwithrespecttoanyoftheelementsoftheframework (avoidminimizeremediateandoffsetTable3)Althoughdiscussedintheliteraturemostof these incentive approaches are yet tobe implemented inthe realworldparticularly forby-catchThereforeuntil empiricalevidenceoftheireffectivenessisavailablethesesuggestionscomewithacaveat

Financial costsofby-catchmitigationactions canarise for in-stancefromlostcatchcapitalinvestmentsinnewgearormitigation

equipmentor the lossofaccesstoafisheryCostsmayalsoarisefromthedeploymentofby-catchobserversortrainingintheuseofnewgearThesecostscanbepaidbyfishingcompaniesorindivid-ualsorbygovernmentsNGOsorseafoodconsumersWhetherornotcompensationforcostsincurredbyfishersisseenasappropri-atedependsonwhetherby-catchreductionisseenasasocialgoodthatfishersareproviding(inwhichcasetheyshouldbecompensatedforit)orasputtingrighttheharmthattheyaredoingtobiodiver-sitywhilegeneratingtheirownprivategain(ineconomiclanguagewhetherby-catchisviewedasanunpricedexternalityinwhichcasetheyshouldpay)Italsodependsonwhethereconomichardshipwillensueacaseforcompensationofby-catchreductioncostsincurredbypeopledependenton fishing for their livelihoodsmaybemoresympatheticallyreceivedbyotheractorsthanacasemadebyalargemultinationalfishingcompany

Ifby-catchisseenasanunpricedexternalityitmightbesociallyoptimaltotaxfishersfortheirby-catchsothatthisexternalityisin-ternalizedThisplacesanexplicitpriceuponby-catch(Boyce1996Pascoeetal2010SquiresampGarcia2014)Theby-catchprice islikely to be incorporated into the price of the target species andtherebybecomespartofthetargetspeciescostThispricecouldbeset differently for different demographic classesof theby-caughtspecies depending on the impact the loss of an individualwouldhaveonthepopulationAllelsebeingequalputtingapriceonby-catchmeans that theseafoodproduct that is the targetcatchbe-comesmoreexpensiveandconsumershave topaymore for theirseafoodreducingdemandTheninprincipleeveryfirminthesup-plychaineveryvesselandeveryconsumerhaveanincentivetore-duceby-catchuntileacheconomicactorrsquosmarginalcostofby-catchreductionequals thecommonpriceofby-catch that theyall faceOffsetsareonewaytopriceandinternalizetheby-catchexternalitycostIfanoffsettingactioniscostlytoimplementandmustbepaidforwith each unit of by-catch it implicitly prices the residual by-catch In this circumstance the effect from a financial standpointisthesameasaby-catchtaxwiththe levelsetbasedonthecostoftheoffsetVariousinstitutionalstructurestosupportthischargeperunitofby-catcharepossiblewithdifferentimplicationsintermsofthedistributionofcostsandbenefitsForexampleaninsuranceschemecouldbepaidintobyfishersthatpaysoutintheeventofaby-catcheventtherebyspreadingthecostofunavoidablerareby-catcheventsOratradablepermitschemecouldoperatesuchthatfisherswhoexperienceaby-catcheventcanbuyapermitwiththecostvaryingdependingondemandforpermits (henceprovidingavessel-levelincentivetoinnovatetoreduceby-catch)

If there isdemandforconservation inan internationalmarketthen price premiums and market access (through eco-labellingsupply chain certification other food sustainability campaignsWardampPhillips2010)orboycottsactingasstrategicthreatsfromconsumers (Kotchen 2013 Segerson 2010) could act as positiveornegativeeconomic leversonthe fisheryprovidingan incentivefor fishers to reduce their by-catch voluntarily (as has been sug-gested for the Brazilianmahi-mahi fishery Table3) For exampletheMarine StewardshipCouncil now includesby-catchmitigation

emspensp emsp | emsp11MILNER- GULLAND Et AL

intheircertificationprocess(MSC2014)Demand-ledleversmaybemoreorlessapplicableatdifferentlevelsinthehierarchyforexam-pleavoidancemayberelativelyhardtoevidencewhileoffsettingmaybelesseasytoselltoaconsumerthanminimizationorreme-diationConcerns about the unintended consequences of positiveincentives (particularlyfordirectsubsidiesratherthanconditionalincentives)maydeterminewhethertheyareanappropriateinstru-mentinagivencaseForexampletheymaybeinappropriateifthereisariskthattheadditionalmoneyisreinvestedinincreasedfishingcapacityor iftheremaybeconsumptionproductionorconserva-tionleakages(transferoftheproblemsomewhereelse)whetheratthe vessel fishery or trans-national levelHigh transactions costsmayalsolimitthebenefitsofincentivesschemes

Otherchangeswhichmayneedtobeincentivizedforsuccessfulimplementationofby-catchreductionpoliciesmaybelessamenabletofinancialmeasuresatleastpartlybecauseitislessclearhowtoassign financial value to theactionsor to thebenefits and losseswhichtheyproduceForexampleperceivedreductionsinsafetyforfishingcrews(fromweightedlonglinesfor instance)arecoststhatmaybehardtovaluefinanciallyOtherprerequisitesfor long-termsustainable behaviour change such as changes in social norms sothatfishingcommunitiesseeby-catchreductionasappropriatebe-haviourortechnicalskillacquisitionsothattheycanusenewmeth-odsmaybeincentivizedbycarefullydesignedinterventionsworkingwithfishers(Halletal2007)Conservationpoliciesbasedoneco-nomic incentives (extrinsicmotivation) are not always superior tothosebasedupon intrinsicmotivation Infact incentive-basedby-catch reduction policy instruments could even be counterproduc-tivebyreducingtheeffectivenessofintrinsicmotivationdependingupon the situation (although the empirical evidence on this topicisweak RodeGoacutemez-BaggethunampKrause 2015) If the changerequiredforby-catchreductiontoworkmeetscultural resistancethenparticipatory researchmightbeespeciallyeffective inbreak-ingdownbarriersbetweenthosewhowantby-catchreductiontotakeplaceandthosewhoactuallyhavetoimplementit(thefishers)ForexampleinAustraliathegovernment-fundedbodyOceanwatchfacilitatesengagementbetweencommunities thefishing industryseafood suppliers and government to improve knowledge sharing(wwwoceanwatchorgau)Innovationiscrucialinfisheriesandfish-ersareaccustomedtoadoptingnewtechnologyorprocessespo-tentiallymakingan incentivizedparticipatory researchprogrammeespeciallyfruitful

Sometimes the most efficient way to solve problems is a so-cial instrumentoran institutionalchange inplaceoforaswellasan economic instrument For example supporting developmentof fisherorganizations rather than instituting a vessel-level taxorsubsidy might provide the impetus needed to change behaviourInstitutingcatchshares(individualtransferablequotas)mayprovideanenablingenvironmentforby-catchreductionforexamplebypro-motingmoreeffectivemonitoring(Grimmetal2012)Experiencein terrestrial system produces similar insights incentive-basedschemeswhichalsobuildcommunitycohesionandsupportthede-velopment or strengthening of localmanagement institutions are

more effective in the longer run than direct economic incentives(Clementsetal2010)

6emsp |emspCONCLUSIONS

The framework we present here is novel It draws upon and ex-tends the frameworks for conceptualizing by-catch developed byHall (1996) and Hall Alverson andMetuzals (2000) It amalgam-atesHallrsquos frameworkwith themitigationhierarchyasused in theEnvironmental Impact Assessment literature (BBOP 2012) Thesuggestions about goals metric andmitigation actions are drawnfromtheempiricalby-catchliteratureandtheissueswediscussin-tegratetheconcernsoftheextensiveterrestrialandnascentmarineoffsetting literature with the by-catch literature The frameworkmakesclear thatanearlycrucial step is toclarify thegoalofanyby-catch reduction policyOverarching goals like those issued bytheConventiononBiologicalDiversity(egAichiTarget11that10ofmarinehabitatshouldbeunderprotectionby2020)needtobetranslatedintooperationaltermswithineachfisheryCurrentlyleg-islatedoragreedby-catch reductiongoals tend tobe less specificthantheycouldbeandthisleadstoproblemsininterpretingthesegoals inordertoplanaby-catchmitigationstrategy(seethecase-studies inTable3 for examples) This ambiguity is tobe expectedwithinnegotiatedtargetsbutitisachallengenonetheless(Maxwelletal2015)Usingacommonunitofby-catch impactsuchastheΔλTwhichweuseherewouldbehelpfulbothinclarifyingexpecta-tionsandevaluatingtheeffectivenessofelementsofthemitigationhierarchy

Once the by-catch goal is known options for implementingavoidanceminimizationremediationandoffsetscanbeclarified(asinTable2)Howeveroutsideof the interconnectedbiologyof theecosystemby-catch isembeddedwithinsocialandeconomicsys-temsDifferentunitsofanalysismaybeneededatdifferent levelsofthehierarchytocopewiththechallengesofincompleteoverlapbetween jurisdictional units fisheries target stocks and by-catchstocksJurisdictionalissuesareimportantandcomplexpotentiallyimpeding implementationFleets interact raisingtheriskofpolicyleakageforexampleifpeopleshifttootherfisheriesgearorliveli-hoodsThereforethescaleatwhicheachelementofthemitigationhierarchyisimplementedislikelytovarywithincentivestomitigateoftenbeingbest appliedat thevessel level focussedon reducingindividualmortalitywhileoffsettingisimplementedatthescaleoftheby-catchspeciesrsquostockWithtransboundaryspeciesunilateralconservationinonejurisdictioncreatesthepotentialforproductiontrade and conservation leakages For example a conserving Statecouldimplementtheavoidancestepandshutdownordramaticallycurtailitsownproductionofswordfishtoreduceseaturtleby-catchbuttheknock-oneffectmaybemoreimportationofswordfishfromfleetswithhigherseaturtleby-catch(RausserHamiltonKovachampStifter2009)

Translatingtheframeworkfromaspeciestoanecosystemlevelwill require consideration of the potential interactions between

12emsp |emsp emspensp MILNER- GULLAND Et AL

by-catchmitigationapproachestargetedatdifferentspecies(Serafyetal 2012) Actions to mitigate by-catch for one group of spe-cies can increase or decrease it for others and so a system-wideapproach isneededForexample changing fromJ-hooks tocirclehookstoreducemortalityofturtlesmaydecreaseorincreasesharkmortality(Andrakaetal2013GodinCarlsonampBurgener2012)In terrestrial systems similar interactions arise and value judge-mentsaremade(whetherexplicitlyorimplicitly)astowhatlossandgain of ldquobiodiversityrdquo translates to in operational terms andwhatelementsofbiodiversitymattermosttoimplementers

Uncertainty is high in ocean ecosystems creating both chal-lengesandopportunitiesinapplyingtheconceptofNNLthroughamitigationhierarchythatincludesoffsettingInparticularformarinemegafaunathereishighuncertaintyintheprocesseslinkinganyel-ementofthemitigationhierarchythroughtochangesinpopulationgrowthrateFurthermore impactscanbelong-termhardtomea-sureandspatiallydiffuseanduncertaintyisnotpredictablyspreadthroughthehierarchyThiscreatesadifferentsetofchallengestothosefacedinterrestrialsystemswhereatleastforsometypesofenvironmentalimpactthelinksbetweenactionandimpactarerel-ativelydirectandmeasurableanduncertaintygenerally increasesthroughthemitigationhierarchy (fromavoidthroughminimizere-mediatetooffset)

By-catch reduction measures have had significant successesoverthelastdecadesasaresultofsubstantialinvestmentoftimeand funding by researchers management authorities conserva-tionorganizationsandfishers(Coxetal2007)Howeverthissuc-cessisnotuniversalJustasforanyfisheriesmanagementissueapoorregulatoryregimelimitedcomplianceandlackofinforma-tionhampereffortstoreduceby-catchInsomeplaceshighlevelsofby-catch limitedoptions formitigationandweakgovernance(leadingtopoorenforcement)cancombinetomaketheby-catchproblemintractableOurframeworkwillnotsolvetheseproblemsHowever itbrings together the full rangeofapproaches forby-catchmitigationinastructuredandsystematicwaywhichrequiresatargettobeexpressedagainstwhichoutcomescanbeevaluatedByexposingareasofuncertaintyanddatadeficiencyitcouldchal-lengescientistsandmanagerstoobtainthedatarequiredproperlytoevaluate theeffectivenessofmitigationmeasuresThis couldthensupportandencourageclearerdecision-makingandprioriti-zationofactionsOurframeworkdemonstratesthattheprincipleof implementing thegoalofnonet loss throughamitigationhi-erarchy isasapplicable tomarinemegafaunaby-catchas to ter-restrial systems where it is already widely used in challengingdata-poorcircumstances

There isuntappedpotential forcost-effectiveby-catchmitiga-tionwhichcouldberealizedwiththeadoptionofthisframeworkandwithconsiderationofnewapproachestoincentivizingby-catchmitigationwithinthestepsofthehierarchyApplyingittoafewcase-studiesinpracticewilldemonstrateempiricallywhereandhowthepotentialforimprovedeffectivenesscouldbestberealizedExistinglegalframeworksoftenprecludeapproacheswhichimplicitlyorex-plicitly permit by-catch including the use of economic incentives

ornewapproachessuchasoffsetsHoweverinthiscontextofdy-namicuncertaintythedividendsofthinkingmorecreativelyaboutby-catchmitigationcouldbehigh

ACKNOWLEDG EMENTS

EJMG acknowledges the Pew Charitable Foundation for its sup-port of thiswork This article originated at a 2013workshop co-organized by NOAA-Fisheries and IUCN-CEEM-FEG entitledldquoMultidisciplinaryWorkshoptoAddressEcosystem-LevelImpactsofFisheriesBycatchonMarineMegafaunaBiodiversityConservationthrough Mitigation Policy Economic Instruments and TechnicalChangerdquo We thank the reviewers for their insightful commentswhichmuchimprovedthemanuscript

ORCID

E J Milner-Gulland httporcidorg0000-0003-0324-2710

R E FE R E N C E S

Alfaro-Shigueto J Dutton P H amp Mangel J (2007) Interactionsbetween leatherback turtles and Peruvian artisanal fisher-ies Chelonian Conservation and Biology 6 129ndash134 httpsdoiorg1027441071-8443(2007)6[129ibltap]20co2

Alfaro-Shigueto JMangel JCBernedoFDuttonPHSeminoffJAampGodleyB J (2011) Small-scale fisheriesofPeruAmajorsinkformarineturtles inthePacificJournal of Applied Ecology481432ndash1440httpsdoiorg101111j1365-2664201102040x

Alfaro-ShiguetoJMangelJCPajueloMDuttonPHSeminoffJ A amp Godley B J (2010) Where small can have a large im-pact Structure and characterization of small-scale fisheries inPeru Fisheries Research 106 8ndash17 httpsdoiorg101016jfishres201006004

Andraka SMugM HallM PonsM Pacheco L ParralesM hellipOrtega D (2013) Circle hooks Developing better fishing prac-ticesintheartisanallonglinefisheriesoftheEasternPacificOceanBiological Conservation 160 214ndash224 httpsdoiorg101016jbiocon201301019

ApostolopoulouEampAdamsWM(2017)BiodiversityoffsettingandconservationReframingnaturetosaveitOryx5123ndash31httpsdoiorg101017S0030605315000782

BaacuteezJCRealRGarciacutea-SotoCJoseacuteMMaciacuteasDampCamintildeasJA(2007)Loggerheadturtleby-catchdependsondistancetothecoastindependentoffishingeffortImplicationsforconservationandfish-eries management Marine Ecology Progress Series 338 249ndash256httpsdoiorg101017S0030605315000782

BBOP (2012) Standard on biodiversity offsets Business and biodiversity offsets programmeWashingtonDCForestTrends

Bishop J (2006) Standardizing fishery-dependent catch and ef-fort data in complex fisheries with technology change Reviews in Fish Biology and Fisheries 16 21ndash38 httpsdoiorg101007s11160-006-0004-9

BoyceJ(1996)AneconomicanalysisofthefisheriesbycatchproblemJournal of Environmental Economics and Management31 314ndash336httpsdoiorg101006jeem19960047

BugoniLManciniPLMonteiroDSNascimentoLampNevesTS(2008)SeabirdbycatchintheBrazilianpelagiclonglinefisheryandareviewofcaptureratesinthesouthwesternAtlanticOceanEndangered Species Research5137ndash147httpsdoiorg103354esr00115

emspensp emsp | emsp13MILNER- GULLAND Et AL

BullJWampBrownlieS(2017)Thetransitionfromnonetlosstoanetgainof biodiversity is far from trivialOryx51 53ndash59 httpsdoiorg101017S0030605315000861

BullJWBryantCBakerJampMilner-GullandEJ(2015December28)Developing measuring and communicating the outcomes of cor-porate biodiversity strategies [pdfdocument]RetrievedfromhttpwwwwildbusinessorgBull_etal_2015_WBLpdf

BullJWGordonAWatsonJEampMaronM(2016)Seekingcon-vergenceonthekeyconceptsinlsquononetlossrsquopolicyJournal of Applied Ecology531686ndash1693httpsdoiorg1011111365-266412726

BullJWHardyMJMoilanenAampGordonA (2015)Categoriesof flexibility in biodiversity offsetting and their implications forconservation Biological Conservation 192 522ndash532 httpsdoiorg101016jbiocon201508003

Bull JW Lloyd S P amp StrangeN (2017) Implementation gap be-tween the theory and practice of biodiversity offset multipliersConservation Lettershttpsdoiorg101111conl12335

Bull JW SuttleKBGordonA SinghN JampMilner-Gulland EJ(2013)BiodiversityoffsetsintheoryandpracticeOryx47369ndash380httpsdoiorg101017S003060531200172X

CampbellLMampCornwellML(2008)Humandimensionsofbycatchreduction technology Current assumptions and directions for fu-tureresearchEndangered Species Research5325ndash334httpsdoiorg103354esr00172

Caswell H Brault S Read A J amp Smith T D (1998) Harborporpoise and fisheries An uncertainty analysis of inciden-tal mortality Ecological Applications 8 1226ndash1238 httpsdoiorg1018901051-0761(1998)008[1226hpafau]20co2

ClementsTJohnANielsenKAnDTanSampMilner-GullandEJ (2010)Payments forbiodiversityconservation in thecontextofweak institutions Comparison of three programs from CambodiaEcological Economics 69 1283ndash1291 httpsdoiorg101016jecolecon200911010

CoxTLewisonRŽydelisRCrowderLSafinaCampReadA(2007)ComparingeffectivenessofexperimentalandimplementedbycatchreductionmeasuresTheidealandtherealConservation Biology211155ndash1164httpsdoiorg101111j1523-1739200700772x

CrollDADewarHDulvyNKFernandoDFrancisMPGalvaacuten-Magantildea F hellip Newton K M (2016) Vulnerabilities and fisher-ies impactsTheuncertain futureofmanta anddevil raysAquatic Conservation Marine and Freshwater Ecosystems 26 562ndash575httpsdoiorg101002aqc2591

Damalas D amp Vassilopoulou V (2013) Slack regulation com-pliance in the Mediterranean fisheries A paradigm from theGreek Aegean Sea demersal trawl fishery modelling discardogives Fisheries Management and Ecology 20 21ndash33 httpsdoiorg101111j1365-2400201200860x

DuttonDLDuttonPHChaloupkaMampBoulonRH(2005)IncreaseofaCaribbeanleatherbackturtleDermochelys coriaceanestingpop-ulation linked to long-termnestprotectionBiological Conservation126186ndash194httpsdoiorg101016jbiocon200505013

DuttonPJosephJSquiresDampWilliamsM(2011)Bellagioblue-print foractiononseaturtlesChapter2 InPDuttonDSquiresampM Ahmed (Eds) Conservation of pacific sea turtles (pp 15ndash36)HonoluluHIUniversityofHawaiiPress

DuttonPampSquiresD (2008)AholisticstrategyforPacificseatur-tlerecoveryOcean Development and International Law39200ndash222httpsdoiorg10108000908320802013685

FAO (2011 January 5) International guidelines on bycatch manage-ment and reduction of discards Rome Italy Food and AgricultureOrganisation [pdf document] Retrieved from httpwwwfaoorgdocrephelliptba0022t00pdf

Finkelstein M Bakker V Doak D F Sullivan B Lewison RSatterthwaite W H hellip Henry R W (2008) Evaluating the po-tential effectiveness of compensatory mitigation strategies for

marinebycatchPLoS ONE3 e2480httpsdoiorg101371jour-nalpone0002480

FowlerSJ(2016January5)Draft best practice mitigation guidelines for sharks and rays taken in purse- seine and long-line fisheries Convention on Migratory Species[pdfdocument]RetrievedfromhttpwwwcmsintsitesdefaultfilesdocumentCMS_Sharks_CWG1_Doc_3_2pdf

FrancisMP(2014)Survival and depth distribution of spinetail devilrays (Mobula japanica) released from purse-seine catches NIWA ClientReportNoWLG2014-2WellingtonNewZealandDepartmentofConservation

Fulton E A Smith A D Smith D C amp van Putten I E (2011)Human behaviour The key source of uncertainty in fish-eries management Fish and Fisheries 12 2ndash17 httpsdoiorg101111j1467-2979201000371x

GardnerTAHaseABrownlieSEkstromJMPilgrimJDSavyCEhellipTenKateK(2013)BiodiversityoffsetsandthechallengeofachievingnonetlossConservation Biology271254ndash1264httpsdoiorg101111cobi12118

GjertsenHHallMampSquiresD(2010)IncentivestoaddressbycatchInRAllenJJosephampDSquires(Eds)Conservation and manage-ment of transnational tuna fisheries (pp225ndash250)Ames IAWiley-Blackwellhttpsdoiorg1010029780813820262ch14

Gjertsen H Squires D Dutton P amp Eguchi T (2014) Cost-effectivenessofalternativeconservationstrategieswithapplicationtothePacificLeatherbackTurtleConservation Biology28140ndash149httpsdoiorg101111cobi12239

GodinACCarlson JKampBurgenerV (2012)Theeffectofcirclehooks on shark catchability and at-vessel mortality rates in long-lines fisheriesBulletin of Marine Science88 469ndash483 httpsdoiorg105343bms20111054

GrimmDBarkhornIFestaDBonzonKBoomhowerJHovlandV amp Blau J (2012) Assessing catch sharesrsquo effects evidencefrom Federal United States and associated British Columbianfisheries Marine Policy 36 644ndash657 httpsdoiorg101016jmarpol201110014

HallMA(1996)OnbycatchesReviews in Fish Biology and Fisheries6319ndash352httpsdoiorg101007BF00122585

HallMAAlversonDLampMetuzalsKI(2000)By-catchProblemsand solutions Marine Pollution Bulletin 41 204ndash219 httpsdoiorg101016S0025-326X(00)00111-9

HallMANakanoHClarke S Thomas SMolloy J PeckhamSHhellipHallSJ (2007)Workingwithfisherstoreduceby-catchesIn S J Kenelly (Ed)By-catch reduction in the worldrsquos fisheries (pp235ndash288) Dordrecht The Netherlands Springer httpsdoiorg101007978-1-4020-6078-6_8

HallM amp RomanM (2013)Bycatch and non-tuna catch in the tropi-cal tuna purse seine fisheries of the worldFisheriesandAquacultureTechnicalPaper568RomeItalyFAO

HallMASwimmerYampPargaM(2012)NoldquosilverbulletsrdquobutplentyofoptionsWorkingwiththeeasternpacificartisanalfisherstore-duceseaturtlemortalityinfisheriesInJASeminoffampBWallace(Eds)Sea turtles of the eastern pacific Advances in research and con-servation(pp136ndash153)TucsonAZUniversityofArizonaPress

HamnerRMWadePOremusMStanleyMBrownPConstantineR amp Baker C S (2014) Critically low abundance and limits tohuman-relatedmortalityfortheMauirsquosdolphinEndangered Species Research2687ndash92httpsdoiorg103354esr00621

HatchSA(2003)Statisticalpowerfordetectingtrendswithapplica-tions to seabird monitoringBiological Conservation 111 317ndash329httpsdoiorg101016S0006-3207(02)00301-4

HeppellSSCrowderLBampCrouseDT(1996)Modelstoevaluateheadstartingasamanagementtoolforlong-livedturtlesEcological Applications6556ndash565httpsdoiorg1023072269391

HoughPampRobertsonM(2009)MitigationunderSection404oftheCleanWater ActWhere it comes from what it meansWetlands

14emsp |emsp emspensp MILNER- GULLAND Et AL

Ecology and Management 17 15ndash33 httpsdoiorg101007s11273-008-9093-7

IATTC(2015)Resolution on the conservation of mobulid rays caught in as-sociation with fisheries in the IATTC convention area Inter-AmericanTropical TunaCommission89thAnnualMeetingResolutionC-15-04LaJollaCAInter-AmericanTropicalTunaCommission

IFC(2012)Performance standard 6 Biodiversity conservation and sustain-able management of natural resources January 1 2012WashingtonDCInternationalFinanceCorporation

Innes J Pascoe S Wilcox C Jennings S amp Paredes S (2015)MitigatingundesirableimpactsinthemarineenvironmentAreviewofmarket-basedmanagementmeasuresFrontiers in Marine Science276httpsdoiorg103389fmars201500076

JanniseCSquiresDSeminoffJampDuttonP (2010)Conservationinvestments andmitigationTheCaliforniadrift gillnet fishery andpacificseaturtles InRQGraftonRHilbornDSquiresMTaitampMJWilliams(Eds)Handbook of marine fisheries conservation and management(pp231ndash240)OxfordUKOxfordUniversityPress

Jones E amp FrancisM (2012)Protected rays ndash Occurrence and devel-opment of mitigation methods in the New Zealand tuna purse seine fishery Auckland New Zealand National Institute of Water andAtmosphericResearch

KormosRKormosCFHumleTLanjouwARainerHVicturineR hellipWilliamson E A (2014) Great apes and biodiversity offsetprojectsinAfricaThecasefornationaloffsetstrategiesPLoS ONE9(11)e111671httpsdoiorg101371journalpone0111671

KotchenMJ (2013)Voluntaryand information-basedapproachestoenvironmentalmanagementApubliceconomicsperspectiveReview of Environmental Economics and Policy 7(2) 276ndash295 httpsdoiorg101093reepret012

Kyriazi Z LejanoRMaes FampDegraer S (2015)Bargaining a netgaincompensationagreementbetweenamarinerenewableenergydeveloperandamarineprotectedareamanagerMarine Policy6040ndash48httpsdoiorg101016jmarpol201506005

LentRampSquiresD(2017)ReducingmarinemammalbycatchinglobalfisheriesAneconomicsapproachDeep Sea Research Part II Topical Studies in Oceanography 140 268ndash277 httpsdoiorg101016jdsr2201703005

Lewison R L Crowder L B Read A J amp Freeman S A (2004)Understanding impactsof fisheriesbycatchonmarinemegafaunaTrends in Ecology amp Evolution19598ndash604httpsdoiorg101016jtree200409004

MannC (2015)StrategiesforsustainablepolicydesignConstructiveassessmentofbiodiversityoffsetsandbankingEcosystem Services16266ndash274httpsdoiorg101016jecoser201507001

Marine Stewardship Council (2014 June 21) MSC fisheries certifica-tion requirements v20 [pdf doc] httpswwwmscorgdocumentsscheme-documentsfisheries-certification-scheme-documentsfisheries-certification-requirements-version-20

MaronM IvesCDKujalaHBullJWMaseykFJBekessyShellip Possingham H P (2016) Taming a wicked problem Resolvingcontroversies inbiodiversityoffsettingBioScience66(6)489ndash498httpsdoiorg101093bioscibiw038

MaxwellSLMilner-GullandEJJonesJPKnightATBunnefeldNNunoAhellipRhodesJR(2015)BeingsmartaboutSMARTenvi-ronmentaltargetsScience3471075ndash1076httpsdoiorg101126scienceaaa1451

Moilanen A Van Teeffelen A J Ben-Haim Y amp Ferrier S (2009)Howmuch compensation is enoughA framework for incorporat-inguncertaintyandtimediscountingwhencalculatingoffsetratiosfor impactedhabitatRestoration Ecology17 470ndash478 httpsdoiorg101111j1526-100X200800382x

MorarNToadvineTampBohannanBJ(2015)Biodiversityattwenty-fiveyearsRevolutionorredherringEthics Policy amp Environment1816ndash29httpsdoiorg1010802155008520151018380

OrphanidesCDampPalkaDL(2013)Analysisofharborporpoisegill-netbycatchcomplianceandenforcement trends in theUSnorth-western Atlantic January 1999 to May 2010 Endangered Species Research20251ndash269httpsdoiorg103354esr00499

Pascoe S Innes J Holland D Finas M Theacutebaud O TownsendR hellip Hutton T (2010) Use of incentive-based managementsystems to limit bycatch and discarding International Review of Environmental and Resource Economics 4 123ndash161 httpsdoiorg10156110100000032

PhalanBHayesG Brooks SMarshDHoward PCostelloeBhellip Whitaker S (2017) Avoiding impacts on biodiversity throughstrengthening the first stage of the mitigation hierarchy Oryxhttpsdoiorg101017S0030605316001034

Queacutetier F Regnery B amp Levrel H (2014) No net loss of biodiver-sity or paper offsets A critical review of the French no net losspolicy Environmental Science amp Policy 38 120ndash131 httpsdoiorg101016jenvsci201311009

RadzioTASmolinskyJAampRoosenburgWM(2013)Lowuseofre-quiredterrapinbycatchreductiondevicesinarecreationalcrabpotfisheryHerpetological Conservation and Biology8222ndash227

RaineyHJPollardEHBDutsonGEkstromJMLivingstoneSRTempleHJampPilgrimJD(2015)AreviewofcorporategoalsofnonetlossandnetpositiveimpactonbiodiversityOryx49232ndash238httpsdoiorg101017S0030605313001476

Rausser G C Hamilton S F Kovach M amp Stifter R (2009)UnintendedconsequencesThe spillovereffectsof commonprop-ertyregulationsMarine Policy3324ndash39httpsdoiorg101016jmarpol200803020

Rice J (2014) Evolution of international commitments for fisheriessustainability ICES Journal of Marine Science Journal du Conseil71157ndash165httpsdoiorg101093icesjmsfst078

RichardYampAbrahamER(2013)ApplicationofPotentialBiologicalRemoval methods to seabird populations New Zealand AquaticEnvironmentandBiodiversityReport108

RodeJGoacutemez-BaggethunEampKrauseT(2015)Motivationcrowd-ingbyeconomic incentives inconservationpolicyAreviewoftheempiricalevidenceEcological Economics117270ndash282httpsdoiorg101016jecolecon201411019

RogersAA(2013)SocialwelfareandmarinereservesIswillingnesstopayforconservationdependentonmanagementprocessAdiscretechoiceexperimentoftheNingalooMarineParkinAustraliaCanadian Journal of Agricultural EconomicsRevue Canadienne Drsquoagroeconomie61217ndash238httpsdoiorg101111cjag12008

Rosenberg A A amp McLeod K L (2005) Implementing ecosystem-basedapproachestomanagementfortheconservationofecosystemservicesMarine Ecology Progress Series300 270ndash274 httpsdoiorg103354meps300270

Segerson K (2010) Can voluntary programs reduce sea turtle by-catch Insights from the literature in environmental economics InRQGraftonRHilbornDSquiresMTaitampMJWilliams(Eds)Handbook of marine fisheries conservation and management(pp618ndash629)OxfordUKOxfordUniversityPress

Serafy JECookeS JDiazGAGraves JEHallMShivjiMampSwimmerY(2012)CirclehooksincommercialrecreationalandartisanalfisheriesResearchstatusandneedsforimprovedconser-vation and management Bulletin of Marine Science 88 371ndash391httpsdoiorg105343bms20121038

ShiodeDHu F ShigaM Yokota K amp Tokai T (2005)Midwaterfloatsystemforstandardizinghookdepthsontunalonglinestore-duce sea turtleby-catchFisheries Science71 1182ndash1184httpsdoiorg101111j1444-2906200501080x

Sims M Cox T amp Lewison R (2008) Modeling spatial patternsin fisheries bycatch Improving bycatch maps to aid fisheriesmanagement Ecological Applications 18 649ndash661 httpsdoiorg10189007-06851

emspensp emsp | emsp15MILNER- GULLAND Et AL

Squires D amp Garcia SM (2014) Ecosystem-level impacts of fisheries bycatch on marine megafauna Biodiversity conservation through miti-gation policy economic instruments and technical changeReportofthe IUCN-CEM-FEGScientificworkshopGland Switzerland 7ndash10October2013GlandSwitzerlandIUCN

SquiresDampGarciaSM(inpress)Fisheries bycatch in marine ecosys-tems Policy economic instruments and technical change ChichesterUKJWileyampSons

SwimmerYArauzRMcCrackenMMcNaughtonLBallesteroJMusylMhellipBrillR(2006)DivingbehavioranddelayedmortalityofoliveridleyseaturtlesLepidochelys olivaceaaftertheirreleasefromlongline fishing gearMarine Ecology Progress Series323 253ndash261httpsdoiorg103354meps323253

TolottiMTFilmalterJDBachPTravassosPSeretBampDagornL(2015)BanningisnotenoughThecomplexitiesofoceanicsharkmanagementbytunaregional fisheriesmanagementorganizationsGlobal Ecology and Conservation 4 1ndash7 httpsdoiorg101016jgecco201505003

Tuck G N Polacheck T amp Bulman C M (2003) Spatio-temporaltrendsoflonglinefishingeffortintheSouthernOceanandimplica-tionsforseabirdbycatchBiological Conservation1141ndash27httpsdoiorg101016S0006-3207(02)00378-6

UNEP-WCMC(2016)Marine no net loss A feasibility assessment of imple-menting no net loss of biodiversity in the seaCambridgeUKUnitedNationsEnvironmentProgramme

Vaissiegravere A-C Levrel H Pioch S amp Carlier A (2014) Biodiversityoffsets for offshore wind farm projects The current situation inEurope Marine Policy 48 172ndash183 httpsdoiorg101016jmarpol201403023

Wallace B P Heppell S S Lewison R L Kelez S amp CrowderL B (2008) Impacts of fisheries bycatch on loggerhead tur-tles worldwide inferred from reproductive value analy-ses Journal of Applied Ecology 45 1076ndash1085 httpsdoiorg101111j1365-2664200801507x

Wanless R M Ryan P G Altwegg R Angel A Cooper JCuthbert R amp Hilton G M (2009) From both sides Dire de-mographic consequences of carnivorous mice and longlining for

the critically endangered Tristan albatrosses on Gough IslandBiological Conservation 142 1710ndash1718 httpsdoiorg101016jbiocon200903008

WardP LawrenceEDarbyshireRampHindmarshS (2008) Large-scale experiment shows that nylon leaders reduce shark bycatchandbenefitpelagiclonglinefishersFisheries Research90100ndash108httpsdoiorg101016jfishres200709034

WardTampPhillipsB(2010)SeafoodecolabelingInRQGraftonRHilbornDSquiresMTaitampMJWilliams(Eds)Handbook of ma-rine fisheries conservation and management (pp 608ndash617) OxfordUKOxfordUniversityPress

WilcoxCampDonlanCJ (2007)Compensatorymitigationasasolu-tion to fisheries bycatch-biodiversity conservation conflictsFrontiers in Ecology and the Environment 5 325ndash331 httpsdoiorg1018901540-9295(2007)5[325cmaast]20co2

WilcoxCampDonlanCJ (2009)NeedforaclearandfairevaluationofbiodiversityoffsetsforfisheriesbycatchConservation Biology23770ndash772httpsdoiorg101111j1523-1739200901173x

Wolf SHartlBCarrollCNeelMCampGreenwaldDN (2015)Beyond PVAWhy recovery under the Endangered Species Act ismorethanpopulationviabilityBioScience65200ndash207httpsdoiorg101093bioscibiu218

ZedlerJBampCallawayJC (1999)TrackingwetlandrestorationDomitigation sites follow desired trajectories Restoration Ecology 769ndash73httpsdoiorg101046j1526-100X199907108x

Žydelis R Wallace B P Gilman E L amp Werner T B (2009)Conservation of marine megafauna through minimization of fish-eries bycatch Conservation Biology 23 608ndash616 httpsdoiorg101111j1523-1739200901172x

How to cite this articleMilner-GullandEJGarciaSArlidgeW etalTranslatingtheterrestrialmitigationhierarchytomarinemegafaunaby-catchFish Fish 2018001ndash15 httpsdoiorg101111faf12273

Page 11: Translating the terrestrial mitigation hierarchy to marine ......of marine megafauna by-catch in fisheries, going from defining an overarching goal with an associated quantitative

emspensp emsp | emsp11MILNER- GULLAND Et AL

intheircertificationprocess(MSC2014)Demand-ledleversmaybemoreorlessapplicableatdifferentlevelsinthehierarchyforexam-pleavoidancemayberelativelyhardtoevidencewhileoffsettingmaybelesseasytoselltoaconsumerthanminimizationorreme-diationConcerns about the unintended consequences of positiveincentives (particularlyfordirectsubsidiesratherthanconditionalincentives)maydeterminewhethertheyareanappropriateinstru-mentinagivencaseForexampletheymaybeinappropriateifthereisariskthattheadditionalmoneyisreinvestedinincreasedfishingcapacityor iftheremaybeconsumptionproductionorconserva-tionleakages(transferoftheproblemsomewhereelse)whetheratthe vessel fishery or trans-national levelHigh transactions costsmayalsolimitthebenefitsofincentivesschemes

Otherchangeswhichmayneedtobeincentivizedforsuccessfulimplementationofby-catchreductionpoliciesmaybelessamenabletofinancialmeasuresatleastpartlybecauseitislessclearhowtoassign financial value to theactionsor to thebenefits and losseswhichtheyproduceForexampleperceivedreductionsinsafetyforfishingcrews(fromweightedlonglinesfor instance)arecoststhatmaybehardtovaluefinanciallyOtherprerequisitesfor long-termsustainable behaviour change such as changes in social norms sothatfishingcommunitiesseeby-catchreductionasappropriatebe-haviourortechnicalskillacquisitionsothattheycanusenewmeth-odsmaybeincentivizedbycarefullydesignedinterventionsworkingwithfishers(Halletal2007)Conservationpoliciesbasedoneco-nomic incentives (extrinsicmotivation) are not always superior tothosebasedupon intrinsicmotivation Infact incentive-basedby-catch reduction policy instruments could even be counterproduc-tivebyreducingtheeffectivenessofintrinsicmotivationdependingupon the situation (although the empirical evidence on this topicisweak RodeGoacutemez-BaggethunampKrause 2015) If the changerequiredforby-catchreductiontoworkmeetscultural resistancethenparticipatory researchmightbeespeciallyeffective inbreak-ingdownbarriersbetweenthosewhowantby-catchreductiontotakeplaceandthosewhoactuallyhavetoimplementit(thefishers)ForexampleinAustraliathegovernment-fundedbodyOceanwatchfacilitatesengagementbetweencommunities thefishing industryseafood suppliers and government to improve knowledge sharing(wwwoceanwatchorgau)Innovationiscrucialinfisheriesandfish-ersareaccustomedtoadoptingnewtechnologyorprocessespo-tentiallymakingan incentivizedparticipatory researchprogrammeespeciallyfruitful

Sometimes the most efficient way to solve problems is a so-cial instrumentoran institutionalchange inplaceoforaswellasan economic instrument For example supporting developmentof fisherorganizations rather than instituting a vessel-level taxorsubsidy might provide the impetus needed to change behaviourInstitutingcatchshares(individualtransferablequotas)mayprovideanenablingenvironmentforby-catchreductionforexamplebypro-motingmoreeffectivemonitoring(Grimmetal2012)Experiencein terrestrial system produces similar insights incentive-basedschemeswhichalsobuildcommunitycohesionandsupportthede-velopment or strengthening of localmanagement institutions are

more effective in the longer run than direct economic incentives(Clementsetal2010)

6emsp |emspCONCLUSIONS

The framework we present here is novel It draws upon and ex-tends the frameworks for conceptualizing by-catch developed byHall (1996) and Hall Alverson andMetuzals (2000) It amalgam-atesHallrsquos frameworkwith themitigationhierarchyasused in theEnvironmental Impact Assessment literature (BBOP 2012) Thesuggestions about goals metric andmitigation actions are drawnfromtheempiricalby-catchliteratureandtheissueswediscussin-tegratetheconcernsoftheextensiveterrestrialandnascentmarineoffsetting literature with the by-catch literature The frameworkmakesclear thatanearlycrucial step is toclarify thegoalofanyby-catch reduction policyOverarching goals like those issued bytheConventiononBiologicalDiversity(egAichiTarget11that10ofmarinehabitatshouldbeunderprotectionby2020)needtobetranslatedintooperationaltermswithineachfisheryCurrentlyleg-islatedoragreedby-catch reductiongoals tend tobe less specificthantheycouldbeandthisleadstoproblemsininterpretingthesegoals inordertoplanaby-catchmitigationstrategy(seethecase-studies inTable3 for examples) This ambiguity is tobe expectedwithinnegotiatedtargetsbutitisachallengenonetheless(Maxwelletal2015)Usingacommonunitofby-catch impactsuchastheΔλTwhichweuseherewouldbehelpfulbothinclarifyingexpecta-tionsandevaluatingtheeffectivenessofelementsofthemitigationhierarchy

Once the by-catch goal is known options for implementingavoidanceminimizationremediationandoffsetscanbeclarified(asinTable2)Howeveroutsideof the interconnectedbiologyof theecosystemby-catch isembeddedwithinsocialandeconomicsys-temsDifferentunitsofanalysismaybeneededatdifferent levelsofthehierarchytocopewiththechallengesofincompleteoverlapbetween jurisdictional units fisheries target stocks and by-catchstocksJurisdictionalissuesareimportantandcomplexpotentiallyimpeding implementationFleets interact raisingtheriskofpolicyleakageforexampleifpeopleshifttootherfisheriesgearorliveli-hoodsThereforethescaleatwhicheachelementofthemitigationhierarchyisimplementedislikelytovarywithincentivestomitigateoftenbeingbest appliedat thevessel level focussedon reducingindividualmortalitywhileoffsettingisimplementedatthescaleoftheby-catchspeciesrsquostockWithtransboundaryspeciesunilateralconservationinonejurisdictioncreatesthepotentialforproductiontrade and conservation leakages For example a conserving Statecouldimplementtheavoidancestepandshutdownordramaticallycurtailitsownproductionofswordfishtoreduceseaturtleby-catchbuttheknock-oneffectmaybemoreimportationofswordfishfromfleetswithhigherseaturtleby-catch(RausserHamiltonKovachampStifter2009)

Translatingtheframeworkfromaspeciestoanecosystemlevelwill require consideration of the potential interactions between

12emsp |emsp emspensp MILNER- GULLAND Et AL

by-catchmitigationapproachestargetedatdifferentspecies(Serafyetal 2012) Actions to mitigate by-catch for one group of spe-cies can increase or decrease it for others and so a system-wideapproach isneededForexample changing fromJ-hooks tocirclehookstoreducemortalityofturtlesmaydecreaseorincreasesharkmortality(Andrakaetal2013GodinCarlsonampBurgener2012)In terrestrial systems similar interactions arise and value judge-mentsaremade(whetherexplicitlyorimplicitly)astowhatlossandgain of ldquobiodiversityrdquo translates to in operational terms andwhatelementsofbiodiversitymattermosttoimplementers

Uncertainty is high in ocean ecosystems creating both chal-lengesandopportunitiesinapplyingtheconceptofNNLthroughamitigationhierarchythatincludesoffsettingInparticularformarinemegafaunathereishighuncertaintyintheprocesseslinkinganyel-ementofthemitigationhierarchythroughtochangesinpopulationgrowthrateFurthermore impactscanbelong-termhardtomea-sureandspatiallydiffuseanduncertaintyisnotpredictablyspreadthroughthehierarchyThiscreatesadifferentsetofchallengestothosefacedinterrestrialsystemswhereatleastforsometypesofenvironmentalimpactthelinksbetweenactionandimpactarerel-ativelydirectandmeasurableanduncertaintygenerally increasesthroughthemitigationhierarchy (fromavoidthroughminimizere-mediatetooffset)

By-catch reduction measures have had significant successesoverthelastdecadesasaresultofsubstantialinvestmentoftimeand funding by researchers management authorities conserva-tionorganizationsandfishers(Coxetal2007)Howeverthissuc-cessisnotuniversalJustasforanyfisheriesmanagementissueapoorregulatoryregimelimitedcomplianceandlackofinforma-tionhampereffortstoreduceby-catchInsomeplaceshighlevelsofby-catch limitedoptions formitigationandweakgovernance(leadingtopoorenforcement)cancombinetomaketheby-catchproblemintractableOurframeworkwillnotsolvetheseproblemsHowever itbrings together the full rangeofapproaches forby-catchmitigationinastructuredandsystematicwaywhichrequiresatargettobeexpressedagainstwhichoutcomescanbeevaluatedByexposingareasofuncertaintyanddatadeficiencyitcouldchal-lengescientistsandmanagerstoobtainthedatarequiredproperlytoevaluate theeffectivenessofmitigationmeasuresThis couldthensupportandencourageclearerdecision-makingandprioriti-zationofactionsOurframeworkdemonstratesthattheprincipleof implementing thegoalofnonet loss throughamitigationhi-erarchy isasapplicable tomarinemegafaunaby-catchas to ter-restrial systems where it is already widely used in challengingdata-poorcircumstances

There isuntappedpotential forcost-effectiveby-catchmitiga-tionwhichcouldberealizedwiththeadoptionofthisframeworkandwithconsiderationofnewapproachestoincentivizingby-catchmitigationwithinthestepsofthehierarchyApplyingittoafewcase-studiesinpracticewilldemonstrateempiricallywhereandhowthepotentialforimprovedeffectivenesscouldbestberealizedExistinglegalframeworksoftenprecludeapproacheswhichimplicitlyorex-plicitly permit by-catch including the use of economic incentives

ornewapproachessuchasoffsetsHoweverinthiscontextofdy-namicuncertaintythedividendsofthinkingmorecreativelyaboutby-catchmitigationcouldbehigh

ACKNOWLEDG EMENTS

EJMG acknowledges the Pew Charitable Foundation for its sup-port of thiswork This article originated at a 2013workshop co-organized by NOAA-Fisheries and IUCN-CEEM-FEG entitledldquoMultidisciplinaryWorkshoptoAddressEcosystem-LevelImpactsofFisheriesBycatchonMarineMegafaunaBiodiversityConservationthrough Mitigation Policy Economic Instruments and TechnicalChangerdquo We thank the reviewers for their insightful commentswhichmuchimprovedthemanuscript

ORCID

E J Milner-Gulland httporcidorg0000-0003-0324-2710

R E FE R E N C E S

Alfaro-Shigueto J Dutton P H amp Mangel J (2007) Interactionsbetween leatherback turtles and Peruvian artisanal fisher-ies Chelonian Conservation and Biology 6 129ndash134 httpsdoiorg1027441071-8443(2007)6[129ibltap]20co2

Alfaro-Shigueto JMangel JCBernedoFDuttonPHSeminoffJAampGodleyB J (2011) Small-scale fisheriesofPeruAmajorsinkformarineturtles inthePacificJournal of Applied Ecology481432ndash1440httpsdoiorg101111j1365-2664201102040x

Alfaro-ShiguetoJMangelJCPajueloMDuttonPHSeminoffJ A amp Godley B J (2010) Where small can have a large im-pact Structure and characterization of small-scale fisheries inPeru Fisheries Research 106 8ndash17 httpsdoiorg101016jfishres201006004

Andraka SMugM HallM PonsM Pacheco L ParralesM hellipOrtega D (2013) Circle hooks Developing better fishing prac-ticesintheartisanallonglinefisheriesoftheEasternPacificOceanBiological Conservation 160 214ndash224 httpsdoiorg101016jbiocon201301019

ApostolopoulouEampAdamsWM(2017)BiodiversityoffsettingandconservationReframingnaturetosaveitOryx5123ndash31httpsdoiorg101017S0030605315000782

BaacuteezJCRealRGarciacutea-SotoCJoseacuteMMaciacuteasDampCamintildeasJA(2007)Loggerheadturtleby-catchdependsondistancetothecoastindependentoffishingeffortImplicationsforconservationandfish-eries management Marine Ecology Progress Series 338 249ndash256httpsdoiorg101017S0030605315000782

BBOP (2012) Standard on biodiversity offsets Business and biodiversity offsets programmeWashingtonDCForestTrends

Bishop J (2006) Standardizing fishery-dependent catch and ef-fort data in complex fisheries with technology change Reviews in Fish Biology and Fisheries 16 21ndash38 httpsdoiorg101007s11160-006-0004-9

BoyceJ(1996)AneconomicanalysisofthefisheriesbycatchproblemJournal of Environmental Economics and Management31 314ndash336httpsdoiorg101006jeem19960047

BugoniLManciniPLMonteiroDSNascimentoLampNevesTS(2008)SeabirdbycatchintheBrazilianpelagiclonglinefisheryandareviewofcaptureratesinthesouthwesternAtlanticOceanEndangered Species Research5137ndash147httpsdoiorg103354esr00115

emspensp emsp | emsp13MILNER- GULLAND Et AL

BullJWampBrownlieS(2017)Thetransitionfromnonetlosstoanetgainof biodiversity is far from trivialOryx51 53ndash59 httpsdoiorg101017S0030605315000861

BullJWBryantCBakerJampMilner-GullandEJ(2015December28)Developing measuring and communicating the outcomes of cor-porate biodiversity strategies [pdfdocument]RetrievedfromhttpwwwwildbusinessorgBull_etal_2015_WBLpdf

BullJWGordonAWatsonJEampMaronM(2016)Seekingcon-vergenceonthekeyconceptsinlsquononetlossrsquopolicyJournal of Applied Ecology531686ndash1693httpsdoiorg1011111365-266412726

BullJWHardyMJMoilanenAampGordonA (2015)Categoriesof flexibility in biodiversity offsetting and their implications forconservation Biological Conservation 192 522ndash532 httpsdoiorg101016jbiocon201508003

Bull JW Lloyd S P amp StrangeN (2017) Implementation gap be-tween the theory and practice of biodiversity offset multipliersConservation Lettershttpsdoiorg101111conl12335

Bull JW SuttleKBGordonA SinghN JampMilner-Gulland EJ(2013)BiodiversityoffsetsintheoryandpracticeOryx47369ndash380httpsdoiorg101017S003060531200172X

CampbellLMampCornwellML(2008)Humandimensionsofbycatchreduction technology Current assumptions and directions for fu-tureresearchEndangered Species Research5325ndash334httpsdoiorg103354esr00172

Caswell H Brault S Read A J amp Smith T D (1998) Harborporpoise and fisheries An uncertainty analysis of inciden-tal mortality Ecological Applications 8 1226ndash1238 httpsdoiorg1018901051-0761(1998)008[1226hpafau]20co2

ClementsTJohnANielsenKAnDTanSampMilner-GullandEJ (2010)Payments forbiodiversityconservation in thecontextofweak institutions Comparison of three programs from CambodiaEcological Economics 69 1283ndash1291 httpsdoiorg101016jecolecon200911010

CoxTLewisonRŽydelisRCrowderLSafinaCampReadA(2007)ComparingeffectivenessofexperimentalandimplementedbycatchreductionmeasuresTheidealandtherealConservation Biology211155ndash1164httpsdoiorg101111j1523-1739200700772x

CrollDADewarHDulvyNKFernandoDFrancisMPGalvaacuten-Magantildea F hellip Newton K M (2016) Vulnerabilities and fisher-ies impactsTheuncertain futureofmanta anddevil raysAquatic Conservation Marine and Freshwater Ecosystems 26 562ndash575httpsdoiorg101002aqc2591

Damalas D amp Vassilopoulou V (2013) Slack regulation com-pliance in the Mediterranean fisheries A paradigm from theGreek Aegean Sea demersal trawl fishery modelling discardogives Fisheries Management and Ecology 20 21ndash33 httpsdoiorg101111j1365-2400201200860x

DuttonDLDuttonPHChaloupkaMampBoulonRH(2005)IncreaseofaCaribbeanleatherbackturtleDermochelys coriaceanestingpop-ulation linked to long-termnestprotectionBiological Conservation126186ndash194httpsdoiorg101016jbiocon200505013

DuttonPJosephJSquiresDampWilliamsM(2011)Bellagioblue-print foractiononseaturtlesChapter2 InPDuttonDSquiresampM Ahmed (Eds) Conservation of pacific sea turtles (pp 15ndash36)HonoluluHIUniversityofHawaiiPress

DuttonPampSquiresD (2008)AholisticstrategyforPacificseatur-tlerecoveryOcean Development and International Law39200ndash222httpsdoiorg10108000908320802013685

FAO (2011 January 5) International guidelines on bycatch manage-ment and reduction of discards Rome Italy Food and AgricultureOrganisation [pdf document] Retrieved from httpwwwfaoorgdocrephelliptba0022t00pdf

Finkelstein M Bakker V Doak D F Sullivan B Lewison RSatterthwaite W H hellip Henry R W (2008) Evaluating the po-tential effectiveness of compensatory mitigation strategies for

marinebycatchPLoS ONE3 e2480httpsdoiorg101371jour-nalpone0002480

FowlerSJ(2016January5)Draft best practice mitigation guidelines for sharks and rays taken in purse- seine and long-line fisheries Convention on Migratory Species[pdfdocument]RetrievedfromhttpwwwcmsintsitesdefaultfilesdocumentCMS_Sharks_CWG1_Doc_3_2pdf

FrancisMP(2014)Survival and depth distribution of spinetail devilrays (Mobula japanica) released from purse-seine catches NIWA ClientReportNoWLG2014-2WellingtonNewZealandDepartmentofConservation

Fulton E A Smith A D Smith D C amp van Putten I E (2011)Human behaviour The key source of uncertainty in fish-eries management Fish and Fisheries 12 2ndash17 httpsdoiorg101111j1467-2979201000371x

GardnerTAHaseABrownlieSEkstromJMPilgrimJDSavyCEhellipTenKateK(2013)BiodiversityoffsetsandthechallengeofachievingnonetlossConservation Biology271254ndash1264httpsdoiorg101111cobi12118

GjertsenHHallMampSquiresD(2010)IncentivestoaddressbycatchInRAllenJJosephampDSquires(Eds)Conservation and manage-ment of transnational tuna fisheries (pp225ndash250)Ames IAWiley-Blackwellhttpsdoiorg1010029780813820262ch14

Gjertsen H Squires D Dutton P amp Eguchi T (2014) Cost-effectivenessofalternativeconservationstrategieswithapplicationtothePacificLeatherbackTurtleConservation Biology28140ndash149httpsdoiorg101111cobi12239

GodinACCarlson JKampBurgenerV (2012)Theeffectofcirclehooks on shark catchability and at-vessel mortality rates in long-lines fisheriesBulletin of Marine Science88 469ndash483 httpsdoiorg105343bms20111054

GrimmDBarkhornIFestaDBonzonKBoomhowerJHovlandV amp Blau J (2012) Assessing catch sharesrsquo effects evidencefrom Federal United States and associated British Columbianfisheries Marine Policy 36 644ndash657 httpsdoiorg101016jmarpol201110014

HallMA(1996)OnbycatchesReviews in Fish Biology and Fisheries6319ndash352httpsdoiorg101007BF00122585

HallMAAlversonDLampMetuzalsKI(2000)By-catchProblemsand solutions Marine Pollution Bulletin 41 204ndash219 httpsdoiorg101016S0025-326X(00)00111-9

HallMANakanoHClarke S Thomas SMolloy J PeckhamSHhellipHallSJ (2007)Workingwithfisherstoreduceby-catchesIn S J Kenelly (Ed)By-catch reduction in the worldrsquos fisheries (pp235ndash288) Dordrecht The Netherlands Springer httpsdoiorg101007978-1-4020-6078-6_8

HallM amp RomanM (2013)Bycatch and non-tuna catch in the tropi-cal tuna purse seine fisheries of the worldFisheriesandAquacultureTechnicalPaper568RomeItalyFAO

HallMASwimmerYampPargaM(2012)NoldquosilverbulletsrdquobutplentyofoptionsWorkingwiththeeasternpacificartisanalfisherstore-duceseaturtlemortalityinfisheriesInJASeminoffampBWallace(Eds)Sea turtles of the eastern pacific Advances in research and con-servation(pp136ndash153)TucsonAZUniversityofArizonaPress

HamnerRMWadePOremusMStanleyMBrownPConstantineR amp Baker C S (2014) Critically low abundance and limits tohuman-relatedmortalityfortheMauirsquosdolphinEndangered Species Research2687ndash92httpsdoiorg103354esr00621

HatchSA(2003)Statisticalpowerfordetectingtrendswithapplica-tions to seabird monitoringBiological Conservation 111 317ndash329httpsdoiorg101016S0006-3207(02)00301-4

HeppellSSCrowderLBampCrouseDT(1996)Modelstoevaluateheadstartingasamanagementtoolforlong-livedturtlesEcological Applications6556ndash565httpsdoiorg1023072269391

HoughPampRobertsonM(2009)MitigationunderSection404oftheCleanWater ActWhere it comes from what it meansWetlands

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Ecology and Management 17 15ndash33 httpsdoiorg101007s11273-008-9093-7

IATTC(2015)Resolution on the conservation of mobulid rays caught in as-sociation with fisheries in the IATTC convention area Inter-AmericanTropical TunaCommission89thAnnualMeetingResolutionC-15-04LaJollaCAInter-AmericanTropicalTunaCommission

IFC(2012)Performance standard 6 Biodiversity conservation and sustain-able management of natural resources January 1 2012WashingtonDCInternationalFinanceCorporation

Innes J Pascoe S Wilcox C Jennings S amp Paredes S (2015)MitigatingundesirableimpactsinthemarineenvironmentAreviewofmarket-basedmanagementmeasuresFrontiers in Marine Science276httpsdoiorg103389fmars201500076

JanniseCSquiresDSeminoffJampDuttonP (2010)Conservationinvestments andmitigationTheCaliforniadrift gillnet fishery andpacificseaturtles InRQGraftonRHilbornDSquiresMTaitampMJWilliams(Eds)Handbook of marine fisheries conservation and management(pp231ndash240)OxfordUKOxfordUniversityPress

Jones E amp FrancisM (2012)Protected rays ndash Occurrence and devel-opment of mitigation methods in the New Zealand tuna purse seine fishery Auckland New Zealand National Institute of Water andAtmosphericResearch

KormosRKormosCFHumleTLanjouwARainerHVicturineR hellipWilliamson E A (2014) Great apes and biodiversity offsetprojectsinAfricaThecasefornationaloffsetstrategiesPLoS ONE9(11)e111671httpsdoiorg101371journalpone0111671

KotchenMJ (2013)Voluntaryand information-basedapproachestoenvironmentalmanagementApubliceconomicsperspectiveReview of Environmental Economics and Policy 7(2) 276ndash295 httpsdoiorg101093reepret012

Kyriazi Z LejanoRMaes FampDegraer S (2015)Bargaining a netgaincompensationagreementbetweenamarinerenewableenergydeveloperandamarineprotectedareamanagerMarine Policy6040ndash48httpsdoiorg101016jmarpol201506005

LentRampSquiresD(2017)ReducingmarinemammalbycatchinglobalfisheriesAneconomicsapproachDeep Sea Research Part II Topical Studies in Oceanography 140 268ndash277 httpsdoiorg101016jdsr2201703005

Lewison R L Crowder L B Read A J amp Freeman S A (2004)Understanding impactsof fisheriesbycatchonmarinemegafaunaTrends in Ecology amp Evolution19598ndash604httpsdoiorg101016jtree200409004

MannC (2015)StrategiesforsustainablepolicydesignConstructiveassessmentofbiodiversityoffsetsandbankingEcosystem Services16266ndash274httpsdoiorg101016jecoser201507001

Marine Stewardship Council (2014 June 21) MSC fisheries certifica-tion requirements v20 [pdf doc] httpswwwmscorgdocumentsscheme-documentsfisheries-certification-scheme-documentsfisheries-certification-requirements-version-20

MaronM IvesCDKujalaHBullJWMaseykFJBekessyShellip Possingham H P (2016) Taming a wicked problem Resolvingcontroversies inbiodiversityoffsettingBioScience66(6)489ndash498httpsdoiorg101093bioscibiw038

MaxwellSLMilner-GullandEJJonesJPKnightATBunnefeldNNunoAhellipRhodesJR(2015)BeingsmartaboutSMARTenvi-ronmentaltargetsScience3471075ndash1076httpsdoiorg101126scienceaaa1451

Moilanen A Van Teeffelen A J Ben-Haim Y amp Ferrier S (2009)Howmuch compensation is enoughA framework for incorporat-inguncertaintyandtimediscountingwhencalculatingoffsetratiosfor impactedhabitatRestoration Ecology17 470ndash478 httpsdoiorg101111j1526-100X200800382x

MorarNToadvineTampBohannanBJ(2015)Biodiversityattwenty-fiveyearsRevolutionorredherringEthics Policy amp Environment1816ndash29httpsdoiorg1010802155008520151018380

OrphanidesCDampPalkaDL(2013)Analysisofharborporpoisegill-netbycatchcomplianceandenforcement trends in theUSnorth-western Atlantic January 1999 to May 2010 Endangered Species Research20251ndash269httpsdoiorg103354esr00499

Pascoe S Innes J Holland D Finas M Theacutebaud O TownsendR hellip Hutton T (2010) Use of incentive-based managementsystems to limit bycatch and discarding International Review of Environmental and Resource Economics 4 123ndash161 httpsdoiorg10156110100000032

PhalanBHayesG Brooks SMarshDHoward PCostelloeBhellip Whitaker S (2017) Avoiding impacts on biodiversity throughstrengthening the first stage of the mitigation hierarchy Oryxhttpsdoiorg101017S0030605316001034

Queacutetier F Regnery B amp Levrel H (2014) No net loss of biodiver-sity or paper offsets A critical review of the French no net losspolicy Environmental Science amp Policy 38 120ndash131 httpsdoiorg101016jenvsci201311009

RadzioTASmolinskyJAampRoosenburgWM(2013)Lowuseofre-quiredterrapinbycatchreductiondevicesinarecreationalcrabpotfisheryHerpetological Conservation and Biology8222ndash227

RaineyHJPollardEHBDutsonGEkstromJMLivingstoneSRTempleHJampPilgrimJD(2015)AreviewofcorporategoalsofnonetlossandnetpositiveimpactonbiodiversityOryx49232ndash238httpsdoiorg101017S0030605313001476

Rausser G C Hamilton S F Kovach M amp Stifter R (2009)UnintendedconsequencesThe spillovereffectsof commonprop-ertyregulationsMarine Policy3324ndash39httpsdoiorg101016jmarpol200803020

Rice J (2014) Evolution of international commitments for fisheriessustainability ICES Journal of Marine Science Journal du Conseil71157ndash165httpsdoiorg101093icesjmsfst078

RichardYampAbrahamER(2013)ApplicationofPotentialBiologicalRemoval methods to seabird populations New Zealand AquaticEnvironmentandBiodiversityReport108

RodeJGoacutemez-BaggethunEampKrauseT(2015)Motivationcrowd-ingbyeconomic incentives inconservationpolicyAreviewoftheempiricalevidenceEcological Economics117270ndash282httpsdoiorg101016jecolecon201411019

RogersAA(2013)SocialwelfareandmarinereservesIswillingnesstopayforconservationdependentonmanagementprocessAdiscretechoiceexperimentoftheNingalooMarineParkinAustraliaCanadian Journal of Agricultural EconomicsRevue Canadienne Drsquoagroeconomie61217ndash238httpsdoiorg101111cjag12008

Rosenberg A A amp McLeod K L (2005) Implementing ecosystem-basedapproachestomanagementfortheconservationofecosystemservicesMarine Ecology Progress Series300 270ndash274 httpsdoiorg103354meps300270

Segerson K (2010) Can voluntary programs reduce sea turtle by-catch Insights from the literature in environmental economics InRQGraftonRHilbornDSquiresMTaitampMJWilliams(Eds)Handbook of marine fisheries conservation and management(pp618ndash629)OxfordUKOxfordUniversityPress

Serafy JECookeS JDiazGAGraves JEHallMShivjiMampSwimmerY(2012)CirclehooksincommercialrecreationalandartisanalfisheriesResearchstatusandneedsforimprovedconser-vation and management Bulletin of Marine Science 88 371ndash391httpsdoiorg105343bms20121038

ShiodeDHu F ShigaM Yokota K amp Tokai T (2005)Midwaterfloatsystemforstandardizinghookdepthsontunalonglinestore-duce sea turtleby-catchFisheries Science71 1182ndash1184httpsdoiorg101111j1444-2906200501080x

Sims M Cox T amp Lewison R (2008) Modeling spatial patternsin fisheries bycatch Improving bycatch maps to aid fisheriesmanagement Ecological Applications 18 649ndash661 httpsdoiorg10189007-06851

emspensp emsp | emsp15MILNER- GULLAND Et AL

Squires D amp Garcia SM (2014) Ecosystem-level impacts of fisheries bycatch on marine megafauna Biodiversity conservation through miti-gation policy economic instruments and technical changeReportofthe IUCN-CEM-FEGScientificworkshopGland Switzerland 7ndash10October2013GlandSwitzerlandIUCN

SquiresDampGarciaSM(inpress)Fisheries bycatch in marine ecosys-tems Policy economic instruments and technical change ChichesterUKJWileyampSons

SwimmerYArauzRMcCrackenMMcNaughtonLBallesteroJMusylMhellipBrillR(2006)DivingbehavioranddelayedmortalityofoliveridleyseaturtlesLepidochelys olivaceaaftertheirreleasefromlongline fishing gearMarine Ecology Progress Series323 253ndash261httpsdoiorg103354meps323253

TolottiMTFilmalterJDBachPTravassosPSeretBampDagornL(2015)BanningisnotenoughThecomplexitiesofoceanicsharkmanagementbytunaregional fisheriesmanagementorganizationsGlobal Ecology and Conservation 4 1ndash7 httpsdoiorg101016jgecco201505003

Tuck G N Polacheck T amp Bulman C M (2003) Spatio-temporaltrendsoflonglinefishingeffortintheSouthernOceanandimplica-tionsforseabirdbycatchBiological Conservation1141ndash27httpsdoiorg101016S0006-3207(02)00378-6

UNEP-WCMC(2016)Marine no net loss A feasibility assessment of imple-menting no net loss of biodiversity in the seaCambridgeUKUnitedNationsEnvironmentProgramme

Vaissiegravere A-C Levrel H Pioch S amp Carlier A (2014) Biodiversityoffsets for offshore wind farm projects The current situation inEurope Marine Policy 48 172ndash183 httpsdoiorg101016jmarpol201403023

Wallace B P Heppell S S Lewison R L Kelez S amp CrowderL B (2008) Impacts of fisheries bycatch on loggerhead tur-tles worldwide inferred from reproductive value analy-ses Journal of Applied Ecology 45 1076ndash1085 httpsdoiorg101111j1365-2664200801507x

Wanless R M Ryan P G Altwegg R Angel A Cooper JCuthbert R amp Hilton G M (2009) From both sides Dire de-mographic consequences of carnivorous mice and longlining for

the critically endangered Tristan albatrosses on Gough IslandBiological Conservation 142 1710ndash1718 httpsdoiorg101016jbiocon200903008

WardP LawrenceEDarbyshireRampHindmarshS (2008) Large-scale experiment shows that nylon leaders reduce shark bycatchandbenefitpelagiclonglinefishersFisheries Research90100ndash108httpsdoiorg101016jfishres200709034

WardTampPhillipsB(2010)SeafoodecolabelingInRQGraftonRHilbornDSquiresMTaitampMJWilliams(Eds)Handbook of ma-rine fisheries conservation and management (pp 608ndash617) OxfordUKOxfordUniversityPress

WilcoxCampDonlanCJ (2007)Compensatorymitigationasasolu-tion to fisheries bycatch-biodiversity conservation conflictsFrontiers in Ecology and the Environment 5 325ndash331 httpsdoiorg1018901540-9295(2007)5[325cmaast]20co2

WilcoxCampDonlanCJ (2009)NeedforaclearandfairevaluationofbiodiversityoffsetsforfisheriesbycatchConservation Biology23770ndash772httpsdoiorg101111j1523-1739200901173x

Wolf SHartlBCarrollCNeelMCampGreenwaldDN (2015)Beyond PVAWhy recovery under the Endangered Species Act ismorethanpopulationviabilityBioScience65200ndash207httpsdoiorg101093bioscibiu218

ZedlerJBampCallawayJC (1999)TrackingwetlandrestorationDomitigation sites follow desired trajectories Restoration Ecology 769ndash73httpsdoiorg101046j1526-100X199907108x

Žydelis R Wallace B P Gilman E L amp Werner T B (2009)Conservation of marine megafauna through minimization of fish-eries bycatch Conservation Biology 23 608ndash616 httpsdoiorg101111j1523-1739200901172x

How to cite this articleMilner-GullandEJGarciaSArlidgeW etalTranslatingtheterrestrialmitigationhierarchytomarinemegafaunaby-catchFish Fish 2018001ndash15 httpsdoiorg101111faf12273

Page 12: Translating the terrestrial mitigation hierarchy to marine ......of marine megafauna by-catch in fisheries, going from defining an overarching goal with an associated quantitative

12emsp |emsp emspensp MILNER- GULLAND Et AL

by-catchmitigationapproachestargetedatdifferentspecies(Serafyetal 2012) Actions to mitigate by-catch for one group of spe-cies can increase or decrease it for others and so a system-wideapproach isneededForexample changing fromJ-hooks tocirclehookstoreducemortalityofturtlesmaydecreaseorincreasesharkmortality(Andrakaetal2013GodinCarlsonampBurgener2012)In terrestrial systems similar interactions arise and value judge-mentsaremade(whetherexplicitlyorimplicitly)astowhatlossandgain of ldquobiodiversityrdquo translates to in operational terms andwhatelementsofbiodiversitymattermosttoimplementers

Uncertainty is high in ocean ecosystems creating both chal-lengesandopportunitiesinapplyingtheconceptofNNLthroughamitigationhierarchythatincludesoffsettingInparticularformarinemegafaunathereishighuncertaintyintheprocesseslinkinganyel-ementofthemitigationhierarchythroughtochangesinpopulationgrowthrateFurthermore impactscanbelong-termhardtomea-sureandspatiallydiffuseanduncertaintyisnotpredictablyspreadthroughthehierarchyThiscreatesadifferentsetofchallengestothosefacedinterrestrialsystemswhereatleastforsometypesofenvironmentalimpactthelinksbetweenactionandimpactarerel-ativelydirectandmeasurableanduncertaintygenerally increasesthroughthemitigationhierarchy (fromavoidthroughminimizere-mediatetooffset)

By-catch reduction measures have had significant successesoverthelastdecadesasaresultofsubstantialinvestmentoftimeand funding by researchers management authorities conserva-tionorganizationsandfishers(Coxetal2007)Howeverthissuc-cessisnotuniversalJustasforanyfisheriesmanagementissueapoorregulatoryregimelimitedcomplianceandlackofinforma-tionhampereffortstoreduceby-catchInsomeplaceshighlevelsofby-catch limitedoptions formitigationandweakgovernance(leadingtopoorenforcement)cancombinetomaketheby-catchproblemintractableOurframeworkwillnotsolvetheseproblemsHowever itbrings together the full rangeofapproaches forby-catchmitigationinastructuredandsystematicwaywhichrequiresatargettobeexpressedagainstwhichoutcomescanbeevaluatedByexposingareasofuncertaintyanddatadeficiencyitcouldchal-lengescientistsandmanagerstoobtainthedatarequiredproperlytoevaluate theeffectivenessofmitigationmeasuresThis couldthensupportandencourageclearerdecision-makingandprioriti-zationofactionsOurframeworkdemonstratesthattheprincipleof implementing thegoalofnonet loss throughamitigationhi-erarchy isasapplicable tomarinemegafaunaby-catchas to ter-restrial systems where it is already widely used in challengingdata-poorcircumstances

There isuntappedpotential forcost-effectiveby-catchmitiga-tionwhichcouldberealizedwiththeadoptionofthisframeworkandwithconsiderationofnewapproachestoincentivizingby-catchmitigationwithinthestepsofthehierarchyApplyingittoafewcase-studiesinpracticewilldemonstrateempiricallywhereandhowthepotentialforimprovedeffectivenesscouldbestberealizedExistinglegalframeworksoftenprecludeapproacheswhichimplicitlyorex-plicitly permit by-catch including the use of economic incentives

ornewapproachessuchasoffsetsHoweverinthiscontextofdy-namicuncertaintythedividendsofthinkingmorecreativelyaboutby-catchmitigationcouldbehigh

ACKNOWLEDG EMENTS

EJMG acknowledges the Pew Charitable Foundation for its sup-port of thiswork This article originated at a 2013workshop co-organized by NOAA-Fisheries and IUCN-CEEM-FEG entitledldquoMultidisciplinaryWorkshoptoAddressEcosystem-LevelImpactsofFisheriesBycatchonMarineMegafaunaBiodiversityConservationthrough Mitigation Policy Economic Instruments and TechnicalChangerdquo We thank the reviewers for their insightful commentswhichmuchimprovedthemanuscript

ORCID

E J Milner-Gulland httporcidorg0000-0003-0324-2710

R E FE R E N C E S

Alfaro-Shigueto J Dutton P H amp Mangel J (2007) Interactionsbetween leatherback turtles and Peruvian artisanal fisher-ies Chelonian Conservation and Biology 6 129ndash134 httpsdoiorg1027441071-8443(2007)6[129ibltap]20co2

Alfaro-Shigueto JMangel JCBernedoFDuttonPHSeminoffJAampGodleyB J (2011) Small-scale fisheriesofPeruAmajorsinkformarineturtles inthePacificJournal of Applied Ecology481432ndash1440httpsdoiorg101111j1365-2664201102040x

Alfaro-ShiguetoJMangelJCPajueloMDuttonPHSeminoffJ A amp Godley B J (2010) Where small can have a large im-pact Structure and characterization of small-scale fisheries inPeru Fisheries Research 106 8ndash17 httpsdoiorg101016jfishres201006004

Andraka SMugM HallM PonsM Pacheco L ParralesM hellipOrtega D (2013) Circle hooks Developing better fishing prac-ticesintheartisanallonglinefisheriesoftheEasternPacificOceanBiological Conservation 160 214ndash224 httpsdoiorg101016jbiocon201301019

ApostolopoulouEampAdamsWM(2017)BiodiversityoffsettingandconservationReframingnaturetosaveitOryx5123ndash31httpsdoiorg101017S0030605315000782

BaacuteezJCRealRGarciacutea-SotoCJoseacuteMMaciacuteasDampCamintildeasJA(2007)Loggerheadturtleby-catchdependsondistancetothecoastindependentoffishingeffortImplicationsforconservationandfish-eries management Marine Ecology Progress Series 338 249ndash256httpsdoiorg101017S0030605315000782

BBOP (2012) Standard on biodiversity offsets Business and biodiversity offsets programmeWashingtonDCForestTrends

Bishop J (2006) Standardizing fishery-dependent catch and ef-fort data in complex fisheries with technology change Reviews in Fish Biology and Fisheries 16 21ndash38 httpsdoiorg101007s11160-006-0004-9

BoyceJ(1996)AneconomicanalysisofthefisheriesbycatchproblemJournal of Environmental Economics and Management31 314ndash336httpsdoiorg101006jeem19960047

BugoniLManciniPLMonteiroDSNascimentoLampNevesTS(2008)SeabirdbycatchintheBrazilianpelagiclonglinefisheryandareviewofcaptureratesinthesouthwesternAtlanticOceanEndangered Species Research5137ndash147httpsdoiorg103354esr00115

emspensp emsp | emsp13MILNER- GULLAND Et AL

BullJWampBrownlieS(2017)Thetransitionfromnonetlosstoanetgainof biodiversity is far from trivialOryx51 53ndash59 httpsdoiorg101017S0030605315000861

BullJWBryantCBakerJampMilner-GullandEJ(2015December28)Developing measuring and communicating the outcomes of cor-porate biodiversity strategies [pdfdocument]RetrievedfromhttpwwwwildbusinessorgBull_etal_2015_WBLpdf

BullJWGordonAWatsonJEampMaronM(2016)Seekingcon-vergenceonthekeyconceptsinlsquononetlossrsquopolicyJournal of Applied Ecology531686ndash1693httpsdoiorg1011111365-266412726

BullJWHardyMJMoilanenAampGordonA (2015)Categoriesof flexibility in biodiversity offsetting and their implications forconservation Biological Conservation 192 522ndash532 httpsdoiorg101016jbiocon201508003

Bull JW Lloyd S P amp StrangeN (2017) Implementation gap be-tween the theory and practice of biodiversity offset multipliersConservation Lettershttpsdoiorg101111conl12335

Bull JW SuttleKBGordonA SinghN JampMilner-Gulland EJ(2013)BiodiversityoffsetsintheoryandpracticeOryx47369ndash380httpsdoiorg101017S003060531200172X

CampbellLMampCornwellML(2008)Humandimensionsofbycatchreduction technology Current assumptions and directions for fu-tureresearchEndangered Species Research5325ndash334httpsdoiorg103354esr00172

Caswell H Brault S Read A J amp Smith T D (1998) Harborporpoise and fisheries An uncertainty analysis of inciden-tal mortality Ecological Applications 8 1226ndash1238 httpsdoiorg1018901051-0761(1998)008[1226hpafau]20co2

ClementsTJohnANielsenKAnDTanSampMilner-GullandEJ (2010)Payments forbiodiversityconservation in thecontextofweak institutions Comparison of three programs from CambodiaEcological Economics 69 1283ndash1291 httpsdoiorg101016jecolecon200911010

CoxTLewisonRŽydelisRCrowderLSafinaCampReadA(2007)ComparingeffectivenessofexperimentalandimplementedbycatchreductionmeasuresTheidealandtherealConservation Biology211155ndash1164httpsdoiorg101111j1523-1739200700772x

CrollDADewarHDulvyNKFernandoDFrancisMPGalvaacuten-Magantildea F hellip Newton K M (2016) Vulnerabilities and fisher-ies impactsTheuncertain futureofmanta anddevil raysAquatic Conservation Marine and Freshwater Ecosystems 26 562ndash575httpsdoiorg101002aqc2591

Damalas D amp Vassilopoulou V (2013) Slack regulation com-pliance in the Mediterranean fisheries A paradigm from theGreek Aegean Sea demersal trawl fishery modelling discardogives Fisheries Management and Ecology 20 21ndash33 httpsdoiorg101111j1365-2400201200860x

DuttonDLDuttonPHChaloupkaMampBoulonRH(2005)IncreaseofaCaribbeanleatherbackturtleDermochelys coriaceanestingpop-ulation linked to long-termnestprotectionBiological Conservation126186ndash194httpsdoiorg101016jbiocon200505013

DuttonPJosephJSquiresDampWilliamsM(2011)Bellagioblue-print foractiononseaturtlesChapter2 InPDuttonDSquiresampM Ahmed (Eds) Conservation of pacific sea turtles (pp 15ndash36)HonoluluHIUniversityofHawaiiPress

DuttonPampSquiresD (2008)AholisticstrategyforPacificseatur-tlerecoveryOcean Development and International Law39200ndash222httpsdoiorg10108000908320802013685

FAO (2011 January 5) International guidelines on bycatch manage-ment and reduction of discards Rome Italy Food and AgricultureOrganisation [pdf document] Retrieved from httpwwwfaoorgdocrephelliptba0022t00pdf

Finkelstein M Bakker V Doak D F Sullivan B Lewison RSatterthwaite W H hellip Henry R W (2008) Evaluating the po-tential effectiveness of compensatory mitigation strategies for

marinebycatchPLoS ONE3 e2480httpsdoiorg101371jour-nalpone0002480

FowlerSJ(2016January5)Draft best practice mitigation guidelines for sharks and rays taken in purse- seine and long-line fisheries Convention on Migratory Species[pdfdocument]RetrievedfromhttpwwwcmsintsitesdefaultfilesdocumentCMS_Sharks_CWG1_Doc_3_2pdf

FrancisMP(2014)Survival and depth distribution of spinetail devilrays (Mobula japanica) released from purse-seine catches NIWA ClientReportNoWLG2014-2WellingtonNewZealandDepartmentofConservation

Fulton E A Smith A D Smith D C amp van Putten I E (2011)Human behaviour The key source of uncertainty in fish-eries management Fish and Fisheries 12 2ndash17 httpsdoiorg101111j1467-2979201000371x

GardnerTAHaseABrownlieSEkstromJMPilgrimJDSavyCEhellipTenKateK(2013)BiodiversityoffsetsandthechallengeofachievingnonetlossConservation Biology271254ndash1264httpsdoiorg101111cobi12118

GjertsenHHallMampSquiresD(2010)IncentivestoaddressbycatchInRAllenJJosephampDSquires(Eds)Conservation and manage-ment of transnational tuna fisheries (pp225ndash250)Ames IAWiley-Blackwellhttpsdoiorg1010029780813820262ch14

Gjertsen H Squires D Dutton P amp Eguchi T (2014) Cost-effectivenessofalternativeconservationstrategieswithapplicationtothePacificLeatherbackTurtleConservation Biology28140ndash149httpsdoiorg101111cobi12239

GodinACCarlson JKampBurgenerV (2012)Theeffectofcirclehooks on shark catchability and at-vessel mortality rates in long-lines fisheriesBulletin of Marine Science88 469ndash483 httpsdoiorg105343bms20111054

GrimmDBarkhornIFestaDBonzonKBoomhowerJHovlandV amp Blau J (2012) Assessing catch sharesrsquo effects evidencefrom Federal United States and associated British Columbianfisheries Marine Policy 36 644ndash657 httpsdoiorg101016jmarpol201110014

HallMA(1996)OnbycatchesReviews in Fish Biology and Fisheries6319ndash352httpsdoiorg101007BF00122585

HallMAAlversonDLampMetuzalsKI(2000)By-catchProblemsand solutions Marine Pollution Bulletin 41 204ndash219 httpsdoiorg101016S0025-326X(00)00111-9

HallMANakanoHClarke S Thomas SMolloy J PeckhamSHhellipHallSJ (2007)Workingwithfisherstoreduceby-catchesIn S J Kenelly (Ed)By-catch reduction in the worldrsquos fisheries (pp235ndash288) Dordrecht The Netherlands Springer httpsdoiorg101007978-1-4020-6078-6_8

HallM amp RomanM (2013)Bycatch and non-tuna catch in the tropi-cal tuna purse seine fisheries of the worldFisheriesandAquacultureTechnicalPaper568RomeItalyFAO

HallMASwimmerYampPargaM(2012)NoldquosilverbulletsrdquobutplentyofoptionsWorkingwiththeeasternpacificartisanalfisherstore-duceseaturtlemortalityinfisheriesInJASeminoffampBWallace(Eds)Sea turtles of the eastern pacific Advances in research and con-servation(pp136ndash153)TucsonAZUniversityofArizonaPress

HamnerRMWadePOremusMStanleyMBrownPConstantineR amp Baker C S (2014) Critically low abundance and limits tohuman-relatedmortalityfortheMauirsquosdolphinEndangered Species Research2687ndash92httpsdoiorg103354esr00621

HatchSA(2003)Statisticalpowerfordetectingtrendswithapplica-tions to seabird monitoringBiological Conservation 111 317ndash329httpsdoiorg101016S0006-3207(02)00301-4

HeppellSSCrowderLBampCrouseDT(1996)Modelstoevaluateheadstartingasamanagementtoolforlong-livedturtlesEcological Applications6556ndash565httpsdoiorg1023072269391

HoughPampRobertsonM(2009)MitigationunderSection404oftheCleanWater ActWhere it comes from what it meansWetlands

14emsp |emsp emspensp MILNER- GULLAND Et AL

Ecology and Management 17 15ndash33 httpsdoiorg101007s11273-008-9093-7

IATTC(2015)Resolution on the conservation of mobulid rays caught in as-sociation with fisheries in the IATTC convention area Inter-AmericanTropical TunaCommission89thAnnualMeetingResolutionC-15-04LaJollaCAInter-AmericanTropicalTunaCommission

IFC(2012)Performance standard 6 Biodiversity conservation and sustain-able management of natural resources January 1 2012WashingtonDCInternationalFinanceCorporation

Innes J Pascoe S Wilcox C Jennings S amp Paredes S (2015)MitigatingundesirableimpactsinthemarineenvironmentAreviewofmarket-basedmanagementmeasuresFrontiers in Marine Science276httpsdoiorg103389fmars201500076

JanniseCSquiresDSeminoffJampDuttonP (2010)Conservationinvestments andmitigationTheCaliforniadrift gillnet fishery andpacificseaturtles InRQGraftonRHilbornDSquiresMTaitampMJWilliams(Eds)Handbook of marine fisheries conservation and management(pp231ndash240)OxfordUKOxfordUniversityPress

Jones E amp FrancisM (2012)Protected rays ndash Occurrence and devel-opment of mitigation methods in the New Zealand tuna purse seine fishery Auckland New Zealand National Institute of Water andAtmosphericResearch

KormosRKormosCFHumleTLanjouwARainerHVicturineR hellipWilliamson E A (2014) Great apes and biodiversity offsetprojectsinAfricaThecasefornationaloffsetstrategiesPLoS ONE9(11)e111671httpsdoiorg101371journalpone0111671

KotchenMJ (2013)Voluntaryand information-basedapproachestoenvironmentalmanagementApubliceconomicsperspectiveReview of Environmental Economics and Policy 7(2) 276ndash295 httpsdoiorg101093reepret012

Kyriazi Z LejanoRMaes FampDegraer S (2015)Bargaining a netgaincompensationagreementbetweenamarinerenewableenergydeveloperandamarineprotectedareamanagerMarine Policy6040ndash48httpsdoiorg101016jmarpol201506005

LentRampSquiresD(2017)ReducingmarinemammalbycatchinglobalfisheriesAneconomicsapproachDeep Sea Research Part II Topical Studies in Oceanography 140 268ndash277 httpsdoiorg101016jdsr2201703005

Lewison R L Crowder L B Read A J amp Freeman S A (2004)Understanding impactsof fisheriesbycatchonmarinemegafaunaTrends in Ecology amp Evolution19598ndash604httpsdoiorg101016jtree200409004

MannC (2015)StrategiesforsustainablepolicydesignConstructiveassessmentofbiodiversityoffsetsandbankingEcosystem Services16266ndash274httpsdoiorg101016jecoser201507001

Marine Stewardship Council (2014 June 21) MSC fisheries certifica-tion requirements v20 [pdf doc] httpswwwmscorgdocumentsscheme-documentsfisheries-certification-scheme-documentsfisheries-certification-requirements-version-20

MaronM IvesCDKujalaHBullJWMaseykFJBekessyShellip Possingham H P (2016) Taming a wicked problem Resolvingcontroversies inbiodiversityoffsettingBioScience66(6)489ndash498httpsdoiorg101093bioscibiw038

MaxwellSLMilner-GullandEJJonesJPKnightATBunnefeldNNunoAhellipRhodesJR(2015)BeingsmartaboutSMARTenvi-ronmentaltargetsScience3471075ndash1076httpsdoiorg101126scienceaaa1451

Moilanen A Van Teeffelen A J Ben-Haim Y amp Ferrier S (2009)Howmuch compensation is enoughA framework for incorporat-inguncertaintyandtimediscountingwhencalculatingoffsetratiosfor impactedhabitatRestoration Ecology17 470ndash478 httpsdoiorg101111j1526-100X200800382x

MorarNToadvineTampBohannanBJ(2015)Biodiversityattwenty-fiveyearsRevolutionorredherringEthics Policy amp Environment1816ndash29httpsdoiorg1010802155008520151018380

OrphanidesCDampPalkaDL(2013)Analysisofharborporpoisegill-netbycatchcomplianceandenforcement trends in theUSnorth-western Atlantic January 1999 to May 2010 Endangered Species Research20251ndash269httpsdoiorg103354esr00499

Pascoe S Innes J Holland D Finas M Theacutebaud O TownsendR hellip Hutton T (2010) Use of incentive-based managementsystems to limit bycatch and discarding International Review of Environmental and Resource Economics 4 123ndash161 httpsdoiorg10156110100000032

PhalanBHayesG Brooks SMarshDHoward PCostelloeBhellip Whitaker S (2017) Avoiding impacts on biodiversity throughstrengthening the first stage of the mitigation hierarchy Oryxhttpsdoiorg101017S0030605316001034

Queacutetier F Regnery B amp Levrel H (2014) No net loss of biodiver-sity or paper offsets A critical review of the French no net losspolicy Environmental Science amp Policy 38 120ndash131 httpsdoiorg101016jenvsci201311009

RadzioTASmolinskyJAampRoosenburgWM(2013)Lowuseofre-quiredterrapinbycatchreductiondevicesinarecreationalcrabpotfisheryHerpetological Conservation and Biology8222ndash227

RaineyHJPollardEHBDutsonGEkstromJMLivingstoneSRTempleHJampPilgrimJD(2015)AreviewofcorporategoalsofnonetlossandnetpositiveimpactonbiodiversityOryx49232ndash238httpsdoiorg101017S0030605313001476

Rausser G C Hamilton S F Kovach M amp Stifter R (2009)UnintendedconsequencesThe spillovereffectsof commonprop-ertyregulationsMarine Policy3324ndash39httpsdoiorg101016jmarpol200803020

Rice J (2014) Evolution of international commitments for fisheriessustainability ICES Journal of Marine Science Journal du Conseil71157ndash165httpsdoiorg101093icesjmsfst078

RichardYampAbrahamER(2013)ApplicationofPotentialBiologicalRemoval methods to seabird populations New Zealand AquaticEnvironmentandBiodiversityReport108

RodeJGoacutemez-BaggethunEampKrauseT(2015)Motivationcrowd-ingbyeconomic incentives inconservationpolicyAreviewoftheempiricalevidenceEcological Economics117270ndash282httpsdoiorg101016jecolecon201411019

RogersAA(2013)SocialwelfareandmarinereservesIswillingnesstopayforconservationdependentonmanagementprocessAdiscretechoiceexperimentoftheNingalooMarineParkinAustraliaCanadian Journal of Agricultural EconomicsRevue Canadienne Drsquoagroeconomie61217ndash238httpsdoiorg101111cjag12008

Rosenberg A A amp McLeod K L (2005) Implementing ecosystem-basedapproachestomanagementfortheconservationofecosystemservicesMarine Ecology Progress Series300 270ndash274 httpsdoiorg103354meps300270

Segerson K (2010) Can voluntary programs reduce sea turtle by-catch Insights from the literature in environmental economics InRQGraftonRHilbornDSquiresMTaitampMJWilliams(Eds)Handbook of marine fisheries conservation and management(pp618ndash629)OxfordUKOxfordUniversityPress

Serafy JECookeS JDiazGAGraves JEHallMShivjiMampSwimmerY(2012)CirclehooksincommercialrecreationalandartisanalfisheriesResearchstatusandneedsforimprovedconser-vation and management Bulletin of Marine Science 88 371ndash391httpsdoiorg105343bms20121038

ShiodeDHu F ShigaM Yokota K amp Tokai T (2005)Midwaterfloatsystemforstandardizinghookdepthsontunalonglinestore-duce sea turtleby-catchFisheries Science71 1182ndash1184httpsdoiorg101111j1444-2906200501080x

Sims M Cox T amp Lewison R (2008) Modeling spatial patternsin fisheries bycatch Improving bycatch maps to aid fisheriesmanagement Ecological Applications 18 649ndash661 httpsdoiorg10189007-06851

emspensp emsp | emsp15MILNER- GULLAND Et AL

Squires D amp Garcia SM (2014) Ecosystem-level impacts of fisheries bycatch on marine megafauna Biodiversity conservation through miti-gation policy economic instruments and technical changeReportofthe IUCN-CEM-FEGScientificworkshopGland Switzerland 7ndash10October2013GlandSwitzerlandIUCN

SquiresDampGarciaSM(inpress)Fisheries bycatch in marine ecosys-tems Policy economic instruments and technical change ChichesterUKJWileyampSons

SwimmerYArauzRMcCrackenMMcNaughtonLBallesteroJMusylMhellipBrillR(2006)DivingbehavioranddelayedmortalityofoliveridleyseaturtlesLepidochelys olivaceaaftertheirreleasefromlongline fishing gearMarine Ecology Progress Series323 253ndash261httpsdoiorg103354meps323253

TolottiMTFilmalterJDBachPTravassosPSeretBampDagornL(2015)BanningisnotenoughThecomplexitiesofoceanicsharkmanagementbytunaregional fisheriesmanagementorganizationsGlobal Ecology and Conservation 4 1ndash7 httpsdoiorg101016jgecco201505003

Tuck G N Polacheck T amp Bulman C M (2003) Spatio-temporaltrendsoflonglinefishingeffortintheSouthernOceanandimplica-tionsforseabirdbycatchBiological Conservation1141ndash27httpsdoiorg101016S0006-3207(02)00378-6

UNEP-WCMC(2016)Marine no net loss A feasibility assessment of imple-menting no net loss of biodiversity in the seaCambridgeUKUnitedNationsEnvironmentProgramme

Vaissiegravere A-C Levrel H Pioch S amp Carlier A (2014) Biodiversityoffsets for offshore wind farm projects The current situation inEurope Marine Policy 48 172ndash183 httpsdoiorg101016jmarpol201403023

Wallace B P Heppell S S Lewison R L Kelez S amp CrowderL B (2008) Impacts of fisheries bycatch on loggerhead tur-tles worldwide inferred from reproductive value analy-ses Journal of Applied Ecology 45 1076ndash1085 httpsdoiorg101111j1365-2664200801507x

Wanless R M Ryan P G Altwegg R Angel A Cooper JCuthbert R amp Hilton G M (2009) From both sides Dire de-mographic consequences of carnivorous mice and longlining for

the critically endangered Tristan albatrosses on Gough IslandBiological Conservation 142 1710ndash1718 httpsdoiorg101016jbiocon200903008

WardP LawrenceEDarbyshireRampHindmarshS (2008) Large-scale experiment shows that nylon leaders reduce shark bycatchandbenefitpelagiclonglinefishersFisheries Research90100ndash108httpsdoiorg101016jfishres200709034

WardTampPhillipsB(2010)SeafoodecolabelingInRQGraftonRHilbornDSquiresMTaitampMJWilliams(Eds)Handbook of ma-rine fisheries conservation and management (pp 608ndash617) OxfordUKOxfordUniversityPress

WilcoxCampDonlanCJ (2007)Compensatorymitigationasasolu-tion to fisheries bycatch-biodiversity conservation conflictsFrontiers in Ecology and the Environment 5 325ndash331 httpsdoiorg1018901540-9295(2007)5[325cmaast]20co2

WilcoxCampDonlanCJ (2009)NeedforaclearandfairevaluationofbiodiversityoffsetsforfisheriesbycatchConservation Biology23770ndash772httpsdoiorg101111j1523-1739200901173x

Wolf SHartlBCarrollCNeelMCampGreenwaldDN (2015)Beyond PVAWhy recovery under the Endangered Species Act ismorethanpopulationviabilityBioScience65200ndash207httpsdoiorg101093bioscibiu218

ZedlerJBampCallawayJC (1999)TrackingwetlandrestorationDomitigation sites follow desired trajectories Restoration Ecology 769ndash73httpsdoiorg101046j1526-100X199907108x

Žydelis R Wallace B P Gilman E L amp Werner T B (2009)Conservation of marine megafauna through minimization of fish-eries bycatch Conservation Biology 23 608ndash616 httpsdoiorg101111j1523-1739200901172x

How to cite this articleMilner-GullandEJGarciaSArlidgeW etalTranslatingtheterrestrialmitigationhierarchytomarinemegafaunaby-catchFish Fish 2018001ndash15 httpsdoiorg101111faf12273

Page 13: Translating the terrestrial mitigation hierarchy to marine ......of marine megafauna by-catch in fisheries, going from defining an overarching goal with an associated quantitative

emspensp emsp | emsp13MILNER- GULLAND Et AL

BullJWampBrownlieS(2017)Thetransitionfromnonetlosstoanetgainof biodiversity is far from trivialOryx51 53ndash59 httpsdoiorg101017S0030605315000861

BullJWBryantCBakerJampMilner-GullandEJ(2015December28)Developing measuring and communicating the outcomes of cor-porate biodiversity strategies [pdfdocument]RetrievedfromhttpwwwwildbusinessorgBull_etal_2015_WBLpdf

BullJWGordonAWatsonJEampMaronM(2016)Seekingcon-vergenceonthekeyconceptsinlsquononetlossrsquopolicyJournal of Applied Ecology531686ndash1693httpsdoiorg1011111365-266412726

BullJWHardyMJMoilanenAampGordonA (2015)Categoriesof flexibility in biodiversity offsetting and their implications forconservation Biological Conservation 192 522ndash532 httpsdoiorg101016jbiocon201508003

Bull JW Lloyd S P amp StrangeN (2017) Implementation gap be-tween the theory and practice of biodiversity offset multipliersConservation Lettershttpsdoiorg101111conl12335

Bull JW SuttleKBGordonA SinghN JampMilner-Gulland EJ(2013)BiodiversityoffsetsintheoryandpracticeOryx47369ndash380httpsdoiorg101017S003060531200172X

CampbellLMampCornwellML(2008)Humandimensionsofbycatchreduction technology Current assumptions and directions for fu-tureresearchEndangered Species Research5325ndash334httpsdoiorg103354esr00172

Caswell H Brault S Read A J amp Smith T D (1998) Harborporpoise and fisheries An uncertainty analysis of inciden-tal mortality Ecological Applications 8 1226ndash1238 httpsdoiorg1018901051-0761(1998)008[1226hpafau]20co2

ClementsTJohnANielsenKAnDTanSampMilner-GullandEJ (2010)Payments forbiodiversityconservation in thecontextofweak institutions Comparison of three programs from CambodiaEcological Economics 69 1283ndash1291 httpsdoiorg101016jecolecon200911010

CoxTLewisonRŽydelisRCrowderLSafinaCampReadA(2007)ComparingeffectivenessofexperimentalandimplementedbycatchreductionmeasuresTheidealandtherealConservation Biology211155ndash1164httpsdoiorg101111j1523-1739200700772x

CrollDADewarHDulvyNKFernandoDFrancisMPGalvaacuten-Magantildea F hellip Newton K M (2016) Vulnerabilities and fisher-ies impactsTheuncertain futureofmanta anddevil raysAquatic Conservation Marine and Freshwater Ecosystems 26 562ndash575httpsdoiorg101002aqc2591

Damalas D amp Vassilopoulou V (2013) Slack regulation com-pliance in the Mediterranean fisheries A paradigm from theGreek Aegean Sea demersal trawl fishery modelling discardogives Fisheries Management and Ecology 20 21ndash33 httpsdoiorg101111j1365-2400201200860x

DuttonDLDuttonPHChaloupkaMampBoulonRH(2005)IncreaseofaCaribbeanleatherbackturtleDermochelys coriaceanestingpop-ulation linked to long-termnestprotectionBiological Conservation126186ndash194httpsdoiorg101016jbiocon200505013

DuttonPJosephJSquiresDampWilliamsM(2011)Bellagioblue-print foractiononseaturtlesChapter2 InPDuttonDSquiresampM Ahmed (Eds) Conservation of pacific sea turtles (pp 15ndash36)HonoluluHIUniversityofHawaiiPress

DuttonPampSquiresD (2008)AholisticstrategyforPacificseatur-tlerecoveryOcean Development and International Law39200ndash222httpsdoiorg10108000908320802013685

FAO (2011 January 5) International guidelines on bycatch manage-ment and reduction of discards Rome Italy Food and AgricultureOrganisation [pdf document] Retrieved from httpwwwfaoorgdocrephelliptba0022t00pdf

Finkelstein M Bakker V Doak D F Sullivan B Lewison RSatterthwaite W H hellip Henry R W (2008) Evaluating the po-tential effectiveness of compensatory mitigation strategies for

marinebycatchPLoS ONE3 e2480httpsdoiorg101371jour-nalpone0002480

FowlerSJ(2016January5)Draft best practice mitigation guidelines for sharks and rays taken in purse- seine and long-line fisheries Convention on Migratory Species[pdfdocument]RetrievedfromhttpwwwcmsintsitesdefaultfilesdocumentCMS_Sharks_CWG1_Doc_3_2pdf

FrancisMP(2014)Survival and depth distribution of spinetail devilrays (Mobula japanica) released from purse-seine catches NIWA ClientReportNoWLG2014-2WellingtonNewZealandDepartmentofConservation

Fulton E A Smith A D Smith D C amp van Putten I E (2011)Human behaviour The key source of uncertainty in fish-eries management Fish and Fisheries 12 2ndash17 httpsdoiorg101111j1467-2979201000371x

GardnerTAHaseABrownlieSEkstromJMPilgrimJDSavyCEhellipTenKateK(2013)BiodiversityoffsetsandthechallengeofachievingnonetlossConservation Biology271254ndash1264httpsdoiorg101111cobi12118

GjertsenHHallMampSquiresD(2010)IncentivestoaddressbycatchInRAllenJJosephampDSquires(Eds)Conservation and manage-ment of transnational tuna fisheries (pp225ndash250)Ames IAWiley-Blackwellhttpsdoiorg1010029780813820262ch14

Gjertsen H Squires D Dutton P amp Eguchi T (2014) Cost-effectivenessofalternativeconservationstrategieswithapplicationtothePacificLeatherbackTurtleConservation Biology28140ndash149httpsdoiorg101111cobi12239

GodinACCarlson JKampBurgenerV (2012)Theeffectofcirclehooks on shark catchability and at-vessel mortality rates in long-lines fisheriesBulletin of Marine Science88 469ndash483 httpsdoiorg105343bms20111054

GrimmDBarkhornIFestaDBonzonKBoomhowerJHovlandV amp Blau J (2012) Assessing catch sharesrsquo effects evidencefrom Federal United States and associated British Columbianfisheries Marine Policy 36 644ndash657 httpsdoiorg101016jmarpol201110014

HallMA(1996)OnbycatchesReviews in Fish Biology and Fisheries6319ndash352httpsdoiorg101007BF00122585

HallMAAlversonDLampMetuzalsKI(2000)By-catchProblemsand solutions Marine Pollution Bulletin 41 204ndash219 httpsdoiorg101016S0025-326X(00)00111-9

HallMANakanoHClarke S Thomas SMolloy J PeckhamSHhellipHallSJ (2007)Workingwithfisherstoreduceby-catchesIn S J Kenelly (Ed)By-catch reduction in the worldrsquos fisheries (pp235ndash288) Dordrecht The Netherlands Springer httpsdoiorg101007978-1-4020-6078-6_8

HallM amp RomanM (2013)Bycatch and non-tuna catch in the tropi-cal tuna purse seine fisheries of the worldFisheriesandAquacultureTechnicalPaper568RomeItalyFAO

HallMASwimmerYampPargaM(2012)NoldquosilverbulletsrdquobutplentyofoptionsWorkingwiththeeasternpacificartisanalfisherstore-duceseaturtlemortalityinfisheriesInJASeminoffampBWallace(Eds)Sea turtles of the eastern pacific Advances in research and con-servation(pp136ndash153)TucsonAZUniversityofArizonaPress

HamnerRMWadePOremusMStanleyMBrownPConstantineR amp Baker C S (2014) Critically low abundance and limits tohuman-relatedmortalityfortheMauirsquosdolphinEndangered Species Research2687ndash92httpsdoiorg103354esr00621

HatchSA(2003)Statisticalpowerfordetectingtrendswithapplica-tions to seabird monitoringBiological Conservation 111 317ndash329httpsdoiorg101016S0006-3207(02)00301-4

HeppellSSCrowderLBampCrouseDT(1996)Modelstoevaluateheadstartingasamanagementtoolforlong-livedturtlesEcological Applications6556ndash565httpsdoiorg1023072269391

HoughPampRobertsonM(2009)MitigationunderSection404oftheCleanWater ActWhere it comes from what it meansWetlands

14emsp |emsp emspensp MILNER- GULLAND Et AL

Ecology and Management 17 15ndash33 httpsdoiorg101007s11273-008-9093-7

IATTC(2015)Resolution on the conservation of mobulid rays caught in as-sociation with fisheries in the IATTC convention area Inter-AmericanTropical TunaCommission89thAnnualMeetingResolutionC-15-04LaJollaCAInter-AmericanTropicalTunaCommission

IFC(2012)Performance standard 6 Biodiversity conservation and sustain-able management of natural resources January 1 2012WashingtonDCInternationalFinanceCorporation

Innes J Pascoe S Wilcox C Jennings S amp Paredes S (2015)MitigatingundesirableimpactsinthemarineenvironmentAreviewofmarket-basedmanagementmeasuresFrontiers in Marine Science276httpsdoiorg103389fmars201500076

JanniseCSquiresDSeminoffJampDuttonP (2010)Conservationinvestments andmitigationTheCaliforniadrift gillnet fishery andpacificseaturtles InRQGraftonRHilbornDSquiresMTaitampMJWilliams(Eds)Handbook of marine fisheries conservation and management(pp231ndash240)OxfordUKOxfordUniversityPress

Jones E amp FrancisM (2012)Protected rays ndash Occurrence and devel-opment of mitigation methods in the New Zealand tuna purse seine fishery Auckland New Zealand National Institute of Water andAtmosphericResearch

KormosRKormosCFHumleTLanjouwARainerHVicturineR hellipWilliamson E A (2014) Great apes and biodiversity offsetprojectsinAfricaThecasefornationaloffsetstrategiesPLoS ONE9(11)e111671httpsdoiorg101371journalpone0111671

KotchenMJ (2013)Voluntaryand information-basedapproachestoenvironmentalmanagementApubliceconomicsperspectiveReview of Environmental Economics and Policy 7(2) 276ndash295 httpsdoiorg101093reepret012

Kyriazi Z LejanoRMaes FampDegraer S (2015)Bargaining a netgaincompensationagreementbetweenamarinerenewableenergydeveloperandamarineprotectedareamanagerMarine Policy6040ndash48httpsdoiorg101016jmarpol201506005

LentRampSquiresD(2017)ReducingmarinemammalbycatchinglobalfisheriesAneconomicsapproachDeep Sea Research Part II Topical Studies in Oceanography 140 268ndash277 httpsdoiorg101016jdsr2201703005

Lewison R L Crowder L B Read A J amp Freeman S A (2004)Understanding impactsof fisheriesbycatchonmarinemegafaunaTrends in Ecology amp Evolution19598ndash604httpsdoiorg101016jtree200409004

MannC (2015)StrategiesforsustainablepolicydesignConstructiveassessmentofbiodiversityoffsetsandbankingEcosystem Services16266ndash274httpsdoiorg101016jecoser201507001

Marine Stewardship Council (2014 June 21) MSC fisheries certifica-tion requirements v20 [pdf doc] httpswwwmscorgdocumentsscheme-documentsfisheries-certification-scheme-documentsfisheries-certification-requirements-version-20

MaronM IvesCDKujalaHBullJWMaseykFJBekessyShellip Possingham H P (2016) Taming a wicked problem Resolvingcontroversies inbiodiversityoffsettingBioScience66(6)489ndash498httpsdoiorg101093bioscibiw038

MaxwellSLMilner-GullandEJJonesJPKnightATBunnefeldNNunoAhellipRhodesJR(2015)BeingsmartaboutSMARTenvi-ronmentaltargetsScience3471075ndash1076httpsdoiorg101126scienceaaa1451

Moilanen A Van Teeffelen A J Ben-Haim Y amp Ferrier S (2009)Howmuch compensation is enoughA framework for incorporat-inguncertaintyandtimediscountingwhencalculatingoffsetratiosfor impactedhabitatRestoration Ecology17 470ndash478 httpsdoiorg101111j1526-100X200800382x

MorarNToadvineTampBohannanBJ(2015)Biodiversityattwenty-fiveyearsRevolutionorredherringEthics Policy amp Environment1816ndash29httpsdoiorg1010802155008520151018380

OrphanidesCDampPalkaDL(2013)Analysisofharborporpoisegill-netbycatchcomplianceandenforcement trends in theUSnorth-western Atlantic January 1999 to May 2010 Endangered Species Research20251ndash269httpsdoiorg103354esr00499

Pascoe S Innes J Holland D Finas M Theacutebaud O TownsendR hellip Hutton T (2010) Use of incentive-based managementsystems to limit bycatch and discarding International Review of Environmental and Resource Economics 4 123ndash161 httpsdoiorg10156110100000032

PhalanBHayesG Brooks SMarshDHoward PCostelloeBhellip Whitaker S (2017) Avoiding impacts on biodiversity throughstrengthening the first stage of the mitigation hierarchy Oryxhttpsdoiorg101017S0030605316001034

Queacutetier F Regnery B amp Levrel H (2014) No net loss of biodiver-sity or paper offsets A critical review of the French no net losspolicy Environmental Science amp Policy 38 120ndash131 httpsdoiorg101016jenvsci201311009

RadzioTASmolinskyJAampRoosenburgWM(2013)Lowuseofre-quiredterrapinbycatchreductiondevicesinarecreationalcrabpotfisheryHerpetological Conservation and Biology8222ndash227

RaineyHJPollardEHBDutsonGEkstromJMLivingstoneSRTempleHJampPilgrimJD(2015)AreviewofcorporategoalsofnonetlossandnetpositiveimpactonbiodiversityOryx49232ndash238httpsdoiorg101017S0030605313001476

Rausser G C Hamilton S F Kovach M amp Stifter R (2009)UnintendedconsequencesThe spillovereffectsof commonprop-ertyregulationsMarine Policy3324ndash39httpsdoiorg101016jmarpol200803020

Rice J (2014) Evolution of international commitments for fisheriessustainability ICES Journal of Marine Science Journal du Conseil71157ndash165httpsdoiorg101093icesjmsfst078

RichardYampAbrahamER(2013)ApplicationofPotentialBiologicalRemoval methods to seabird populations New Zealand AquaticEnvironmentandBiodiversityReport108

RodeJGoacutemez-BaggethunEampKrauseT(2015)Motivationcrowd-ingbyeconomic incentives inconservationpolicyAreviewoftheempiricalevidenceEcological Economics117270ndash282httpsdoiorg101016jecolecon201411019

RogersAA(2013)SocialwelfareandmarinereservesIswillingnesstopayforconservationdependentonmanagementprocessAdiscretechoiceexperimentoftheNingalooMarineParkinAustraliaCanadian Journal of Agricultural EconomicsRevue Canadienne Drsquoagroeconomie61217ndash238httpsdoiorg101111cjag12008

Rosenberg A A amp McLeod K L (2005) Implementing ecosystem-basedapproachestomanagementfortheconservationofecosystemservicesMarine Ecology Progress Series300 270ndash274 httpsdoiorg103354meps300270

Segerson K (2010) Can voluntary programs reduce sea turtle by-catch Insights from the literature in environmental economics InRQGraftonRHilbornDSquiresMTaitampMJWilliams(Eds)Handbook of marine fisheries conservation and management(pp618ndash629)OxfordUKOxfordUniversityPress

Serafy JECookeS JDiazGAGraves JEHallMShivjiMampSwimmerY(2012)CirclehooksincommercialrecreationalandartisanalfisheriesResearchstatusandneedsforimprovedconser-vation and management Bulletin of Marine Science 88 371ndash391httpsdoiorg105343bms20121038

ShiodeDHu F ShigaM Yokota K amp Tokai T (2005)Midwaterfloatsystemforstandardizinghookdepthsontunalonglinestore-duce sea turtleby-catchFisheries Science71 1182ndash1184httpsdoiorg101111j1444-2906200501080x

Sims M Cox T amp Lewison R (2008) Modeling spatial patternsin fisheries bycatch Improving bycatch maps to aid fisheriesmanagement Ecological Applications 18 649ndash661 httpsdoiorg10189007-06851

emspensp emsp | emsp15MILNER- GULLAND Et AL

Squires D amp Garcia SM (2014) Ecosystem-level impacts of fisheries bycatch on marine megafauna Biodiversity conservation through miti-gation policy economic instruments and technical changeReportofthe IUCN-CEM-FEGScientificworkshopGland Switzerland 7ndash10October2013GlandSwitzerlandIUCN

SquiresDampGarciaSM(inpress)Fisheries bycatch in marine ecosys-tems Policy economic instruments and technical change ChichesterUKJWileyampSons

SwimmerYArauzRMcCrackenMMcNaughtonLBallesteroJMusylMhellipBrillR(2006)DivingbehavioranddelayedmortalityofoliveridleyseaturtlesLepidochelys olivaceaaftertheirreleasefromlongline fishing gearMarine Ecology Progress Series323 253ndash261httpsdoiorg103354meps323253

TolottiMTFilmalterJDBachPTravassosPSeretBampDagornL(2015)BanningisnotenoughThecomplexitiesofoceanicsharkmanagementbytunaregional fisheriesmanagementorganizationsGlobal Ecology and Conservation 4 1ndash7 httpsdoiorg101016jgecco201505003

Tuck G N Polacheck T amp Bulman C M (2003) Spatio-temporaltrendsoflonglinefishingeffortintheSouthernOceanandimplica-tionsforseabirdbycatchBiological Conservation1141ndash27httpsdoiorg101016S0006-3207(02)00378-6

UNEP-WCMC(2016)Marine no net loss A feasibility assessment of imple-menting no net loss of biodiversity in the seaCambridgeUKUnitedNationsEnvironmentProgramme

Vaissiegravere A-C Levrel H Pioch S amp Carlier A (2014) Biodiversityoffsets for offshore wind farm projects The current situation inEurope Marine Policy 48 172ndash183 httpsdoiorg101016jmarpol201403023

Wallace B P Heppell S S Lewison R L Kelez S amp CrowderL B (2008) Impacts of fisheries bycatch on loggerhead tur-tles worldwide inferred from reproductive value analy-ses Journal of Applied Ecology 45 1076ndash1085 httpsdoiorg101111j1365-2664200801507x

Wanless R M Ryan P G Altwegg R Angel A Cooper JCuthbert R amp Hilton G M (2009) From both sides Dire de-mographic consequences of carnivorous mice and longlining for

the critically endangered Tristan albatrosses on Gough IslandBiological Conservation 142 1710ndash1718 httpsdoiorg101016jbiocon200903008

WardP LawrenceEDarbyshireRampHindmarshS (2008) Large-scale experiment shows that nylon leaders reduce shark bycatchandbenefitpelagiclonglinefishersFisheries Research90100ndash108httpsdoiorg101016jfishres200709034

WardTampPhillipsB(2010)SeafoodecolabelingInRQGraftonRHilbornDSquiresMTaitampMJWilliams(Eds)Handbook of ma-rine fisheries conservation and management (pp 608ndash617) OxfordUKOxfordUniversityPress

WilcoxCampDonlanCJ (2007)Compensatorymitigationasasolu-tion to fisheries bycatch-biodiversity conservation conflictsFrontiers in Ecology and the Environment 5 325ndash331 httpsdoiorg1018901540-9295(2007)5[325cmaast]20co2

WilcoxCampDonlanCJ (2009)NeedforaclearandfairevaluationofbiodiversityoffsetsforfisheriesbycatchConservation Biology23770ndash772httpsdoiorg101111j1523-1739200901173x

Wolf SHartlBCarrollCNeelMCampGreenwaldDN (2015)Beyond PVAWhy recovery under the Endangered Species Act ismorethanpopulationviabilityBioScience65200ndash207httpsdoiorg101093bioscibiu218

ZedlerJBampCallawayJC (1999)TrackingwetlandrestorationDomitigation sites follow desired trajectories Restoration Ecology 769ndash73httpsdoiorg101046j1526-100X199907108x

Žydelis R Wallace B P Gilman E L amp Werner T B (2009)Conservation of marine megafauna through minimization of fish-eries bycatch Conservation Biology 23 608ndash616 httpsdoiorg101111j1523-1739200901172x

How to cite this articleMilner-GullandEJGarciaSArlidgeW etalTranslatingtheterrestrialmitigationhierarchytomarinemegafaunaby-catchFish Fish 2018001ndash15 httpsdoiorg101111faf12273

Page 14: Translating the terrestrial mitigation hierarchy to marine ......of marine megafauna by-catch in fisheries, going from defining an overarching goal with an associated quantitative

14emsp |emsp emspensp MILNER- GULLAND Et AL

Ecology and Management 17 15ndash33 httpsdoiorg101007s11273-008-9093-7

IATTC(2015)Resolution on the conservation of mobulid rays caught in as-sociation with fisheries in the IATTC convention area Inter-AmericanTropical TunaCommission89thAnnualMeetingResolutionC-15-04LaJollaCAInter-AmericanTropicalTunaCommission

IFC(2012)Performance standard 6 Biodiversity conservation and sustain-able management of natural resources January 1 2012WashingtonDCInternationalFinanceCorporation

Innes J Pascoe S Wilcox C Jennings S amp Paredes S (2015)MitigatingundesirableimpactsinthemarineenvironmentAreviewofmarket-basedmanagementmeasuresFrontiers in Marine Science276httpsdoiorg103389fmars201500076

JanniseCSquiresDSeminoffJampDuttonP (2010)Conservationinvestments andmitigationTheCaliforniadrift gillnet fishery andpacificseaturtles InRQGraftonRHilbornDSquiresMTaitampMJWilliams(Eds)Handbook of marine fisheries conservation and management(pp231ndash240)OxfordUKOxfordUniversityPress

Jones E amp FrancisM (2012)Protected rays ndash Occurrence and devel-opment of mitigation methods in the New Zealand tuna purse seine fishery Auckland New Zealand National Institute of Water andAtmosphericResearch

KormosRKormosCFHumleTLanjouwARainerHVicturineR hellipWilliamson E A (2014) Great apes and biodiversity offsetprojectsinAfricaThecasefornationaloffsetstrategiesPLoS ONE9(11)e111671httpsdoiorg101371journalpone0111671

KotchenMJ (2013)Voluntaryand information-basedapproachestoenvironmentalmanagementApubliceconomicsperspectiveReview of Environmental Economics and Policy 7(2) 276ndash295 httpsdoiorg101093reepret012

Kyriazi Z LejanoRMaes FampDegraer S (2015)Bargaining a netgaincompensationagreementbetweenamarinerenewableenergydeveloperandamarineprotectedareamanagerMarine Policy6040ndash48httpsdoiorg101016jmarpol201506005

LentRampSquiresD(2017)ReducingmarinemammalbycatchinglobalfisheriesAneconomicsapproachDeep Sea Research Part II Topical Studies in Oceanography 140 268ndash277 httpsdoiorg101016jdsr2201703005

Lewison R L Crowder L B Read A J amp Freeman S A (2004)Understanding impactsof fisheriesbycatchonmarinemegafaunaTrends in Ecology amp Evolution19598ndash604httpsdoiorg101016jtree200409004

MannC (2015)StrategiesforsustainablepolicydesignConstructiveassessmentofbiodiversityoffsetsandbankingEcosystem Services16266ndash274httpsdoiorg101016jecoser201507001

Marine Stewardship Council (2014 June 21) MSC fisheries certifica-tion requirements v20 [pdf doc] httpswwwmscorgdocumentsscheme-documentsfisheries-certification-scheme-documentsfisheries-certification-requirements-version-20

MaronM IvesCDKujalaHBullJWMaseykFJBekessyShellip Possingham H P (2016) Taming a wicked problem Resolvingcontroversies inbiodiversityoffsettingBioScience66(6)489ndash498httpsdoiorg101093bioscibiw038

MaxwellSLMilner-GullandEJJonesJPKnightATBunnefeldNNunoAhellipRhodesJR(2015)BeingsmartaboutSMARTenvi-ronmentaltargetsScience3471075ndash1076httpsdoiorg101126scienceaaa1451

Moilanen A Van Teeffelen A J Ben-Haim Y amp Ferrier S (2009)Howmuch compensation is enoughA framework for incorporat-inguncertaintyandtimediscountingwhencalculatingoffsetratiosfor impactedhabitatRestoration Ecology17 470ndash478 httpsdoiorg101111j1526-100X200800382x

MorarNToadvineTampBohannanBJ(2015)Biodiversityattwenty-fiveyearsRevolutionorredherringEthics Policy amp Environment1816ndash29httpsdoiorg1010802155008520151018380

OrphanidesCDampPalkaDL(2013)Analysisofharborporpoisegill-netbycatchcomplianceandenforcement trends in theUSnorth-western Atlantic January 1999 to May 2010 Endangered Species Research20251ndash269httpsdoiorg103354esr00499

Pascoe S Innes J Holland D Finas M Theacutebaud O TownsendR hellip Hutton T (2010) Use of incentive-based managementsystems to limit bycatch and discarding International Review of Environmental and Resource Economics 4 123ndash161 httpsdoiorg10156110100000032

PhalanBHayesG Brooks SMarshDHoward PCostelloeBhellip Whitaker S (2017) Avoiding impacts on biodiversity throughstrengthening the first stage of the mitigation hierarchy Oryxhttpsdoiorg101017S0030605316001034

Queacutetier F Regnery B amp Levrel H (2014) No net loss of biodiver-sity or paper offsets A critical review of the French no net losspolicy Environmental Science amp Policy 38 120ndash131 httpsdoiorg101016jenvsci201311009

RadzioTASmolinskyJAampRoosenburgWM(2013)Lowuseofre-quiredterrapinbycatchreductiondevicesinarecreationalcrabpotfisheryHerpetological Conservation and Biology8222ndash227

RaineyHJPollardEHBDutsonGEkstromJMLivingstoneSRTempleHJampPilgrimJD(2015)AreviewofcorporategoalsofnonetlossandnetpositiveimpactonbiodiversityOryx49232ndash238httpsdoiorg101017S0030605313001476

Rausser G C Hamilton S F Kovach M amp Stifter R (2009)UnintendedconsequencesThe spillovereffectsof commonprop-ertyregulationsMarine Policy3324ndash39httpsdoiorg101016jmarpol200803020

Rice J (2014) Evolution of international commitments for fisheriessustainability ICES Journal of Marine Science Journal du Conseil71157ndash165httpsdoiorg101093icesjmsfst078

RichardYampAbrahamER(2013)ApplicationofPotentialBiologicalRemoval methods to seabird populations New Zealand AquaticEnvironmentandBiodiversityReport108

RodeJGoacutemez-BaggethunEampKrauseT(2015)Motivationcrowd-ingbyeconomic incentives inconservationpolicyAreviewoftheempiricalevidenceEcological Economics117270ndash282httpsdoiorg101016jecolecon201411019

RogersAA(2013)SocialwelfareandmarinereservesIswillingnesstopayforconservationdependentonmanagementprocessAdiscretechoiceexperimentoftheNingalooMarineParkinAustraliaCanadian Journal of Agricultural EconomicsRevue Canadienne Drsquoagroeconomie61217ndash238httpsdoiorg101111cjag12008

Rosenberg A A amp McLeod K L (2005) Implementing ecosystem-basedapproachestomanagementfortheconservationofecosystemservicesMarine Ecology Progress Series300 270ndash274 httpsdoiorg103354meps300270

Segerson K (2010) Can voluntary programs reduce sea turtle by-catch Insights from the literature in environmental economics InRQGraftonRHilbornDSquiresMTaitampMJWilliams(Eds)Handbook of marine fisheries conservation and management(pp618ndash629)OxfordUKOxfordUniversityPress

Serafy JECookeS JDiazGAGraves JEHallMShivjiMampSwimmerY(2012)CirclehooksincommercialrecreationalandartisanalfisheriesResearchstatusandneedsforimprovedconser-vation and management Bulletin of Marine Science 88 371ndash391httpsdoiorg105343bms20121038

ShiodeDHu F ShigaM Yokota K amp Tokai T (2005)Midwaterfloatsystemforstandardizinghookdepthsontunalonglinestore-duce sea turtleby-catchFisheries Science71 1182ndash1184httpsdoiorg101111j1444-2906200501080x

Sims M Cox T amp Lewison R (2008) Modeling spatial patternsin fisheries bycatch Improving bycatch maps to aid fisheriesmanagement Ecological Applications 18 649ndash661 httpsdoiorg10189007-06851

emspensp emsp | emsp15MILNER- GULLAND Et AL

Squires D amp Garcia SM (2014) Ecosystem-level impacts of fisheries bycatch on marine megafauna Biodiversity conservation through miti-gation policy economic instruments and technical changeReportofthe IUCN-CEM-FEGScientificworkshopGland Switzerland 7ndash10October2013GlandSwitzerlandIUCN

SquiresDampGarciaSM(inpress)Fisheries bycatch in marine ecosys-tems Policy economic instruments and technical change ChichesterUKJWileyampSons

SwimmerYArauzRMcCrackenMMcNaughtonLBallesteroJMusylMhellipBrillR(2006)DivingbehavioranddelayedmortalityofoliveridleyseaturtlesLepidochelys olivaceaaftertheirreleasefromlongline fishing gearMarine Ecology Progress Series323 253ndash261httpsdoiorg103354meps323253

TolottiMTFilmalterJDBachPTravassosPSeretBampDagornL(2015)BanningisnotenoughThecomplexitiesofoceanicsharkmanagementbytunaregional fisheriesmanagementorganizationsGlobal Ecology and Conservation 4 1ndash7 httpsdoiorg101016jgecco201505003

Tuck G N Polacheck T amp Bulman C M (2003) Spatio-temporaltrendsoflonglinefishingeffortintheSouthernOceanandimplica-tionsforseabirdbycatchBiological Conservation1141ndash27httpsdoiorg101016S0006-3207(02)00378-6

UNEP-WCMC(2016)Marine no net loss A feasibility assessment of imple-menting no net loss of biodiversity in the seaCambridgeUKUnitedNationsEnvironmentProgramme

Vaissiegravere A-C Levrel H Pioch S amp Carlier A (2014) Biodiversityoffsets for offshore wind farm projects The current situation inEurope Marine Policy 48 172ndash183 httpsdoiorg101016jmarpol201403023

Wallace B P Heppell S S Lewison R L Kelez S amp CrowderL B (2008) Impacts of fisheries bycatch on loggerhead tur-tles worldwide inferred from reproductive value analy-ses Journal of Applied Ecology 45 1076ndash1085 httpsdoiorg101111j1365-2664200801507x

Wanless R M Ryan P G Altwegg R Angel A Cooper JCuthbert R amp Hilton G M (2009) From both sides Dire de-mographic consequences of carnivorous mice and longlining for

the critically endangered Tristan albatrosses on Gough IslandBiological Conservation 142 1710ndash1718 httpsdoiorg101016jbiocon200903008

WardP LawrenceEDarbyshireRampHindmarshS (2008) Large-scale experiment shows that nylon leaders reduce shark bycatchandbenefitpelagiclonglinefishersFisheries Research90100ndash108httpsdoiorg101016jfishres200709034

WardTampPhillipsB(2010)SeafoodecolabelingInRQGraftonRHilbornDSquiresMTaitampMJWilliams(Eds)Handbook of ma-rine fisheries conservation and management (pp 608ndash617) OxfordUKOxfordUniversityPress

WilcoxCampDonlanCJ (2007)Compensatorymitigationasasolu-tion to fisheries bycatch-biodiversity conservation conflictsFrontiers in Ecology and the Environment 5 325ndash331 httpsdoiorg1018901540-9295(2007)5[325cmaast]20co2

WilcoxCampDonlanCJ (2009)NeedforaclearandfairevaluationofbiodiversityoffsetsforfisheriesbycatchConservation Biology23770ndash772httpsdoiorg101111j1523-1739200901173x

Wolf SHartlBCarrollCNeelMCampGreenwaldDN (2015)Beyond PVAWhy recovery under the Endangered Species Act ismorethanpopulationviabilityBioScience65200ndash207httpsdoiorg101093bioscibiu218

ZedlerJBampCallawayJC (1999)TrackingwetlandrestorationDomitigation sites follow desired trajectories Restoration Ecology 769ndash73httpsdoiorg101046j1526-100X199907108x

Žydelis R Wallace B P Gilman E L amp Werner T B (2009)Conservation of marine megafauna through minimization of fish-eries bycatch Conservation Biology 23 608ndash616 httpsdoiorg101111j1523-1739200901172x

How to cite this articleMilner-GullandEJGarciaSArlidgeW etalTranslatingtheterrestrialmitigationhierarchytomarinemegafaunaby-catchFish Fish 2018001ndash15 httpsdoiorg101111faf12273

Page 15: Translating the terrestrial mitigation hierarchy to marine ......of marine megafauna by-catch in fisheries, going from defining an overarching goal with an associated quantitative

emspensp emsp | emsp15MILNER- GULLAND Et AL

Squires D amp Garcia SM (2014) Ecosystem-level impacts of fisheries bycatch on marine megafauna Biodiversity conservation through miti-gation policy economic instruments and technical changeReportofthe IUCN-CEM-FEGScientificworkshopGland Switzerland 7ndash10October2013GlandSwitzerlandIUCN

SquiresDampGarciaSM(inpress)Fisheries bycatch in marine ecosys-tems Policy economic instruments and technical change ChichesterUKJWileyampSons

SwimmerYArauzRMcCrackenMMcNaughtonLBallesteroJMusylMhellipBrillR(2006)DivingbehavioranddelayedmortalityofoliveridleyseaturtlesLepidochelys olivaceaaftertheirreleasefromlongline fishing gearMarine Ecology Progress Series323 253ndash261httpsdoiorg103354meps323253

TolottiMTFilmalterJDBachPTravassosPSeretBampDagornL(2015)BanningisnotenoughThecomplexitiesofoceanicsharkmanagementbytunaregional fisheriesmanagementorganizationsGlobal Ecology and Conservation 4 1ndash7 httpsdoiorg101016jgecco201505003

Tuck G N Polacheck T amp Bulman C M (2003) Spatio-temporaltrendsoflonglinefishingeffortintheSouthernOceanandimplica-tionsforseabirdbycatchBiological Conservation1141ndash27httpsdoiorg101016S0006-3207(02)00378-6

UNEP-WCMC(2016)Marine no net loss A feasibility assessment of imple-menting no net loss of biodiversity in the seaCambridgeUKUnitedNationsEnvironmentProgramme

Vaissiegravere A-C Levrel H Pioch S amp Carlier A (2014) Biodiversityoffsets for offshore wind farm projects The current situation inEurope Marine Policy 48 172ndash183 httpsdoiorg101016jmarpol201403023

Wallace B P Heppell S S Lewison R L Kelez S amp CrowderL B (2008) Impacts of fisheries bycatch on loggerhead tur-tles worldwide inferred from reproductive value analy-ses Journal of Applied Ecology 45 1076ndash1085 httpsdoiorg101111j1365-2664200801507x

Wanless R M Ryan P G Altwegg R Angel A Cooper JCuthbert R amp Hilton G M (2009) From both sides Dire de-mographic consequences of carnivorous mice and longlining for

the critically endangered Tristan albatrosses on Gough IslandBiological Conservation 142 1710ndash1718 httpsdoiorg101016jbiocon200903008

WardP LawrenceEDarbyshireRampHindmarshS (2008) Large-scale experiment shows that nylon leaders reduce shark bycatchandbenefitpelagiclonglinefishersFisheries Research90100ndash108httpsdoiorg101016jfishres200709034

WardTampPhillipsB(2010)SeafoodecolabelingInRQGraftonRHilbornDSquiresMTaitampMJWilliams(Eds)Handbook of ma-rine fisheries conservation and management (pp 608ndash617) OxfordUKOxfordUniversityPress

WilcoxCampDonlanCJ (2007)Compensatorymitigationasasolu-tion to fisheries bycatch-biodiversity conservation conflictsFrontiers in Ecology and the Environment 5 325ndash331 httpsdoiorg1018901540-9295(2007)5[325cmaast]20co2

WilcoxCampDonlanCJ (2009)NeedforaclearandfairevaluationofbiodiversityoffsetsforfisheriesbycatchConservation Biology23770ndash772httpsdoiorg101111j1523-1739200901173x

Wolf SHartlBCarrollCNeelMCampGreenwaldDN (2015)Beyond PVAWhy recovery under the Endangered Species Act ismorethanpopulationviabilityBioScience65200ndash207httpsdoiorg101093bioscibiu218

ZedlerJBampCallawayJC (1999)TrackingwetlandrestorationDomitigation sites follow desired trajectories Restoration Ecology 769ndash73httpsdoiorg101046j1526-100X199907108x

Žydelis R Wallace B P Gilman E L amp Werner T B (2009)Conservation of marine megafauna through minimization of fish-eries bycatch Conservation Biology 23 608ndash616 httpsdoiorg101111j1523-1739200901172x

How to cite this articleMilner-GullandEJGarciaSArlidgeW etalTranslatingtheterrestrialmitigationhierarchytomarinemegafaunaby-catchFish Fish 2018001ndash15 httpsdoiorg101111faf12273


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