Research biases create overrepresented “poster children” of marine invasion ecology 2021 Hannah V. Watkins.pdf


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Received:16September2020Revised:13February2021Accepted:8March2021
DOI:
REVIEW
Researchbiasescreateoverrepresented“posterchildren”
ofmarineinvasionecology
ôté
EarthtoOceanResearchGroup,
DepartmentofBiologicalSciences,SimonAbstract
FraserUniversity,Burnaby,CanadaNonnativemarinespeciesareincreasinglyrecognizedasathreattotheworld’s
Correspondenceoceans,yetarepoorlyunderstoodrelativetotheirterrestrialandfreshwater
ôté,,weconductedasystematicreviewof2,203researcharti-
Sciences,SimonFraserUniversity,8888clesonnonnativemarineanimalstodeterminewhetherthecurrentliterature
UniversityDrive,Burnaby,BCV5A1S6,
,howmuchweknowaboutthese
Email:******@,%
ofnonnativeanimalslistedintheWorldRegisterofIntroducedMarineSpecies
.
-,fewerthanhalfwere
-
Fundinginformationsequencesofmarineintroductions:%ofstudiesquantifiedtheimpactof
NaturalSciencesandEngineering
ResearchCouncilofCanada,Grant/,ourknowledgeofnonnativemarinespeciesisheavily
Number:DiscoveryGrantsProgramlimitedbystrongtaxonomicbiasesconsistentacrossallphyla,resultinginone
ortwodisproportionatelywell-studiedrepresentativesforeachphylum,which
werefertoasthe“posterchildren”
itdifficulttoeffectivelytriagethemostdetrimentalinvasivespeciesformanage-
mentandillustratethechallengesinachievingtheglobalbiodiversitygoalsof
preventingandmanagingtheintroductionandestablishmentofinvasivespecies.
KEYWORDS
biologicalinvasions,bioticintroductions,introducedmarineanimals,invasionecology,sys-
tematicreview,taxonomicbias
1INTRODUCTIONentlackofeffectisduetoalackofpoweratdetect-
ingtheseeffects(Davidson&Hewitt,2014)ordelayed
Marinespecieshavebeentransportedandintroducedtomanifestationofimpactsduetolagtimesintheinva-
areasbeyondtheirnativerangesinvirtuallyallpartsofsionprocess(Crooks,2005;Iacarellaetal.,2015).However,
thecoastalocean(Molnaretal.,2008;Rilov&Crooks,sometranslocatedspeciesbecomereadilyinvasive;they
2009).Manytranslocatedspeciesappeartohavenoimpactincreaseinabundance,competingeffectivelyforresources
onnativecommunitiesandecosystems(.,Antonetal.,withnativespeciesorpreyingonthem(Blackburnetal.,
2019).Somearetrulybenign,whileforothers,anappar-2019;Molnaretal.,2008;Pyšeketal.,2020;Vitousek
etal.,1996;Wallentinus&Nyberg,2007).Insomecases,
thesespeciescanultimatelytriggerdeclinesinnative
ThisisanopenaccessarticleunderthetermsoftheCreativeCommonsAttributionLicense,whichpermitsuse,distributionandreproductioninanymedium,providedthe
originalworkisproperlycited.
©
;
/:.
2of12WATKINSetal.
populations,resultinginlossesinecosystemservicesinvasivealgaeismirroredinmajorgroupsofnonnative
(Blackburnetal.,2019).Nevertheless,-
someinvasivespecieshavebeenhighlighted:theycanbemalphylainWRiMS(Ahyongetal.,2020),aswellas
ecosystemengineers,increasinghabitatorpreyavailabil-theintensivelystudiedphylumCtenophora,weexamined
ityfornativespecies,orreplaceecologicalfunctionsthatthetopicsandlocationsofstudiesofnonnativemarine
wouldotherwisebelostfollowingthedeclineordisappear-animalstoassesstheirrelevancetoourunderstanding
anceofnativespecies(Davisetal.,2011;Katsanevakisetal.,,wealsodocumentedvaria-
2014;Schlaepferetal.,2011).tioninstudyintensityacrossspeciestodetermineifthere
Whethermeasurableimpactshouldbeatthecoreofaremarkedtaxonomicbiasesinwhatscientistschooseto
anydefinitionofinvasivenessisanacademicquestionstudy.
thathasimportantimplicationsformarineconservation.
Blackburnetal.(2014),forexample,proposedageneral
frameworkfortheprioritizationofinvasivespeciesfor2METHODS
managementthatreliedheavilyondemonstratednegative
,Ojaveeretal.(2015)
aframeworkmightunderestimatetheriskofnonnativecriteria
marinespeciesbecausetheimpactsofmarineinvaders
takealongtimetomanifestandmightbesubtleincom-UsingtheISIWebofSciencedatabase,weconducted
,acomprehensivesystematicliteraturereviewfocusing
theeffectsofnonnativemarinespeciesaregenerallynotonninemajorphylaofmarinemacro-animals:Porifera,
wellknownandaretaxonomicallybiased(Crystal-OrnelasCtenophora,Cnidaria,Bryozoa,Annelida,Mollusca,
&Lockwood,2020;Florencioetal.,2019;KatsanevakisArthropoda,Echinodermata,andChordata(separated
etal.,2014;Lowryetal.,2013;Ruizetal.,1999;Vilàetal.,intoTunicataandfishes).Theterminologyusedto
2010).Forexample,recentglobalmeta-analysesofinva-describenonnativespeciesisinconsistentandhighlyvar-
sivemarinespeciesimpactstendtobedominatedbystud-iedamonginvasionbiologists;someclassifyallnonnative
iesofprimaryproducers(.,60%ofstudiesinGuy-Haimspeciesas“invasive,”othersdelineate“introduced”and
etal.,2018;41%ofspeciesinAntonetal.,2019),even“invasive”basedonspreadorimpact,andsomeeven
thoughplantsandalgaeonlyaccountfor25%ofallintro-classifycertainnativespeciesasinvasive(Lockwoodetal.,
ducedspeciesrecordedintheWorldRegisterofIntro-2013).Wethereforechosetousebroadsearchtermsto
ducedMarineSpecies(WRiMS;Ahyongetal.,2020).Per-captureasmuchoftherelevantliteraturepossible(.,
hapsforthisreason,concernshavebeenraisedabouttheinvasive,introduced,nonnative,nonindigenous,alien,
inclusionofonlyonenonnativemarinespecies(.,Plo-exotic).Inthisreview,wespecificallyuse“nonnative”to
tosuslineatus)onthelistofinvasivealienspeciesofcon-refertoanyspeciesfoundoutsideofitsnativegeographical
cerntotheEuropeanUnion(Tsiamisetal.,2020),despiterangeasaconsequenceofhumanactivity(whetherdirect
thewell-knownhighriskofmarineintroductionsintotheorindirect)and“invasive”torefertoanyofthesespecies
MediterraneanSea(Galil,2008;Zenetosetal.,2017).Fur-thathavebeenshowntohavesignificantanddetrimental
thermore,evenforthebetterstudiedprimaryproducers,
theimpactsofonly10%ofknownnonnativeseaweedshavetaxonseparatelywithtaxon-specificsearchtermsfor“all
beenstudied(Davidsonetal.,2015;Schaffelke&Hewitt,years”endingJune2018(seeonlinesupplementforfull
2007;Williams&Smith,2007),aproportionthatmightsearchstrings).Toensurethatusingasingledatabase
applytomarineinvadersingeneral(Antonetal.,2019).wasadequate,weconductedthesamesearchforone
Infact,eventhemostbasicecologicalknowledgeaboutphylum,Cnidaria,usingtheAquaticSciencesandFish-
nonnativemarinespecies,whichcouldhintattheirinva-
sivenessandpotentialimpact,seemstobelacking(Bragaadditionalstudiesthatmetourinclusioncriteria,orjust
etal.,2018;Lowryetal.,2013).Acaseinpointisthelack5%ofthenumberobtainedwithWebofScience.
ofanyinformationaboutreproductivebehaviororontoge-Wefirstrefinedandexcludedallobviouslyirrelevant
netichabitatshiftsbyIndo-Pacificlionfish(Pteroissp.)inarticles,suchasmedicalarticles,usingWebofScienceCat-
thewesternAtlantic,whichisarguablyoneofthebestdoc-,
umentedrecentmarineinvasions(Côté&Smith,2018).ortheabstractwhenthetitlewasinsufficientlyinforma-
Here,(1)notaboutoneof
English-languageliteraturetosurveywhatiscurrentlythetargettaxonomicgroups,(2)notaboutamarinespecies
,(includingarticlesoneuryhalinespeciesinfreshwater),or
weaskedwhethertherelativelypoorunderstandingof(3):.

(mitigationofimpacts,methodsofcontrolorremoval,or
descriptivemethodsfordetectingtheinvader),and(8)

eightsubtopics(seeonlinesupplementfordetails).For
eachstudy,werecordedthemarineprovince(s)inwhich
thestudytookplace(sensuSpaldingetal.,2007)and

multiplesiteswithinaprovince,weselectedcoordinates

provinceswerestudied,werecordedonesetofcoordinates
,werecordedthehabitattype(s)
examinedineachstudy,followingtheInternationalUnion
forConservationofNature(IUCN)HabitatsClassification
Scheme(IUCN,2020;seeonlinesupplementforfull
breakdownofhabitatandsubhabitattypes).
Impactisoftenpoorlyandinconsistentlydefinedacross
thebioticinvasionliterature(Jeschkeetal.,2014).Inthe
mostbasicsenseoftheword,allnonnativespeciesnec-
essarilyhaveanimpactjustbybeingpresentinanew
location(Ricciardietal.,2013).Morecommonlythough,
inthecontextofinvasions,thedefinitiongenerallycom-
FIGURE1Flowchartshowingthestepstakeninevaluatingprisesthreekey,interactingfactors:range,abundance,and
studiesforinclusioninthissystematicreviewpercapitaeffectsoftheinvader(Parkeretal.,1999).To
broadlycaptureallstudieswithinoursearchthatmaybe
whenthenonnativespecieswasstudiedorcollectedfromusedfordecision-makingprocesses,weacceptedallstud-
-drivenrange-iesthatincludedeffects,evenwhenestimatesofrangeor
shiftingspeciesshouldbeclassifiedasintroducedorinva--
siveisacontentiousdebateininvasionbiology(Urban,initionfromRuizetal.(1999),andconsideredimpacts
2020;Wallingfordetal.,2020);tolimitreviewersubjec-asquantifiablechangesinnativepopulations,communi-
tivityandtoincludestudiesinwhichthesourceofintro-ties,ecologicalprocesses,-
ductionwasunclear,weacceptedallstudiesinwhichthetion,forinstance,atrophicstudyanalyzingthegutcon-
authorsdescribedthefocalspeciesasbeingoutofitsnativetentsofanonnativepredatorwouldnotbeconsideredan
-impactstudy,whileatrophicstudymeasuringchanges
culture,weonlyacceptedarticleswhenthespecieshadinnativepreydensityinthepresenceofthenonnative

-analyses(Antonetal.,2019;
(Figure1).Guy-Haimetal.,2018),whichrequirespecificparameters
(.,means,samplesizes,variance)tocompareeffects
,sinceinvasivespeciesmanage-
,includ-
inglessrigorousstudies,webelievethatourmoregen-
Forallacceptedarticles,
locationofstudy,thenonnativespeciesandhabitattypesmeasuringimpact,wealsonotedthestudymethod(.,
examined,,fieldexperiment,ormesocosmorlab
categorizedarticlesintoeightmaintopics:(1)taxon(theexperiment).
taxonomicdescriptionofanewspecies),(2)descriptive
(descriptionsoflife-historytraitsorbodymorphology),
(3)distribution(recordinanewlocation,overallrich-
ness,rangeextensions,orconfirmationofpresence),(4)animals
toxin(toxincontentoruptakebyinvader),(5)genetics
(populationgenetics,genomestudies,identificationofTodeterminetheproportionofknownnonnativemarine
crypticspecies,phylogeography),(6)timing(estimatesspeciesthathavebeenstudied,wecomparedourlistof
oftimesinceinvasion),(7)managementandmethodsspeciesderivedfromtheliteraturesurveywiththatof:Thedocumentwascreatedwith

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