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Fish and Fisheries. 2019;20:729–747. wileyonlinelibrary.com/journal/faf | 729 © 2019 John Wiley & Sons Ltd Received: 20 October 2018 | Revised: 14 April 2019 | Accepted: 16 April 2019 DOI: 10.1111/faf.12373 ORIGINAL ARTICLE Effective monitoring of freshwater fish Johannes Radinger 1 | J. Robert Britton 2 | Stephanie M. Carlson 3 | Anne E. Magurran 4 | Juan Diego Alcaraz‐Hernández 1 | Ana Almodóvar 5 | Lluís Benejam 6 | Carlos Fernández‐Delgado 7 | Graciela G. Nicola 8 | Francisco J. Oliva‐Paterna 9 | Mar Torralva 9 | Emili García‐Berthou 1 1 GRECO, Institute of Aquatic Ecology, University of Girona, Girona, Spain 2 Faculty of Science and Technology, Bournemouth University, Poole, Dorset, UK 3 Department of Environmental Science, Policy, and Management, University of California, Berkeley, California 4 Centre for Biological Diversity, School of Biology, University of St Andrews, St Andrews, UK 5 Department of Biodiversity, Ecology and Evolution, Complutense University of Madrid, Madrid, Spain 6 Aquatic Ecology Group, University of Vic – Central University of Catalonia, Vic, Spain 7 Departamento de Zoología, Facultad de Ciencias, Universidad de Córdoba, Córdoba, Spain 8 Department of Environmental Sciences, University of Castilla‐La Mancha, Toledo, Spain 9 Departamento de Zoología y Antropología Física, Universidad de Murcia, Murcia, Spain Correspondence Johannes Radinger, GRECO, Institute of Aquatic Ecology, University of Girona, 17003 Girona, Spain. Email: [email protected] Funding information Government of Catalonia, Grant/Award Number: 2014 SGR 484 and 2017 SGR 548; Spanish Ministry of Science, Innovation and Universities, Grant/Award Number: BiodivERsA3‐2015‐26, CGL2015‐69311‐ REDT, CGL2016‐80820‐R and PCIN‐2016‐ 168 Abstract Freshwater ecosystems constitute only a small fraction of the planet's water re‐ sources, yet support much of its diversity, with freshwater fish accounting for more species than birds, mammals, amphibians or reptiles. Fresh waters are, however, par‐ ticularly vulnerable to anthropogenic impacts, including habitat loss, climate and land use change, pollution and biological invasions. This environmental degradation, com‐ bined with unprecedented rates of biodiversity change, highlights the importance of robust and replicable programmes to monitor freshwater fish. Such monitoring programmes can have diverse aims, including confirming the presence of a single species (e.g., early detection of alien species), tracking changes in the abundance of threatened species, or documenting long‐term temporal changes in entire communi‐ ties. Irrespective of their motivation, monitoring programmes are only fit for purpose if they have clearly articulated aims and collect data that can meet those aims. This review, therefore, highlights the importance of identifying the key aims in monitor‐ ing programmes and outlines the different methods of sampling freshwater fish that can be used to meet these aims. We emphasize that investigators must address is‐ sues around sampling design, statistical power, species’ detectability, taxonomy and ethics in their monitoring programmes. Additionally, programmes must ensure that high‐quality monitoring data are properly curated and deposited in repositories that will endure. Through fostering improved practice in freshwater fish monitoring, this review aims to help programmes improve understanding of the processes that shape the Earth's freshwater ecosystems and help protect these systems in face of rapid environmental change. KEYWORDS biodiversity targets, ecological monitoring, environmental assessment, environmental management, rivers and lakes, sampling design

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Page 1: Effective monitoring of freshwater fish - UCM

Fish and Fisheries. 2019;20:729–747. wileyonlinelibrary.com/journal/faf  | 729© 2019 John Wiley & Sons Ltd

Received:20October2018  |  Revised:14April2019  |  Accepted:16April2019DOI: 10.1111/faf.12373

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

Effective monitoring of freshwater fish

Johannes Radinger1  | J. Robert Britton2 | Stephanie M. Carlson3  | Anne E. Magurran4  | Juan Diego Alcaraz‐Hernández1  | Ana Almodóvar5  | Lluís Benejam6  | Carlos Fernández‐Delgado7  | Graciela G. Nicola8  | Francisco J. Oliva‐Paterna9 | Mar Torralva9 | Emili García‐Berthou1

1GRECO,InstituteofAquaticEcology,UniversityofGirona,Girona,Spain2FacultyofScienceandTechnology,BournemouthUniversity,Poole,Dorset,UK3DepartmentofEnvironmentalScience,Policy,andManagement,UniversityofCalifornia, Berkeley, California4CentreforBiologicalDiversity,SchoolofBiology,UniversityofStAndrews,StAndrews,UK5DepartmentofBiodiversity,EcologyandEvolution,ComplutenseUniversityofMadrid,Madrid,Spain6AquaticEcologyGroup,UniversityofVic–CentralUniversityofCatalonia,Vic,Spain7DepartamentodeZoología,FacultaddeCiencias,UniversidaddeCórdoba,Córdoba,Spain8DepartmentofEnvironmentalSciences,UniversityofCastilla‐LaMancha,Toledo,Spain9DepartamentodeZoologíayAntropologíaFísica,UniversidaddeMurcia,Murcia,Spain

CorrespondenceJohannesRadinger,GRECO,InstituteofAquaticEcology,UniversityofGirona,17003Girona,Spain.Email:[email protected]

Funding informationGovernmentofCatalonia,Grant/AwardNumber:2014SGR484and2017SGR548;SpanishMinistryofScience,InnovationandUniversities,Grant/AwardNumber:BiodivERsA3‐2015‐26,CGL2015‐69311‐REDT,CGL2016‐80820‐RandPCIN‐2016‐168

AbstractFreshwater ecosystems constitute only a small fraction of the planet's water re‐sources,yetsupportmuchofitsdiversity,withfreshwaterfishaccountingformorespeciesthanbirds,mammals,amphibiansorreptiles.Freshwatersare,however,par‐ticularlyvulnerabletoanthropogenicimpacts,includinghabitatloss,climateandlandusechange,pollutionandbiologicalinvasions.Thisenvironmentaldegradation,com‐binedwithunprecedented ratesof biodiversity change, highlights the importanceof robust and replicableprogrammes tomonitor freshwater fish. Suchmonitoringprogrammes can have diverse aims, including confirming the presence of a singlespecies(e.g.,earlydetectionofalienspecies),trackingchangesintheabundanceofthreatenedspecies,ordocumentinglong‐termtemporalchangesinentirecommuni‐ties.Irrespectiveoftheirmotivation,monitoringprogrammesareonlyfitforpurposeiftheyhaveclearlyarticulatedaimsandcollectdatathatcanmeetthoseaims.Thisreview,therefore,highlightstheimportanceofidentifyingthekeyaimsinmonitor‐ingprogrammesandoutlinesthedifferentmethodsofsamplingfreshwaterfishthatcanbeusedtomeettheseaims.Weemphasizethatinvestigatorsmustaddressis‐suesaroundsamplingdesign,statisticalpower,species’detectability,taxonomyandethicsintheirmonitoringprogrammes.Additionally,programmesmustensurethathigh‐qualitymonitoringdataareproperlycuratedanddepositedinrepositoriesthatwillendure.Throughfosteringimprovedpracticeinfreshwaterfishmonitoring,thisreviewaimstohelpprogrammesimproveunderstandingoftheprocessesthatshapetheEarth'sfreshwaterecosystemsandhelpprotectthesesystemsinfaceofrapidenvironmental change.

K E Y W O R D S

biodiversitytargets,ecologicalmonitoring,environmentalassessment,environmentalmanagement,riversandlakes,samplingdesign

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730  |     RADINGER Et Al.

1  | INTRODUC TION

Human‐driven environmental changes continue to raise sub‐stantial concerns for biodiversity conservation and have led tothe development and implementation of many ecological moni‐toringprogrammesaroundtheworld(Nichols&Williams,2006).Theseprogrammesgenerallyaimtounderstandandmanagetheinteractions of environmental change with biodiversity (Fölster,Johnson,Futter,&Wilander,2014).Giventheincreasingserious‐ness of environmental degradation, the need for effective eco‐logical and biodiversitymonitoring programmes has never beenhigher(Lindenmayer&Likens,2010).Freshwaterecosystemsareparticularly imperilled by anthropogenic activities worldwide.Althoughfreshwaterscover lessthan1%oftheearth'ssurface,they support high levels of biodiversity (Dudgeon et al., 2006;Strayer & Dudgeon, 2010). Extinction rates of freshwater taxaareconsiderablyhigherthanterrestrialspecies(Salaetal.,2000),duetoissuesincludinghabitatloss,climateandlandusechange,pollutionandbiological invasions (Ormerod,Dobson,Hildrew,&Townsend,2010;Stenderaetal.,2012).Atapproximately13,000species, freshwaterfishrepresent40%–45%ofglobalfishdiver‐sity(Lévêque,Oberdorff,Paugy,Stiassny,&Tedesco,2008),withthis highly diverse group including some of themost imperilledanimalsontheplanet(Cooke,Paukert,&Hogan,2012).

Freshwaterfishesalsoprovideecosystemservicesofmajoreco‐nomic,nutritional,scientific,historicalandculturalimportance(IUCNFFSG,2015). For example, freshwater andmarine fisheries jointlyconstitute the largest extractive use of wildlife in the world andcontributetooveralleconomicwell‐beingbymeansofexportcom‐moditytrade,tourismandrecreation(Santhanam,2015).Freshwaterfishprovideamajorsourceofproteinforhumansandsupportthelivelihoodsofmanypeople(Holmlund&Hammer,1999),particularlyintheGlobalSouth.However,thereareseriousthreatstothisvalu‐ableresourcerelatedtoover‐exploitationandotheranthropogenicstressors(Allanetal.,2005;deKerckhove,Minns,&Chu,2015).

Thewiderangeofresponsesoffreshwaterfishestoanthropogenicstressorsmakefishvaluableindicatorsforassessingthebiologicalandecologicalintegrityoffreshwatersandtheircatchments(Fausch,Karr,&Yant,1984;Magurranetal.,2018;Schiemer,2000).Thebreadthoffundamental informationonecologyandtaxonomy,combinedwiththeirhighersocietalimportancecomparedtootherfreshwatertaxa,makesfreshwaterfishapopulartargettaxoninassessmentsofeco‐logicalintegrity(Simon&Evans,2017).Correspondingly,freshwaterfishesarecommonlyusedforevaluatingthefunctioningandstatusoffreshwaterecosystemsandhabitatquality.Theseassessments,how‐ever,areonlyasgoodasthedatathatunderpinthem.Forthisreason,effectiveandmeaningfulmonitoringoffishpopulationsandcommu‐nitiesinfreshwaterhabitatsisessential.

Theneedforeffectivemonitoringinecologicalresearchiswell‐recognized and there are many monitoring programmes that haveprovidedimportantscientificadvancesandcrucialinformationforen‐vironmentalpolicy(Lovettetal.,2007).Forexample,freshwaterfishmonitoringhashighlightedchanges inspeciesdiversityandspecies

status in rivers and lakes (e.g., Counihan et al., 2018; Holmgren,Degerman,Petersson,&Bergquist,2016;Wagner,Deweber,Detar,Kristine,&Sweka,2014),playedacentral role infish‐basedassess‐ment systems (e.g., for the EuropeanWater Framework Directive,Pont,Hugueny,&Rogers,2007),andresultedinguidelinesonstan‐dardizedfishsamplingmethods(e.g.,Bonar,Hubert,&Willis,2009).

There remainsa seriesof issuesandknowledgegapswithhowthese programmes are designed and implemented. In particular,freshwater fishmonitoring that has beenpoorly planned and lacksfocus results in ineffectiveprogrammes that rarelymeet theiraims(Lindenmayer&Likens,2009,2010;Marsh&Trenham,2008;Nichols&Williams,2006).Moreover, there is considerabledisparity acrossdevelopedanddevelopingregionsinhowmonitoringschemesareim‐plemented.Thisisanacuteproblem,asdevelopingregionsareoftencharacterized by high levels of fish diversity but limited resourcesfor research (e.g.,Vörösmartyet al., 2010).Wheremonitoringpro‐grammesareinplace,therearealmostinevitablytrade‐offsintempo‐ralandspatialscalesofmeasurement(Pollocketal.,2002),butthesetrade‐offsareoftenpoorlyquantifiedor justified, resulting in long‐termdatalackingstatisticalpower.Finally,thereareinherentissuesoverprogrammesbeingeitherquestiondrivenormandated,withthelatteroftenlackingrigourindesignresultingintheirprovisionofonlycoarse‐levelsummariesofchange(Lindenmayer&Likens,2010).

Inthisreview,weexaminetheseissuesandknowledgegapsandmake recommendations about how they can be addressedwithinmonitoring programmes. Our aim is to foster improved practices

1 Introduction 730

2Historyoffishmonitoring 731

3Aimsofeffectivemonitoring 731

4Differentquestionsleadtodifferentmonitoringapproaches

731

5Samplingandnetworkdesign,andstatisticalmodels 732

6Approachestofishmonitoring 735

6.1Monitoringquestionsversussamplingmethods 735

6.2Capturetechniquesandapplicationwithinmoni‐toringprogrammes

735

6.3Captureandreleasemethods 735

6.4Non‐capturemonitoringtechniques 737

6.5Anglers’dataanddatamining 737

6.6Complementarityofcaptureandnon‐capturemethods

738

7Majorchallengesinfishmonitoring 738

7.1 Detectability 738

7.2Taxonomy 738

7.3Economiccosts 739

7.4Fishwelfareandethicsinmonitoring 739

8Managementofmonitoringdata 740

9Conclusions 740

Acknowledgments 740

References 741

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     |  731RADINGER Et Al.

by:(a)summarizingkeyquestionsthatmonitoringcanaddresswhenaimsareclear,andtheapproach is rigorous (Sections3and4); (b)synthesizingissuesrelatedtosamplingdesignandstatisticalmodels,andindicatinghowtheymightbeovercome(Section5);(c)review‐ing different monitoring and sampling approaches (Section 6); (d)considering challenges related to species’ detectability, taxonomy,economicalcostsandethics(Section7);and(e)discussingtheimpor‐tanceoftheappropriatemanagementofmonitoringdata(Section8).

2  | HISTORY OF FISH MONITORING

Thelonghistoryofmonitoringprogrammesisreflectedinthescien‐tificliterature(FigureS1.1).Early,thoughpresumablylesssystematic,efforts in freshwater fishmonitoring recorded temporal changes infisheries,suchasreportsofAtlanticsalmon(Salmo salar,Salmonidae)declinesinacentralEuropeanriverthatdatebacktothe18thcentury(reviewedbyWolter,2015).The20thcenturymarkedashifttowardssystematicsamplingwiththemajorityoffishmonitoringprogrammesbeingestablishedbefore1979(Mihoubetal.,2017).Despitethisandin contrast toother taxonomicgroups suchasbirds,mammals andmanyplants,freshwaterfisharegenerallyunder‐representedincon‐temporarybiodiversitystudiesandmonitoringprogrammes(Mihoubet al., 2017; Troudet, Grandcolas, Blin, Vignes‐Lebbe, & Legendre,2017).Thisunderrepresentationoffish,despitetheirhighdiversity,mightbeexplainedpartlybythefactthattheyoccurinaquaticen‐vironments.Thus,incontrasttomanyterrestrialbiota,whichcanbemonitored by visual observations and where community scientists(also known as citizen scientists) can be easily recruited (Thomas,1996), fish require more specialized sampling methods. However,onefeaturesharedwithothertaxa isthatthespatialextentoffishmonitoring ishighlybiased,beingconcentratedintheGlobalNorth(Figure1).Freshwaterecosystems(e.g.,lacustrineandfluvialhabitats)are also generally neglected in fish monitoring programmes, com‐paredtothemarineenvironments(Figure1).Afurther issueisthatevenwhenfreshwaterfisharemonitored,theresultingdataareoftennotpublishedorelectronicallyarchived,andthusareofteninaccessi‐bletothebroaderscientificcommunity(Lindenmayer&Likens,2009;Revenga,Campbell,Abell,Villiers,&Bryer,2005).

3  | AIMS OF EFFEC TIVE MONITORING

Asit isnowwidelyrecognized,ecologicalcommunitiesexperiencecontinuoustemporalturnover,thatischangeinspeciescompositionand abundances (e.g., Darwin, 1859;MacArthur &Wilson, 1967).Somedegreeoftemporalturnoverisnecessarytomaintainecosys‐temfunctionsandproperties.However,therateoftemporalturno‐verincontemporaryassemblagesexceedsthebaselinepredictedbyecologicaltheory(Dornelasetal.,2014).Consequently,theoverallgoalineffectivemonitoringoffreshwaterfishshouldnotbelimitedtodocumentingchangeperse,butshouldalsoaddressthedriversoftheobservedchange(therebyidentifyingpotentialremedies).

Thereareanumberofdefinitionsofmonitoringinconservation,ecologicalandaquaticcontexts(TableS1.1).Here,wedefinefresh‐water fish monitoring as repeated, field‐based measurements of fish that are collected in a systematic manner, allowing the poten‐tial detection of important shifts at population or community lev‐els.Therefore,effectivemonitoringrequiresaclearsetofspecificobjectives linkedtotheoverallgoalofdetectingsystemicshifts infishpopulationsorcommunitiesovertimeandspace,andsoshouldutilizemethodologiesandsamplingeffortthatprovidethedataandstatisticalpowersufficienttomeettheseobjectives.

4  | DIFFERENT QUESTIONS LE AD TO DIFFERENT MONITORING APPROACHES

Monitoringprogrammesneedarigorousdesignandprotocolforcol‐lection of data over a sufficiently long period to ensure sufficientstatisticalpowertodetecttrendsorchangesandtoenablethean‐swering of themotivating questions (Lindenmayer & Likens, 2010;Nichols&Williams, 2006). Irrespectiveof themotivatingquestion,freshwaterfishmonitoringshouldgenerallyhelptoadvanceecosys‐temunderstandingandprovide informationneeded to identifypo‐tentialremedies,requiringthedetectionofsignificantchangesatthecommunitylevel(e.g.,quantifyingtrendsinspeciesrichness,temporalα‐andβ‐diversity,functionaldiversity,foodwebstructure),and/oratthepopulation level (e.g., quantifying trends inpopulation size anddynamics,abundanceofkeystone,threatenedornon‐nativespecies,geneticdiversity,speciesranges,fisheriesstocks,sizeandagestruc‐ture,behaviour,phenology,growth,shape,and/orcondition).Anex‐ceptiontothismightbeinmandated‐monitoringprogrammeswherehighlyspecificdata(e.g.,onspeciespresence,abundance,and/oragestructure)arecomparedagainstpredeterminedstandards(Alexander,2008; Hellawell, 1991; Hurford, 2010), such as in the WaterFrameworkDirectiveoftheEuropeanUnion(Birketal.,2012). Inarestorationcontext,monitoringoftenaimsatassessingthesuccessofimplementedmeasures(Kershner,1997).Thereby,monitoringisnotastand‐aloneactivity;itcontributestoconservation‐orientedscienceandisusedtoinformstructureddecision‐makingprocessesinconser‐vationmanagement(Nichols&Williams,2006).

It is the question(s) that determine the design of amonitoringprogramme.Somequestionscanbeaddressedwithspecies‐specificpresence‐onlydata,whileothersmightrequiresamplingofanentirecommunity (Table1).The lattercasemayutilizearangeofcapturemethods(Zale,Parrish,&Sutton,2012)thatcan,inturn,helpassessthespatialbehaviour,trophicecologyandgeneticcharacteristicsofindividuals(Lucas&Baras,2000;Lundqvistetal.,2010).Alternativesampling methods include more recent approaches such as com‐munityscienceand theuseof socialmedia/crowd‐sourcedscience(Section6).Thedataneedsassociatedwithasuiteofkeymonitoringquestionsare summarized inTable1.Westress the importanceofprogrammesclearlyarticulatingtheirquestionsasthisensuresthatthesamplingdesigncangeneratethedatarequiredtoanswerthem.As aminimum, there shouldbe identificationofwhat needs to be

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732  |     RADINGER Et Al.

measured(e.g.,fishabundance,fishattributes),thespatialandtempo‐ralscopeoftheprogramme(e.g.,duration,scale;cf.Dixon&Chiswell,1996);thecriteriaforreliability(e.g.,precision,power);andtheprac‐ticalconstraints(e.g.,humanresources,costs,socialconflicts).

5  | SAMPLING AND NET WORK DESIGN, AND STATISTIC AL MODEL S

Samplingdesignrelatestothetemporalfrequencyofsamplingwithinadesignednetworkthatcomprisesaseriesofspatiallysegregatedsites.Assuch,decisionsneedtobemaderegardinghowtoallocatemonitor‐ingeffortwithinandamongstyears,andacrosssites(Larsen,Kincaid,Jacobs,&Urquhart,2001).Twomajorprinciples,theavoidanceofbias

intheselectionprocedureandachievementofhighprecision,shouldunderliethedesign(Crawford,1997).Asamplingdesigncanbebasedon probabilistic or non‐probabilistic methods. Probabilistic designsinclude simple random sampling, systematic sampling and stratifiedrandomsampling,withthelattertwobeingmoreappropriateforhet‐erogeneous, hierarchically structuredaquatic environments, suchasriverdrainages(Lowe,Likens,&Power,2006;Thorp,Thoms,&Delong,2006). However, in fishmonitoring, sample sites are frequently se‐lectednon‐probabilistically,oftenbasedonjudgmentorconvenience(Pope,Lochmann,&Young,2010;Wilde&Fisher,1996).Irrespectiveofthis,decisionsonthedesignoftheprogrammeshouldbebasedonaprioridefinedstatisticalmodelsthatcanreliablyanswerthequestionsmotivatingthemonitoringprogramme,suchasthoserelatedtoquan‐tifyingcommunitystructure,speciesabundanceorotherpopulation

F I G U R E 1  Overviewoffishmonitoringprogrammesacrossglobalregions(a),taxonomicorders(b)andbiotopetypes(c)basedonrecordsofthetaxonomicgroupOsteichthyes(n=543)intheGlobalPopulationDynamicsDatabase(GPDD,version2.0,released2010,www.imperial.ac.uk/cpb/gpdd2,NERCCentreforPopulationBiology,ImperialCollege,2010).Note:Theapparentlackofmonitoringin,forexample,AfricaandAustraliamightreflectalimitationofthedatabaseratherthananactuallackofmonitoring[Colourfigurecanbeviewedat wileyonlinelibrary.com]

Number of �sh monitorings per global region

0 1–5 5–10 10–100 >100Record of �sh monitoring scheme

Aulopiformes

Tetraodontiformes

Zeiformes

Cypriniformes

Lophiiformes

Anguilliformes

Gasterosteiformes

Scorpaeniformes

Pleuronectiformes

Clupeiformes

Perciformes

Gadiformes

Salmoniformes

0 5 10 15 20 25 30 35 %

n = 1

n = 1

n = 2

n = 3

n = 3

n = 5

n = 7

n = 12

n = 56

n = 78

n = 82

n = 102

n = 191

Coastal

Fluvial

Lacustrine

Tidal/Intertidal

Marine

0 15 30 45 60 75 %

n = 3

n = 15

n = 18

n = 98

n = 409

Freshwater (n = 33)

(c)

(b)

(a)

Page 5: Effective monitoring of freshwater fish - UCM

     |  733RADINGER Et Al.

TAB

LE 1

 Overviewofkeyquestionsinfishmonitoringprograms,associateddataneedsandmostapplicablesamplingmethods[Colourtablecanbeviewedatwileyonlinelibrary.com]

Not

e: Samplingmethod:1electrofishing,2netting,3trapping,4telemetry(e.g.,acoustic,radioorpassiveintegratedtranspondertags),5mark–recapture,6environmentalDNA,7hydroacousticassess‐

ment,8anglercatchstatistics,9datamining,10communityscience.‐/orange=no,yellow=maybe,green=yes,na=notapplicable.

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734  |     RADINGER Et Al.

parameters(e.g.,agestructure).Thesequestionsrequireconsiderationduringdesignphasesaswellasadditionalresourcesandtime,separatefromthemonitoringprogrammeitself,forcompletion.

Wheretheaimsaretodetectchangesrelatedto(local)manage‐mentactionssuchashabitatrestoration,orto impactassessment,before‐after‐control‐impact (BACI) designs are frequently used(Osenberg,Bolker,White,St.Mary,&Shima,2006;Stewart‐Oaten&Bence,2001;Thiault,Kernaléguen,Osenberg,&Claudet,2017).Here, a prioripoweranalyses(Legg&Nagy,2006;Marsh&Trenham,2008;Maxwell& Jennings, 2005; Peterman, 1990) can guide theestimation of the minimum number of samples needed to detectacertaineffect size (orminimumdetectabledifference)accordingtoadesiredlevelofsignificance(Peterman,1990;Steidl,Hayes,&Schauber,1997).

However, as fish monitoring programmes are typically under‐taken to detect temporal changes in populations over potentiallylargerscales(Cowx,Harvey,Noble,&Nunn,2009),statisticalcon‐trolandreplicationdesignsareoftenunfeasible (Carpenter,Frost,Heisey,&Kratz,1989;Hargrove&Pickering,1992;Schindler,1998;Turner,Gardner,&O'Neill,2001).AdvancedBayesian(hierarchical)models(Hobbs&Hooten,2015)offerusefulalternatives,especiallywhenworkingwithimperfectdatasetsand/oruncertaintyassoci‐atedwithsamplingandobservation,as it isoften thecase in fishmonitoring.Forexample,Wengeret al. (2017) appliedaBayesianapproach to predict the viability of multiple (potentially isolated)populationsofLahontancutthroattrout(Oncorhynchus clarkii hen‐shawi,Salmonidae); thisapproachenabledpredictions tobemadeinminimally sampled or even un‐sampled populations. Other ap‐plications of Bayesianmodels to analysemonitoring data includeestimationsofoccupancyandrichnessoffishwhileaccountingforimperfectdetection(Bayley&Peterson,2001;Coggins,Bacheler,&Gwinn,2014)andforrelatingenvironmentaldriverstostreamfishpopulationdynamics(Letcheretal.,2015;Wheeleretal.,2018).

Thespatial structureofdendriticnetworks,and theirassociatedconnectivityanddirectionality,makesriversystemsparticularlychal‐lengingformonitoring.Theeffectofspatialvariabilitycanbereducedby stratified random sampling, that is the proportional sampling ofstratathatrepresentdifferenthabitatunits(Downesetal.,2002)andiswidelyused inaquaticecosystems (Dukerschein,Bartels, Ickes,&Pearson,2011;Haxton,2011;Wilde&Fisher,1996).Morerecently,SpatialStreamNetwork(SSN)modelshavebeendevelopedtobettercapturethecontinuousnatureofrivers(Fausch,Torgersen,Baxter,&Li,2002)andtoaccountforthespatiallyautocorrelatedrelationshipsbetweenlocationswithinastreamnetwork(Isaaketal.,2014).Forex‐ample, Isaak,VerHoef,Peterson,Horan,andNagel (2017)analyseda large fishdensitydata setusingSSNmodels toobtainpopulationestimatesfortroutspeciesfrom108sitesina735kmrivernetwork.TheSSNmethodology is accessiblevia the statistical tools “STARS”(Peterson&VerHoef,2014)and“SSN”(VerHoef,Peterson,Clifford,&Shah,2014).

Inasystematicsamplingdesign,thefirstsamplesite ischosenrandomlyandallsubsequentsamplesareregularlyplacedinspaceortime(Conroy&Carroll,2009;Quinn&Keough,2002).Asystem‐atic design is useful when investigating effects of environmentalgradients.Arecentdevelopmentinthiscontext istheGeneralizedRandom Tessellation Stratified (GRTS) design (Stevens & Olsen,2003, 2004), available from the statistical package “spsurvey”(Kincaid & Olsen, 2016). GRTS allows design‐based inferences toentire areas based on spatially balanced samples, that is a spatialdistribution of sample locations that balances the advantages ofsimpleorstratifiedrandomsamplesorsystematicsamples(Larsen,Olsen,&Stevens,2008).GRTShasbeenevaluatedasreliableandcost‐effective,forexample,formonitoringNorthAmericansalmo‐nids(Gallagher,Wright,Collins,&Adams,2010).

Theadaptiveapproach(Box1)arguesthatthesamplingdesignshould be re‐evaluated and re‐designed as necessary as data are

Box 1 Adaptive monitoringThereisoftenhighuncertaintyandcomplexityinthedriversoffishcommunitychangethatcanrangefromglobalenvironmentalchange(e.g., climate change;Graham&Harrod, 2009;Radinger et al., 2016) tomore local issues (e.g., altered flow regimes;Harby,Olivier,Merigoux,&Malet,2007).Monitoringprogrammesmustbecapableofprovidingdatasuitableforthecontinuedmanagementoftheresources(Polasky,Carpenter,Folke,&Keeler,2011).Theinformeddecision‐makingprocessofadaptivemonitoring(sensuLindenmayer&Likens,2009)enablesmonitoringprogrammestoevolve inresponsetonewquestions, information,situationsorconditionsorthedevelopmentofnewprotocols(Lindenmayer,Likens,Haywood,&Miezis,2011).Adaptivemonitoringisconsideredalong‐termactivitycloselyrelatedtoscientificresearchandmanagement.Theultimateaimofanyadaptivemonitoringprogrammeistodemonstratethatnewinsightsgainedthroughitsapplicationwillimprovemanagementpractices(Lindenmayeretal.,2011),potentiallyleadingtoincreasesintheeffectivenessofmonitoringforconservation.Anexampleof adaptivemonitoring is outlinedbyFölster et al. (2014) for Swedish freshwaters.At theoutset, theearlynaturalistsmeasuredspecificandlocalizednaturalphenomenasuchastherelationshipbetweenmacrophytesandlakewaterchemistry(Lohammar,1938).However,thescopeofthefreshwatermonitoringprogrammeinSwedenandthenumberofmonitoredsitesincreasedalongwiththeemergenceofnewchallengesrelatedto,forexample,eutrophicationinthe1960s,acidraininthe1970sandtheEUWaterFrameworkDirectivein2000.Today,theprogrammeconsistsofregularlong‐termmonitoringofwaterchemistryandbiodiversity(includingfreshwa‐terfish)in114streamsand110lakes(Fölsteretal.,2014).Thisexamplenotonlyillustratesthevalueofadaptivemonitoringbyprovidinglong‐termdatatounderstandandovercomemanyoftheemergingenvironmentalproblems,butalsoemphasizesitspotentialtoinves‐tigatefuturechallenges,forexamplerelatedtoclimatechange,testingresiliencetheory,orpredictingregimeshiftsandtippingpoints.

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     |  735RADINGER Et Al.

gatheredand theirvariabilityanalysed.Ananalysisof thecompo‐nentsofvarianceandtheir influenceontrenddetectioncapabilitycan help in preparing design‐efficient trend monitoring networks(Larsenetal.,2001).Thisensuresthatchangesinthechemical,phys‐icalorbiologicalconditionsareaccountedforinthesamplingdesign(Bucklandetal.,2012;Strobl&Robillard,2008).

6  | APPROACHES TO FISH MONITORING

6.1 | Monitoring questions versus sampling methods

Thenumeroussamplingmethodsthatcanbeutilizedforfishmoni‐toring, including capture andnon‐capture techniqueshavebeenextensivelyreviewed(e.g.,Bonaretal.,2009;Joy,David,&Lake,2013; Zale et al., 2012). Capture methods involve the physicalremoval of fish from thewater to enable species identification,andthecollectionofbiometricdata(e.g.,length,weight)andhardstructures (e.g., scales) for ageing the fish to determine popula‐tion demographics and dynamics. The most common methodsavailableforcapturingfreshwaterfishincludeelectrofishing,net‐tingandtrapping(Bonaretal.,2009).Non‐capturemethods(e.g.,hydroacoustic surveys) canprovidedata complementary to cap‐ture techniques. They can also be usedwhere capturemethodslack sufficient power to provide robust estimates of populationabundances (Hughes, 1998; Lyons, 1998).However, a featureofsomenon‐capturemethods is their taxonomic ambiguity due toeithertheirlackoffishcapture(Boswell,Wilson,&Wilson,2007)(Section 6.4) or through erroneous identification of specimens(Section7.2).

The application of a sampling method in monitoring mightdiffer markedly according to the programme's aims. For exam‐ple, electrofishing can be applied within point abundance sam‐plingdesignsthatcanbeeffectiveformonitoringthedielactivityof (small) fishes (reviewed by Copp, 2010) or the status of rarespecies (e.g., thecriticallyendangeredEuropeaneel,Anguilla an‐guilla,Anguillidae;Laffaille,Briand,Fatin,Lafage,&Lasne,2005).However,capturingfishinlongerriverreachesusingelectrofishingmightbemoresuitablewherethemonitoringaimistoassessbio‐logical/ecologicalintegrity,asbioticindicesrequiredataatmulti‐pleorganizationlevels,fromsizestructuretoassemblagerichness(e.g.,Noble,Cowx,Goffaux,&Kestemont,2007;Pontetal.,2007;Schmutz,Kaufmann,Vogel, Jungwirth,&Muhar,2000),often inconjunctionwithdataonhabitatquality (e.g.,VanLiefferingeetal.,2010;Milner,Wyatt,&Broad,1998).

6.2 | Capture techniques and application within monitoring programmes

Thechallengeofensuringthatcapturemethodsarefitforpurpose,suchasevaluatingthecompositionofanassemblage(detailsinBox2;e.g.,Zaleetal.,2012)hasresultedinaseriesofstandardizedpro‐tocolsbeingmadeavailableforsampling inlandfishpopulations inmanyareasoftheworld,includingEurope,NorthAmericaandNew

Zealand(Bonaretal.,2009;CEN,2003,2006;Joyetal.,2013;TableS4.1).Standardizationnotonlyreferstotheequipmentusedorhowit isused,butalso to thetimingofsampling, thehabitats thataresampled,andeffortapplied(Bonar,Fehmi,&Mercado‐Silva,2011).Standardizing the collection and reportingof fishmonitoringdataoffersmany advantages including an improved ability to comparedata across regions or time, improved communication across po‐liticalboundaries,andthecontrolofbiasassociatedwithdifferentsampling techniques (Cooke et al., 2016). Standardization in fishsamplinghasbeenconsideredanimportantstepforwardinmanag‐inglong‐termdataandassessingefficacyoflargespatialscaleman‐agementstrategies(Bonaretal.,2017).Thisisofparticularrelevanceinmonitoringprogrammeswheremany researchers combinedatasetstojointlyaddressquestionsovertimeandspace.Foracompre‐hensive overviewon standardisation of fish sampling across sam‐plinggearsandaquaticenvironments,seeBonaretal.(2009).

Twofundamentalconceptshaveemergedinrelationtotheap‐plicationofcapturetechniquesandprotocolstofishmonitoring:theimportanceofsamplingdesign (discussedearlier inSection5)andresponsedesign(Stevens&Urquhart,2000).

Responsedesignincorporatesdecisionsabouthowtomeasurethefishcommunityandpopulationmetricswithaccuracyandpre‐cision(Pollocketal.,2002).Forexample,whereassessmentsofagestructure, growth rates and recruitment are required, then deci‐sionsareneededontheageingmethod,suchaswhethertorelyonlength–frequencyanalysesorcollecthardstructures,suchasscales,fromcaptured fishes (e.g.,Hamidan&Britton,2015). If scalesarecollected,thendecisionsareneededregardinghowmanyindividualfishneedtobesampledandoverwhatsizerange(Busst&Britton,2014). In addition,where hard structures are being used for age‐ing, the frequency of annulus formationmight need validating tomaximizeaccuracy(Beamish&McFarlane,1983),requiringregularsamplingthroughouttheyearormark–recapturemethods(Britton,Harper,&Oyugi,2010;Chisnall&Kalish,1993).Scalesamplesforfishageing,andtissuesamplesforgeneticandstableisotopeanal‐yses, can be collected from fish captured by anglers to comple‐menton‐goingmonitoring(GutmannRoberts,Bašić,AmatTrigo,&Britton,2017).

6.3 | Capture and release methods

Itisoftendesirabletoreleasecapturedfish,unharmed,tothesiteofcapture,withoutfurther intervention.However,attachingtrackingdevicesormarkingfish,priortorelease,cansubstantially increasethe amount of information obtained. For example, biotelemetryusingacoustic,radioorpassiveintegratedtranspondertags(Cooke,Woodley, Brad Eppard, Brown, & Nielsen, 2011; Thiem, Taylor,McConnachie,Binder,&Cooke,2011)canrevealindividualvariabil‐ity inmovementsandbehaviourswithinandbetweenpopulations(Lucas&Batley,1996;Radinger&Wolter,2014),elucidatepopula‐tionmixing and gene flow (Huey, Schmidt, Balcombe,Marshall, &Hughes,2011),assesstheeffectsofconnectivityandhabitatfrag‐mentationonriver fishes (Capraetal.,2017;Linetal.,2018),and

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Box 2 Sampling effort and biodiversity estimationDecisionsaboutthespatialextentanddurationofsamplinghaveimportantimplications.Ifthegoalistoquantifyanattributeofapopula‐tionofinterest,then,allotherthingsbeingequal,estimatesofabundancewillscalepredictablywitheffort.Therearearangeofstatisticaltechniques,suchasremovalsampling(Southwood&Henderson,2000),thatcanbeusedtoestimatepopulationsizeand/ortoensurethateffortisadequatefortheintendedpurpose.Itisrelativelystraightforward,therefore,tocomputetrendsforsinglepopulations.If,ontheotherhand,theaimistoquantifycompositionalturnover(temporalβ‐diversity),ortocalculateametricofα‐diversity,suchasassemblagerichness,itisessentialthatanytemporalorspatialcomparisonstakeaccountoftheinherentunevennessofecologicalas‐semblages.Althoughthenumberofindividuals(acrossallspecies)willtypicallyincreaselinearlyifanassemblageissampledoveralongertimeperiod,ortheareasampledisincreased,thespeciesaccumulationcurvewillgraduallyflatten(Figure2).Asaresult,anymetricsthateitherexplicitlyorimplicitlydependonrichnesscannotbescaledbysimplemultiplicationordivision.Speciesrichnessisthemetricmostobviouslyinfluencedbythis,butmostbiodiversityindices,including,forexample,theBerger‐Parkerdominancemetric(Magurran,2004,2011;Magurran&McGill,2011)andJaccardsimilarity(Baselga,2010),arealsoaffected.Fortunately,therearestatisticalsolutionstothisproblem.Rarefactionisthetraditionalwayofmakingfaircomparisonsacrossassem‐blagesorofcommunitydiversityoverspaceortime(Gotelli&Colwell,2001,2011).Inessence,thesamples(orassemblages)arerarefiedtothesmallestcommonsamplingeffort.Rarefactioncanbecomputedinrelationtotheminimumnumberofindividualssampledortothesmallestnumberofsamplingunits.Whilemostrarefactionanalysesfocusonspeciesrichness,inprinciplemanydifferentbiodiversitymetricscanberarefied.Inthecaseoftemporalorspatialβ‐diversitycomparisons,theinvestigatorshouldusesample‐basedrarefactionasthisautomaticallyretainstheidentityofthespeciesinvolved.Arecentinnovationistoextrapolatetothelargestsamplesizeratherthanrarefytothesmallestone(Chaoetal.,2014;Hsieh,Ma,&Chao,2016).Rarefactioncanalsobeusedtomakeinformedcomparisonsaboutcommunitystructureandcompositionusingnullmodelapproaches(Cayuela&Gotelli,2014;Cayuela,Gotelli,&Colwell,2015).Insummarythen,anycomputationoftrendsincommunityα‐diversityorβ‐diversityshouldeitherbebasedonsamplingthathasbeenrigor‐ouslystandardizedordatathathavebeenstatisticallystandardized(byrarefactionorsimilar)—seeFigure2foranexample.

F I G U R E 2   Illustrationofthevariationofthenumberofspecies(speciesrichness)andnumericalabundancewithsamplingeffort.ThedataarefortworiversitesinTrinidad(top(a)LowerAripo,bottom(b)Maracas,sampledfourtimesannuallyforfiveyears.ThedataaredescribedinMagurranetal.(2018).Ineachcase,thespecies(andnumericalabundance)accumulationcurvesareconstructedbyrandomlyshufflingthetemporalorderofthesamplesa1,000times.Theopenpointsrepresentthemedianvalueoftherandomisedaccumulationcurves;their95%confidencelimits(0.025and0.975quantiles)arealsoshown(speciesrichness‐leftcolumn;numericalabundance‐rightcolumn)[Colourfigurecanbeviewedatwileyonlinelibrary.com]

20S

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helpevaluatemanagementunitsforfisheriesorconservation(Funk,McKay,Hohenlohe,&Allendorf,2012).

Mark–recapturestudiescanalsostronglycomplementfishmon‐itoringbyprovidingalternativeestimatesofpopulationsizeandfishages(Hameletal.,2015;Sassetal.,2010).Theycanalsorevealtheextentofmigrationsofindividualfishbetweenhabitatswithinspe‐cificpopulations(Sandlund,Museth,&Øistad,2016).

6.4 | Non‐capture monitoring techniques

Non‐capturemonitoringmethods to complement capturedata in‐clude environmental DNA and hydroacoustic assessments. Thesemethods are often appliedwithinmonitoring programmes to pro‐videdataondifferentcomponentsofthecommunityorpopulationandareespeciallyusefulforlargerwaterbodieswherecapturetech‐niquesareoftendifficulttoapplyorareinefficient.

EnvironmentalDNA(“eDNA”hereafter)isbasedonthepresenceDNAoffishesinwatersamplesoriginatingfrommucusandfaeces,thesloughingoffofcellsfromtheirgutlining,andthedecompositionofdeadindividuals(Davisonetal.,2016;Jerde,Mahon,Chadderton,&Lodge,2011;Turner,Uy,&Everhart,2015).DNAisextractedfromwatersamples,andpolymerasechainreactionusedinconjunctionwith species‐specific genetic markers to amplify DNA fragmentstoindicatethepresenceoftargetspecies(Turneretal.,2015).Themethodisincreasinglybeingappliedtothemonitoringoffreshwa‐terspecies(FigureS1.1),includingthoseofconservationimportance(Takahara,Minamoto,Yamanaka,Doi,&Kawabata,2012;Thomsenetal.,2012).

TherearetwobasicwaysthateDNAcanbeappliedinafishmoni‐toringprogramme.Watersamplescanbeanalysedtodetectthepres‐enceofaspecificspeciesorcanbescreenedforwholecommunitiesoforganismsusing“eDNAmetabarcoding”(Hänflingetal.,2016;LawsonHandley,2015).Recentrefinementshave improvedthereliabilityofspecies’detection(Hänflingetal.,2016),butsomequestionsremain,forexample,onfactorsaffectingtherateofDNAbreakdownintheenvironment(Barnesetal.,2014).However,thenon‐detectionofspe‐cies‐specificDNAfragmentsinasampleofriverwaterdoesnotnec‐essarily implytheabsenceofthetargetspecies,nordoesapositivesignalnecessarilyimplythatthespeciesispresent,aseDNAcouldhavebeentransportedfromupstreamareas(Roussel,Paillisson,Tréguier,&Petit,2015).Nevertheless,asrefinementsinthetechniquecontinue,itshouldincreasinglyprovideastrongcomplementtocapturemethods,especiallyinregionswhereknowledgeonthespecieslikelytobepres‐entisavailable.AlthoughissuesoverthereliabilityofeDNAtoprovideestimatesofabundancearebeingaddressed,theyremainhighlychal‐lenging(Lacoursière‐Roussel,Côté,Leclerc,&Bernatchez,2016).OneimportantconsiderationwillbetheintegrationofdatacollectedusingtraditionalmethodswithinferencesaboutfishcommunitiesobtainedusingeDNA(seeSection6.6below).

Hydroacousticassessmentsinvolvetheapplicationofanacous‐ticbeamfromatransducerthroughthewater.Anyfishwithinthebeamreturnsasignal,withthetargetstrengthofthereturningsignalindicatingtherelativesizeofthefish.Whilethemethodgenerates

dataonfishdensity,thereishightaxonomicambiguityintermsofspeciespresent,withnobiometricdatacollected (other thancon‐versionoftargetstrengthstoapproximatefishlengths;Boswelletal.,2007).Nevertheless,hydroacousticassessmentshavebeenusedextensively for fishmonitoring,especially in lakeswheresamplingstrategieshavebeendeveloped(e.g.,Guillard&Vergès,2007),withtarget strengths related to species‐specific attributes to increaseknowledgeoncommunitycomposition(Frouzova,Kubecka,Balk,&Frouz,2005).Inlowlandrivers,suchastheRiverThamesandRiverTrentinEngland,mobilehydroacoustictechniqueshavebeenappliedtomonitorthespatialandtemporaldistributionsoffishcommunities(Hughes,1998;Lyons,1998).Themethodhasalsobeenappliedtoassessingthestatusofendangeredfishes(Zhangetal.,2009).

6.5 | Anglers’ data and data mining

Statisticsonanglercatchratesandspeciescompositionhavebeenapplied to themonitoringof fish community compositionof largelowlandriverswhereotherfishcapturemethodsareeitherdifficulttoapplyorinefficient(Jones,Robson,Lakkis,&Kressel,1995).Forexample, in theRiverTrent, England, angler catch statisticsmoni‐tored changes in the fish assemblage in relation to improvementsin water quality (Cooper &Wheatley, 1981; Cowx & Broughton,1986).More recently,catchstatistics from individualanglerswereused to assess the population status of mahseer fishes (Tor spp.,Cyprinidae)intheRiverCauvery,India(Pinder,Raghavan,&Britton,2015a,2015b).Anissuewithangler‐baseddataisthattheytendtobebiasedforspecificspeciesandsizeranges(AmatTrigo,GutmannRoberts,&Britton,2017).

Data mining, where spatial and temporal data on species aregathered through information available from online sources, is adifferentnon‐capturetechniqueformonitoringchangesinthedis‐tribution of species. Databases including the Global BiodiversityInformation Facility (GBIF; www.gbif.org/), the Global PopulationDynamics Database (GPDD;www.imperial.ac.uk/cpb/gpdd2/secure/login.aspx),orVertNet.orgenableuserstoaccessglobaldistribu‐tion recordsof species via directed searches that provide recordswith locationcoordinates forusewithinGIS.TheGPDDalsopro‐videsdataonpopulationdynamics,ratherthanjustdistributiondata.TheFishBasedatabase(Froese&Pauly,2018)providesspecies‐levelinformationgatheredfromtheliterature,includingoccurrencesanda wide range of ecological data.

Analternativemethodtousingtheseonlinedatabasesismonitor‐ing thedistributionof fishesvia community science,particularly viasocialmediaplatforms.Indeed,theapplicationofcommunityscienceandcrowdsourcingtothecollectionofbiologicaldatais increasinglyfrequent(e.g.,www.inaturalist.org,FigureS1.1),thankstomanysmart‐phones now having GPS, high‐resolution cameras, and continuousInternet connection (Bik &Goldstein, 2013; DiMinin, Tenkanen, &Toivonen, 2015). For example, for monitoring distributions of non‐nativefish,anumberofsmartphone“apps”areavailable,withthesegenerally enabling the user to send a geo‐referenced image of thespeciestoaspecificorganizationforvalidationandrecording.Current

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examplesinclude“That'sInvasive”(http://www.rinse‐europe.eu/resources/smartphone‐apps/) and “AquaInvaders” (http://naturelocator.org/aquainvaders.html).Bothofthese“apps”alsoprovideuserswithinformationandimagesonspecificinvaderstofacilitatetheiridentifi‐cationofspecies.Venturelli,Hyder,andSkov(2017)haverecentlyre‐viewedtheopportunitiesandchallengesassociatedwithangler“apps.”

Datacanalsobesourcedfromuser‐generatedcontentonvar‐ioussocialmediaplatforms(DiMininetal.,2015).Bydatamining,thesenon‐biologicalsources,suchasviasearchesofspecificso‐cialmediasources(e.g.,https://www.youtube.com/),recreationalfisheriesforumsandblogs,andnews‐mediachannels,fishdistri‐butionanddispersaldatacanbegenerated.Forexample,thisap‐proachhasbeenappliedsuccessfullytoassessmentsofnon‐nativefishinvasions,suchasperch(Perca fluviatilis,Percidae)andchan‐nel catfish (Ictalurus punctatus, Ictaluridae) in Portugal (Banha,Ilhéu,&Anastácio,2015;Banha,Veríssimo,Ribeiro,&Anastácio,2017).Increasingly,thesesearchescanbeautomatedthroughuseofcomputercode.Forexample,geo‐referencedimagesandvideoofspecificspecieswithinimageandvideohostingwebsites(e.g.,flickr)canbesearched,withGIS interfacesenablingdistributionmapstobeconstructed(seeFigure3)andthustemporalandspa‐tialdistributionpatternsbetterunderstood(CodingClub,2018).

6.6 | Complementarity of capture and non‐capture methods

Dataacquiredfromcaptureandnon‐capturemethodswithinthesamemonitoringprogrammeneedtobeintegratedeffectively.Forexample,fishmonitoring inWindermere,England, a relatively largeanddeepglaciallake,hasrecentlybeencomplementedbyapplicationofeDNAthatrecordedthepresenceof14of16fishspeciesknowntobepre‐sent,whenconcomitantgillnetsurveysonlycapturedfourfishspecies(Hänflingetal.,2016).Windermerehasalsobeenmonitoredregularlyforover60yearsbyothermethods,includingfishtraps,gillnets,hy‐droacousticsandpiscivorousfishdietcomposition(Langangenetal.,2011;Winfield,Fletcher,&James,2008,2012).Thehighcomplemen‐tarityofthesedatasetshasimprovedunderstandingofenvironmental(e.g.,nutrientenrichment,warming)andotherchanges(e.g., invasive

fishes), and illustrated their potential for monitoring other systems(e.g.,Vindenesetal.,2014;Winfield,Fletcher,&James,2010).

7  | MA JOR CHALLENGES IN FISH MONITORING

7.1 | Detectability

Many evaluations of biodiversity, including those of freshwaterfishes (Magurran, 2004; Southwood&Henderson, 2000), assumethatindividualshavebeensampledrandomlyfromtheassemblage(Buckland,Studeny,Magurran,&Newson,2011;Pielou,1975).Thisisrarelyachievableinnature(Pielou,1975).Inmanycases,theproblemarisesbecauseitisdifficult(orimpossible)toknowifaspeciesthatisabsentfromasiteorsampleistrulyabsentorismissingthroughthe ineffectiveness of the samplingmethod. Thus, it is importanttothoroughlyconsiderobservationerrorandcaptureprobabilitiesandtoaddressissuesofdetectabilityanddetectionbiasalsoinfishmonitoring.Potentialsolutionstoissuesofdetectabilityhavebeenextensivelydiscussedelsewhereand includemodellingoccupancy(Bayley & Peterson, 2001; Iknayan, Tingley, Furnas, & Beissinger,2014;MacKenzieetal.,2002,2006;Royle&Link,2006;Wenger&Freeman,2008),estimatingtheprobabilityofdetectionofspecies(and/orindividuals)throughmark–recapture(Borchers,Buckland,&Zucchini,2002;Borchers,Stevenson,Kidney,Thomas,&Marques,2015;Bucklandetal.,2011)ordistancesampling (Bucklandetal.,2001, 2004; 2011), and/or demonstrating that the data are suffi‐cientlyrobusttoaddressthequestionposedwithoutfurthercorrec‐tion(Bucklandetal.,2011;Magurranetal.,2018).

7.2 | Taxonomy

Taxonomic issues can often emerge in biological monitoring pro‐grammes,withthemostobviousonebeingtaxonomicuncertaintyandtheriskofspeciesmisidentificationinthefieldorthelaboratory.Forexample,Daan(2001)reportedextensivespeciesmisidentifica‐tionsinamarinefishdatabaseandtherearemanyothercasesinthefreshwaterfishliterature(e.g.,Hänfling,Bolton,Harley,&Carvalho,

F I G U R E 3  Thedistributionof(a)Northernpike(Esox lucius,Esocidae)and(b)Zander(Sander lucioperca,Percidae)intheUK,between1986and2016,basedondatafromGBIF(www.gbif.org).TheRcode(RCoreTeam,2017)usedtoconstructthefigurewasadoptedfromtheCodingClub(https://ourcodingclub.github.io/2017/03/20/seecc.html)[Colourfigure can be viewed at wileyonlinelibrary.com]

(a) (b)

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2005; Serrao, Steinke, & Hanner, 2014; Vidal, García‐Berthou,Tedesco, & García‐Marín, 2010). Nevertheless, a well‐appreciatedadvantageoffishisthattheirtaxonomyisbetterknownandeasierthaninmostotherfreshwatergroups,suchasinvertebratesoralgae,andthus,fishcanoftenbeidentifiedinthefieldwithoutsacrificingindividuals.However,thisislesslikelytobethecaseinspecies‐richregionssuchasthetropics,wherethetaxonomyislesswell‐known,comparedtoregionswithwell‐characterizedfishfaunas.

The extent of species misidentification in more taxonomicallychallenginggroups, such as stream invertebrates, receives greaterattention than in freshwater fish. For example, Stribling, Pavlik,Holdsworth,andLeppo (2008)compared taxonomic identificationof stream macro‐invertebrates across eight U.S. laboratories andfoundmeans of 21% taxonomic disagreement. These kinds of er‐rorsmightalsooccurinfishmonitoring,especiallyinsampleswithhighspecies richnessor in samples fromregionswhere taxonomyispoorlydescribed.Thesestudiesreinforcethe importanceofad‐equatetrainingandexperience,documentationofstandardproce‐duresandroutinequalitycontrol(Stribling,Moulton,&Lester,2003;Striblingetal.,2008).Speciesmisidentificationisevenmoreimport‐antwhen fishers are interviewed to obtain local knowledge data.Here,thoroughvalidationproceduresareessential(Poizat&Baran,1997;Valbo‐Jørgensen&Poulsen,2000).

A similar problem iswhen taxonomy changes, and it is recog‐nizedthatasinglespeciesinfactcomprisesseveralcrypticspecies.Thisproblemisincreasinglyfrequentgiventheincreasingpowerofmolecular tools (e.g., April,Mayden,Hanner, & Bernatchez, 2011;Laraetal.,2010;Young,McKelvey,Pilgrim,&Schwartz,2013).Forexample,Youngetal.(2013)foundthatthemajorityofspecies‐leveltaxonomicunitsofthegenusCottus(Cottidae)asevaluatedbyDNAbarcodingdidnotassigntopreviouslyrecognizedspeciesinthisre‐gion.Newtaxonomicalignmentshindercomparisonwitholdsam‐plesifnospecimenswerepreserved.Inaddition,thesamespeciesnamesmayhavehaddifferentsynonymsinthepast,meaningthatdatabasesneed tobe carefully revised for inconsistencies ander‐rors.Erroneoussequencesandmisidentificationsarealsofrequentin GenBank and similar sequence databases (Harris, 2003). It hasbeenestimatedthatupto56%ofGermanfreshwaterfishspeciesmay be incorrectly identified to species level in some databases(Knebelsberger, Dunz, Neumann, & Geiger, 2015). Consequently,errors ingeneticsdatabasesmighthavemajoradverse impactsoneDNAasarobusttechnique.It islikelythatthefrequencyofsuchtaxonomicproblemsindataismoreprevalentinmonitoringoffresh‐waterfishthaninresearch(Striblingetal.,2003).Itisthusimportanttofullyreferencethetaxonomicresourcesusedinstudies,notjustasaqualitycheckonmethodology,butalsotorecognizetheimpor‐tanceoftaxonomyandtheworkoftaxonomists(Santos&Branco,2012;Vink,Paquin,&Cruickshank,2012;Wägeleetal.,2011).

7.3 | Economic costs

Foramonitoringprogrammetobeeffective,successfulandsustain‐able over the longer‐term, it must not only be ecologically relevant

andstatisticallycredible,butalsocostefficient,thatistheperceivedbenefitsofecologicalmonitoring(e.g.,informationontrendsorstatuschanges)mustjustifyitscost(Caughlan&Oakley,2001;Charles,Garcia,&Rice,2016;Hinds,1984).Asfinanciallimitationsalwaysapply,sus‐tainedmonitoringrequiresaproperselectionofrelevantvariablesthatneedtobemeasured(Braun&Reynolds,2012).Oftenthetruecostsofmonitoringarenotrecognizedandlikelyunderestimated(Caughlan&Oakley,2001),anditsbenefitsdependonthevaluethatsocietygivestothelong‐termsustainabilityoffreshwaterecosystems.Hence,costsofmonitoringneedtobecontrastedwiththecostsofnotmonitoring.Theseincludeincreaseduncertaintyinevaluatingoutcomesandfutureprojections,andthepossibilitythatmanagersmaynotdetect impor‐tantshiftsuntilitistoolatetoeffectivelyaddressthem.

CaughlanandOakley(2001)providedabreakdownofmonitoringcosts,comprisingofbudgetaryexpensesrelatedto,forexample,datacollection, datamanagement, quality assessment, data analysis, re‐portingandscientificoversight,opportunitycosts(i.e.,otherbenefitsforgonebyallocatingresourcestomonitoring),andexternalcosts(i.e.,costsnotdirectlycoveredbythemonitoringprogrammebudget).Thecostsfordatacollection—whicharefrequentlythelargest—mayvarydependingonthemethodsapplied.Whileestablishedmethodsinfishmonitoring,suchasfield‐basedcapturemethods(e.g.,electrofishing,netting,trapping),arecommonlylabourintensiveinthefieldandthuscostly,thefinancialcostsofemergingmethods,suchasuseofeDNA,theautomatizedcollectionofdata(e.g.,hydroacousticassessments),andtheuseofcommunityscienceanddatamining,areoftenrelatedtopost‐processing,managingandanalysingbigdata(Section6.4).Adetailedreviewofthecostsassociatedwithecologicalmonitoringcanbefoundelsewhere(e.g.,Caughlan&Oakley,2001).

7.4 | Fish welfare and ethics in monitoring

Theimportanceofethicalissuesrelatingtobiologicalfieldworkandtheneedtominimizeharmtospeciesandecosystemshas repeat‐edly been emphasized (e.g., Bennett et al., 2016; Costello et al.,2016; Farnsworth & Rosovsky, 1993); a detailed consideration ofthesematters is beyond the scope of this review.Wenote, how‐ever, that fish welfare issues have received much attention (e.g.,Sloman, Bouyoucos, Brooks, & Sneddon, 2019), often centredaround the question ofwhether fish are sentient and can experi‐encepainandsuffering (e.g.,Arlinghaus,Cooke,Schwab,&Cowx,2007;Braithwaite,2010;Huntingfordetal.,2006,2007;Roseetal.,2014)—achallengingquestionthathasanumberofimplicationsinascientific,ethicalandlegalcontext(Browmanetal.,2019).Browmanet al. (2019) argue for a pragmatic approach using objective indi‐cators of stress, health status and behaviour to inform about fishwell‐being.

Irrespectiveofthescientificdebateonfishwelfare, institutionalrequirements and legal regulations need to be considered duringfreshwater fish monitoring. Fish sampling usually requires specificpermits from responsible authorities, particularly when workingwithprotectedspeciesorinprotectedareas.Dependingontheaimandsamplingmethod,fishmonitoringmightinvolvethecaptureand

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treatmentoffishormightevenrequiremethodsofdestructivesam‐pling, that is thekillingof fish (e.g.,Blessing,Marshall,&Balcombe,2010),suchaswhenindividualsrequiretaxonomicidentificationinthelaboratory,includingwherevoucherspecimensarerequired(Bortolus,2008;Rochaetal.,2014;Section7.2).However,alternativemethodsof identification should be used to avoid collection of rare species(Costello et al., 2016;Minteer,Collins, Love,&Puschendorf, 2014).Protocols for fieldwork (e.g.,Barbour,Gerritsen,Snyder,&Stribling,1999;Brenkman&Connolly,2008;CCME,2011;Cowxetal.,2009;Cowx& Fraser, 2003; Joy et al., 2013) typically provide guidelinesonappropriateandleastinvasivetechniques(e.g.,non‐capturetech‐niquessuchashydroacousticsandeDNAwhereapplicable,Section6.4)andaredesignedtominimizestressordamagecausedbycatching,handling andholding.Developmental stage and speciesdifferencesarealsotakenintoaccount.Thesamplingmethodanddesignshouldconsidertrade‐offsofthepotentialharmtofishversusthequalityoftheobtaineddatainrelationtosamplingefficiency.Inparticular,whencapturetechniquesareapplied,potentialcumulativeeffectsshouldbepaidspecificattentionasfishmonitoringinvolvesrepeatedsamplingofspeciesthatcanbelong‐lived(>20years)andisoftentargetedforprotectedorendangeredspecies(Benejametal.,2012).Forexample,an efficient and common capture technique such as electrofishingmightcausesub‐lethal injuriesthatareoftennotexternallyobviousandpossiblyfatal(Snyder,2003).Moreover,ethicalissuesrelatedtofishmonitoringextendbeyondfishwelfareandmustalsoconsiderim‐pactsonnon‐targetspeciesandecosystemsorthepotentialtransmis‐sionofpestsand/orinvasivespecies(Costelloetal.,2016).

8  | MANAGEMENT OF MONITORING DATA

Forthesustainablesuccessofamonitoringprogrammeandtopo‐tentiallyinferfuturechanges,policiesandproceduresthatguaran‐teethequalityofdatacapture,documentationandpreservationforlong‐termuseisrequired(Michener,2015;Michener&Jones,2012;Rüegg et al., 2014; Sutter, Wainscott, Boetsch, Palmer, & Rugg,2015).Forexample,Vinesetal.(2014)foundthattheavailabilityofresearchdatadeclineswitharticleage,withtheprobabilityoffind‐ingthedatasetdecreasingby17%peryear.

Although the importance of integrating datamanagement intolong‐termecological(monitoring)projectshasbeenemphasizedre‐peatedlyinpreviouspapers(Costello&Wieczorek,2014;Sutteretal.,2015),thisisoftenaneglectedareainfreshwaterfishstudies(butseeMoe,Schmidt‐Kloiber,Dudley,&Hering,2013;Petersonetal.,2013forsomeexamples).Thoroughlyconsideringdatamanagementtopreservedataforlong‐termuseandaccessibility(evenbeyondthelifetimeoftheworkthatgeneratedthem)willrequiremoretimeandresourcestofishmonitoringprogrammesandshouldbeconsideredattheearlieststagesandaccountedforinbudgetaryplans.

Datamanagementisnotlimitedto“what”wascollected(i.e.,fishsamplingdata);manyotherdataoftenassociatedwithsampling,suchasgeospatial information,multimediacontent,voucherspecimens,associated environmental variables and other biological data, also

needtobeconsidered(Costello&Wieczorek,2014).Furthermore,toensuretheutilityofadataset,itmustbeaccompaniedbymeta‐data,that is,adetaileddescriptionofwhocreatedthedata,whenandwherethedatawerecollectedandstored,howandwhythedataweregenerated,processedandanalysed(Michener,2006).

Datamanagementisakeyelementinfreshwaterfishmonitoringprogrammes.Adetaileddiscussionofchallengesandopportunitiesof datamanagement, aswell as practicesof how it canor shouldbeimplementedinfishmonitoringisprovidedelsewhere(Costello,Michener,Gahegan,Zhang,&Bourne,2013;Costello&Wieczorek,2014; Michener & Brunt, 2000; Reichman, Jones, & Schildhauer,2011;Sutteretal.,2015).

9  | CONCLUSIONS

Given the rapid environmental degradation of the Earth's fresh‐water ecosystems and associated unprecedented rates of biodi‐versity change, the importanceof robust, replicable andeffectiveprogrammes to monitor freshwater fish has never been higher.Future challenges related tohabitatdegradation, climateand landuse change, and biological invasions necessitate monitoring pro‐grammes that systematically collect quality data allowing the po‐tentialdetectionof systemic shiftsofpopulationsor communitiesandtherebyimproveourunderstandingofecosystemresponsestoenvironmentalchange.Thereisapressingneedforeffectivemoni‐toringtocomprehensiblyquantifybiodiversitychangeandtoinformevidence‐basedenvironmentaldecision‐making.

Ataminimum,whenestablishingamonitoringprogramme,cleararticulationofthemonitoringaim(s)isessentialandshouldaddress:(a)what should bemonitored and how; (b) how to allocate effortwithintimeandacrosssites;(c)establishcriteriafordatareliability;and(d)identifypracticalconstraints.

Monitoringmustalsotakeintoaccountissuesrelatedtothede‐tectability of species, taxonomy and animal welfare. Additionally,monitoringprogrammesmustintegratedatamanagementpracticesthatensurethequalityofdatacapture,documentationandpreser‐vationofinformationforlong‐termuseandre‐use.

Insummary,carefulreflectiononaims(s)andtheextenttowhichthedatacollectedwillmeettheseaimswillgreatlyimprovethequal‐ityandusefulnessofmonitoringdata.Consistentlyhighmonitoringstandardswillimprovedatacomparabilitywithinandamongstcoun‐triesandsystems.Finally,effectivemonitoringoffreshwaterfishwilladvance our overall understanding of freshwater ecosystems andcontributetothepreservationandmanagementoffreshwaterfishdiversitywhilehelpingmitigateanthropogenicimpacts.

ACKNOWLEDG EMENTS

ThispaperisbasedonaworkshopfundedbytheSpanishMinistryof Science, Innovation and Universities (project CGL2015‐69311‐REDT).Additionalfinancialsupportwasprovidedbythesamemin‐istry(projects:ODYSSEUS,BiodivERsA3‐2015‐26,PCIN‐2016‐168;

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andCGL2016‐80820‐R)andtheGovernmentofCatalonia(ref.2014SGR484and2017SGR548).

ORCID

Johannes Radinger https://orcid.org/0000‐0002‐2637‐9464

Stephanie M. Carlson https://orcid.org/0000‐0003‐3055‐6483

Anne E. Magurran https://orcid.org/0000‐0002‐0036‐2795

Juan Diego Alcaraz‐Hernández https://orcid.org/0000‐0002‐6885‐6695

Ana Almodóvar https://orcid.org/0000‐0003‐1465‐3857

Lluís Benejam https://orcid.org/0000‐0002‐2741‐4858

Carlos Fernández‐Delgado https://orcid.org/0000‐0002‐1359‐435X

Graciela G. Nicola https://orcid.org/0000‐0002‐6898‐307X

Emili García‐Berthou https://orcid.org/0000‐0001‐8412‐741X

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SUPPORTING INFORMATION

Additional supporting information may be found online in theSupportingInformationsectionattheendofthearticle. 

How to cite this article:RadingerJ,BrittonJR,CarlsonSM,etal.Effectivemonitoringoffreshwaterfish.Fish Fish. 2019;20:729–747. https://doi.org/10.1111/faf.12373