Invasion strategy and abiotic activity triggers for non-native gobiids of the River Rhine

16 Pages·2017·5.6 MB·English

RESEARCHARTICLE
Invasion strategy and abiotic activity triggers
for non-native gobiids of the River Rhine
JanBaer1*,FrankHartmann2,AlexanderBrinker1
1 FisheriesResearchStationBaden-Wu¨rttemberg,LAZBW,Langenargen,Germany,
2 Regierungspra¨sidiumKarlsruhe,FisheriesAdministration,Karlsruhe,Germany
*[email protected]
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a1111111111 Abstract
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The24houractivitypatternsofthreenon-nativegobiids(roundgobyNeogobiusmelanosto-
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mus,WesterntubenosegobyProterorhinussemilunarisandbigheadgobyPonticolakes-
sleri)wereassessedover46consecutivemonthsbetween2011and2014fromtheir
occurrenceinthecoolingwaterintakeofanuclearpowerplantontheRiverRhine,Ger-
many.Intotal,117717gobiidswereidentifiedandclassified.Theoccurrenceofallthree
OPENACCESS speciesvariedstronglybetweensamplingyears,andspecies-specificactivitytriggerswere
Citation:BaerJ,HartmannF,BrinkerA(2017) identified.Theactivityofjuvenilesofallthreegobiidsspecieswaspositivelytemperature
Invasionstrategyandabioticactivitytriggersfor dependentwhileadulttubenosegobyactivityappearedtobenegativelytemperaturedepen-
non-nativegobiidsoftheRiverRhine.PLoSONE
dent.Increasingfluvialdischargeintheadjoiningmainriverstimulatedtheactivityofjuvenile
12(9):e0183769.https://doi.org/10.1371/journal.
pone.0183769 roundgobybutinhibitedactivityofadulttubenosegoby.Exceptforadultbigheadgoby,
activitywasalsostructuredbytimeofday,butwithnouniformmean.Meteorologicalfactors
Editor:UlrikeGertrudMunderloh,Universityof
Minnesota,UNITEDSTATES suchasprecipitation,airpressureanddurationofsunshinehourshadlittleornoinfluence
ongobiidactivity.Onselectedrareoccasions,mainlyatnight,allthreespeciesexhibited
Received:May5,2017
pulsedswarmingbehaviour,withthousandsofindividualsrecordedintheintakewater.
Accepted:August10,2017
Roundgobyswarmsexhibitedboththehighestintensityandthelargestswarmingindividu-
Published:September15,2017 als,suggestingapotentialcompetitiveadvantageovertubenoseandbigheadgoby.Electric
Copyright:©2017Baeretal.Thisisanopen fishingsurveysinnaturalriverstretchescorroboratedthisobservation.Negativeeffectson
accessarticledistributedunderthetermsofthe thenativefishfaunawereapparentonlyforthebullhead,Cottusgobio.
CreativeCommonsAttributionLicense,which
Theactivitytriggersidentifiedofferauniqueinsightintotheinvasionmechanismsof
permitsunrestricteduse,distribution,and
reproductioninanymedium,providedtheoriginal theseecosystem-changingnon-nativegobiids.
authorandsourcearecredited.
DataAvailabilityStatement:Thecollectionand
countingofthefishwasdoneunderthepermission
andpaymentofthenuclearpowerplantcompany
(EnBW)andbelongstothecompany.The Introduction
meterologicaldatabelongstothirdparty,too
(Landesanstaltfu¨rUmwelt,Messungenund Theuseofwaterfromnaturalsystemsasacoolantinthermalpowerstationsleadstoawide
Naturschutz).Theauthorgotthepermissionto rangeofecologicalimpactsonaquaticcommunitiesinboththeintakeandouttakestretches.
workwiththedata(statisticalanalyses),butnotto Thermalloadingofcoolingwaterinterferesdirectlywithphysiologicalprocessesofthebiota,
publishthemindetail.Duetothoserestrictons,the
suchasenzymeactivity,feeding,reproduction,respiration,growthandphotosynthesis[1].Of
datasetcannotbemadepubliclyavailable.
stillgreaterpotentialimpact,however,arethelossesofvariouslife-stagesofinvertebratesand
Interestedreseachersshouldcontactthe
fishescapturedonintakescreensorentrainedwithincoolingsystems.Itisnotuncommonfor
Landesanstaltfu¨rUmwelt,Messungenund
Naturschutz([email protected])torequest millionsoffishesandcrustaceanstobeimpingedonpowerplantintakescreenseachyear[2]
PLOSONE|https://doi.org/10.1371/journal.pone.0183769 September15,2017 1/16
Invasionstrategyandactivitytriggersforgobiids
meterologicaldata,Mr.Dr.Vogel(t.vogel@kk. andmanymoreeggs,planktonandlarvaeofinvertebratesandfishesarealsokilled.Absolute
enbw.com)fromtheNPPPfordataregardingthe mortalityfiguresatsomepowerplantshavebeenshowntoexceed1010individualsannually
nuclearpowerplant(amountintakewater)andMr.
[2].
Dr.FrankHartmann([email protected])
Thehugedemandforcoolingwaterbylargethermalpowerstationsmeansmostarelocated
forthegobiiddata.
nearlargewaterbodies.Permanentmonitoringofthefishfaunaatsuchlocationsistime,
Funding:Theauthorsreceivednospecificfunding
labour,andcostintensiveandmethodsarelimitedbytheoftenconsiderabledepthofwater,
forthiswork.
strongcurrents,impairedvisibilityandotherconfoundingfactors.Standardsamplingtech-
Competinginterests:Theauthorshavedeclared niques,suchaselectricfishing,divingortheuseofgillnets,allhavedifferentdisadvantages
thatnocompetinginterestsexist.
renderingthemmostlyineffectiveinthiscontext[3].However,thesheervolumeofintake
watersinlargethermalpowerplants,likeinnuclearpowerplants,constitutesasignificant
samplingoffishstocksinthesourceriverandstudiesoffishoccurrenceincoolingwater
intakeshavefacilitatedthedevelopmentofimportanttimeseries[4],withwhichtostudygen-
eralbiologicaldynamics,suchaschangesinfishcommunitycomposition.Nevertheless,most
ofthesestudiesconductedatnuclearpowerplantsarelookingfortheindirecteffectofthermal
loading[5–9],whilethecostandlogisticsofstudieslookingforthedirecteffectsoftheremoval
offishfromtheintakewaterinnuclearpowerplantsmakessuchprojectscomparativelyrare
[4].Howeversuchdatamightprovideaninsightintootherwiseunknowndynamicsandin
particulartheinvasionstrategiesofvariousnon-nativefishesinlargerivers[10,11].
TheroundgobyNeogobiusmelanostomus(Pallas,1814)isoneoftheworld’smostwide-
ranginginvasivefish,whoserapidexpansionanddeleteriousecosystemeffectsarewelldocu-
mented[12].However,detailedstudiesofautecologicalaspectsofinvasionssuchasactivity
triggersorco-occurrenceeffectsduringthecolonisationofanewhabitatarelargelymissing
[13].Thepresentstudytakesadvantagesofauniquedatasetgeneratedbyhourlyscreeningof
fishandlampreyspeciesfromthecoolingwaterintakeofanuclearpowerplantontheRiver
Rhine.Inthepresentstudy,thishighlyresolveddataisusedtodocumentthechronologyand
theintensityofinvasionsofthreenon-nativegobiidsandtocorrelatetheiroccurrencewith
abioticfactors.Gobyinvasionsfirstreachedtheareaofthesamplingstationin2007:firstcame
theWesterntubenosegobyProterorhinus semilunaris(Heckel,1837),thenthebigheadgoby
Ponticolakessleri(Gu¨nther,1861)in2010andfinallytheroundgobyin2011[14].Allthree
speciesmostprobablyarrivedviatheMain-DanubeCanal,builtin1992toconnecttheDan-
ubewiththeRhinesystem[14].Thegoalofthisstudywastogainareliablepictureofthegoby
invasionfront,inordertobetterunderstandgeneralinvadingmechanisms,andtoidentify
abioticactivitytriggers.
Materialandmethods
Ethicsstatement
Approvalofourpresentstudybyareviewboardinstitutionorethicscommitteewasnotneces-
sarybecauseallfishwerecaughtunderthepermissionofthelocalfisheriesadministration(F.
Hartmann)andallneededqualificationsfortheinvolvedpeople(fishinglicenses)were
checkedregularlybythelocalmemberoftheanimalprotectioncommittee(F.Hartmann).
Basedonthelocalfisherylaw(Landesfischereiverordnung,§2)allnon-nativefishhastobe
removed,thereforeallgobiidswerestunnedbyablowontheheadandexpertlykilledimmedi-
atelybyacardiacstabaccordingtotheGermanAnimalProtectionLaw(§4)andtheordi-
nanceofslaughterandkillingofanimals(Tierschlachtverordnung§13).Nolivinggobiids
wereused.Livenativefishcapturedinthecoolingwaterweremaintainedin50Lplastichold-
ingtanks,thecontentsofwhichwerereleasedeverysixhoursinabucketloweredintothe
mainchanneloftheriver.Electrofishingwasconductedunderalicensefromthefisheries
administration(Regierungspra¨sidiumKarlsruhe).
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Invasionstrategyandactivitytriggersforgobiids
Fig1.LocationofthePhilippsburgnuclearpowerplant(NPPP)inGermanyandsituationontheRiverRhine(herenamedRhein,
arrowindicatingdirectionofflow).
https://doi.org/10.1371/journal.pone.0183769.g001
Studyarea
ThePhilippsburgnuclearpowerplant(NPPP)islocatedinsouth-westernGermany,approxi-
mately30kmnorthofthecityKarlsruhe,onasmallisland(Rheinschanzinsel),642.5km
upstreamfromthemouthoftheRiverRhine(49˚15´N;08˚26´E)(Fig1).Waterfromthe
Rhinehasbeenusedforcoolingthefirst(926Megawatt)unitofNPPPsince1979andthesec-
ond(1468Megawatt)unitsince1984.AftertheFukushimanucleardisasterin2011,theGer-
mangovernmentdecidedtoabandonnuclearpower.NPPPunit1ceasedoperationsthesame
yearanditscoolingwaterintakewasreducedaccordingly.Unit2isduetobeshutdownin
2019accordingtoGermanatomiclaw(Atomgesetz,§7,1a).
Duringthestudyperiod(01.01.2011–31.10.2014)thecoolingwaterintakeofNPPPwas
between3and96ms-1(mean:40.8±standarddeviationSD20.9ms-1).Thiswaterisallowed
tobewarmedby8–10˚Cabovethemeanrivertemperaturebeforebeingdischarged.The
intakeofcoolingwaterhappensviaanartificiallakeconnectedwiththemainchannelofthe
Rhine.Thelakehasameanwettedwithof250mandameanwettedlengthof720m(Fig1).
Waterisreturneddirectlytothemainriver,500mdownstreamofLakeInlet(Fig1).The
RiverRhineadjacenttothemouthofthelakeisapproximately220mwide,withanaverage
depthof3.75mandayearlyaveragedischargeof1265ms-1.Despitethelocationofthecool-
ingintakebeingonthelakesome300mfromtheriver,abstractionisconsideredtotakeplace
fromthemainstreamingwaterbodyoftheRhine.Theintakestructurecandrawupto100m
s-1ofwater,comparabletotheannualdischargeofamediumsizedriverinthispartofGer-
many,andmorethanmostlargertributariesdelivertotheRiverRhine.Thisvolumeissuffi-
cienttogenerateanobservableflowofwaterfromthemainriverchanneltotheintake
structure.Theintakehappensthroughtenverticalconcretesluices,approximately5mhigh
and3mwideeach.Waterisdrawnfromthefullwaterdepthoftheartificiallakeand
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Invasionstrategyandactivitytriggersforgobiids
transportedthroughdifferentbarracks,attheendofwhichfishes,crustaceans,plantmaterial
anddebrisareremovedby12verticalscreenswithasquaremesh-sizeof1mm.Retained
materialisflushedintoatank,thesamplingpoint.
Sampling
Duringthestudyperiod,thetotalbodylengths(TL)ofallfishlongerthan2cmflushedinto
thesamplingtankweremeasuredtothenearestcm.Individualsofeachspeciesandeach1cm
length-classwerecounted.Inordertoreducelabour-intensivespeciesidentificationworkat
timeswhenfishloadswerehigh,fishoflessthan2cmTLwereassignedtoonegenericgroup
called´fishlarvae’.Thesamplingtankwaschecked24timesdaily(attheendofeachhour),by
ateamof20trainedpersonnel(biologistsandsupervisedstudents),exceptduringannual
NPPPserviceandmaintenanceoperationswhencheckswereonlycarriedouteverysecond
day(15.05.-11.06.2011;30.05–16.07.2012;05.05.-04.08.2013;22.06.-21.08.2014).Hourlysam-
plingwasthusachievedon1308days.
TheNPPPcoolingwaterintakeactsasapassivefishinggear[3]andthewaterincludesonly
migratingordriftingindividuals.Thusinthecontextofthisstudy,theoccurrenceofanindi-
vidualinthesamplingcontainerisregardedasaproxyforspeciesactivity.
Single-passelectricfishing(EFKO8000,straightDC,300–600V,Leutkirch,Germany)was
usedtodeterminethecatchperuniteffort(CPUE,individualsm-2)ofgobiidsattwostretches
oftheriver.Bothlocationswerefishedfromaboat.Theseelectricfishingsurveysfocussed
mainlyonshallow,rockyandsandyareas,thepreferredgobiidhabitats.Thesesiteswere10
kmdownstreamoftheNPPP(nearthevillageofKetsch,49˚21´N;08˚29´E)and35km
upstreamoftheNPPP(nearthevillageofPlittersdorf,48˚53´N;08˚08´E).Atthedownstream
sitea1000–2000mstretchwasfishedoneightoccasionsbetween2008and2015,whileatthe
upstreamsite,fishingwascarriedoutona100to3330msectionsixtimesoverthesame
period.
Datatreatment
Basedonaliteraturereview,allsampledgobiidslongerthan2cmTLwereclassifiedasjuve-
niles((cid:20)4cmTL)orpotentiallymatureindividuals(>4cmTL)[12,15–17].Theparameters
selectedforinterrogationwithmultivariatestatisticsinthecurrentstudyare:dailyarithmetic
meansofdischargeoftheRhine(ms-1)nearNPPP(PegelMaxau,Wasser-undSchifffahrt-
samtMannheim);watertemperature(˚C)oftheriver20kmupstreamofNPPPin(LUBW);
dailydurationofsunshinehours;precipitation(mlperday)anddailychangeinairpressure
(hPa)comparedtothepreviousday.Thelatterthreeparameterswereallmeasuredbya
weatherstation3kmsouthofNPPP(DWD).Othervaluesincorporatedintotheanalyseswere
coolingwaterintakeinms-1,timeofday(night,day,andnauticaltwilightaccordingtoGlar-
ner2006[18])andstudyyear.Thegeneralregressionmodelspecifiedthenegativebinomial
distributionfortheresponsevariablefollowingtheargumentationofO’HaraandKotze(2010)
[19],becauseofthehighnumberofzeroobservations.ApowerfulLassotechnique[20],well
suitedforlargedatasetswherecollinearityisoftenaproblem,wasusedtocondensetheinde-
pendentvariables.Toassesstheeffectstrengthofsignificantindependentvariablesinthe
modelformula,MonteCarlosampleswereobtainedbyresamplingtheobserveddata.This
wasdoneundertheassumptionthatfactorsareuncorrelatedandthattheirlikelyvalueswould
notberepresentedbyauniformdistribution.
AllstatisticswererunonJMPPro13.1.0(64bit,SASInstitute).
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Invasionstrategyandactivitytriggersforgobiids
Table1. Absolutenumbersofthe15mostdetectedspeciesinthesamplingcontainerofthePhilippsburgnuclearpowerplantbystudyyear;the
threegobiidspeciesinfocusarehighlightedinbold.
Species 2011 2012 2013 2014 Total
Roach(Rutilusrutilus) 118530 176123 525821 127774 948248
Bream(Abramisbrama) 51113 93584 538179 227809 910685
Perch(Percafluviatilis) 73693 90751 202005 428251 794700
Zander(Sanderlucioperca) 169635 33135 50791 195132 448693
Asp(Leuciscusaspius) 103932 7417 2366 5791 119506
Bleak(Alburnusalburnus) 17771 26151 24216 28515 96653
Roundgoby(Neogobiusmelanostomus) 1458 43033 26888 18899 90278
Three-spinedstickleback(Gasterosteusaculeatus) 10190 18505 37750 12207 78652
Commonnase(Chondrostomanasus) 28429 2854 3694 5237 40214
Ruffe(Gymnocephaluscernua) 6379 4161 11215 271 22026
Sealamprey(Petromyzonmarinus) 7290 5972 3596 1752 18610
Riverlamprey(Lampetrafluviatilis) 4405 6158 4065 1244 15872
Bigheadgoby(Ponticolakessleri) 4303 2102 8047 297 14749
Westerntubenosegoby(Proterorhinussemilunaris) 10466 1150 825 249 12690
Commondace(Leuciscusleuciscus) 5233 434 1.801 201 7669
https://doi.org/10.1371/journal.pone.0183769.t001
Results
Duringthestudyperiodatotalof6654592fishwerecountedinthesamplingcontainer.45.1%
ofthem(n=3001388)werelarvae(<2cmTL,mostlycyprinids)and46.6%(n=3102326)
wereroach(Rutilusrutilus),bream(Abramisbrama),perch(Percafluviatilis)orzander
(Sanderlucioperca)(cid:21)2cmTL.Theremainder(8.3%,all(cid:21)2cmTL,n=550878)belongedto
42differentteleosttaxaandthreelampreyspecies.Of46identifiedfishtaxa,33areconsidered
autochthonous,constituting84.6%ofthenaturalfishfaunaoftheRhine(n=39),while13are
allochthonous(Baeretal.2014).Inoverallabundanceduringthewholestudyperiod,round
gobywererankedinseventhplace(n=90278),bigheadgobyatthirteenth(n=14749)and
tubenosegobyatfourteenth(n=12690)(Table1).
Gobiidswererecordedinthesamplingcontaineralmostyearround,on91.5%ofstudy
days.
Therelativeproportionsofjuvenilegobiidsinthesamplingtankdifferedbetweenspecies:
22.1%oftubenosegoby,28.7%ofbigheadgoby,and51.1%ofroundgobywerebelowthe5cm
TLthresholdforpotentialadulthoodandwerethusregardedasjuveniles.Maximumrecorded
sizeswere20cmTLforbigheadgoby,19cmTLforroundgobyand16cmTLfortubenose
goby.
Thethreenon-nativegobiidsoccurredatallhoursoftheday,butthemajoritywere
recordedbetween9:00amand5:00pmthanatothertimes(Figs2and3).Theoccurrenceof
juveniletubenosegobypeakedinthesecondhalfofthenight(1:00–4:00am)andaround
dawn(7:00–8:00am)(Fig2);largerindividualswerefoundmainlybetween11:00pmand5:00
am,butweregenerallyabsentatdawn(Fig3).Nearly45%ofalljuvenilebigheadgobywere
detectedinthehourjustaftermidnight,withanothersmallerpeakbetween4:00and5:00am
(Fig2).Adultbigheadgobiesweredetectedaroundtheclock,withsmallpeaksinthelatter
halfofthenightandarounddawn(Fig3).Theoccurrenceofjuvenileroundgobiesincreased
aftersunsetandpeakedonehouraftermidnight,withasecondpeakarounddawn(Fig2).
Adultroundgobieswererecordedatallhours,withpeaksduringthesecondhalfofthenight
andarounddawnanddusk(Fig3).
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Invasionstrategyandactivitytriggersforgobiids
Fig2.Relativefrequenciesofjuvenilenon-nativegobiidsinanaverage24hourperiodbasedonindividuals
detectedinthesamplingcontainerduringthestudyperiod;notethediscontinuityofthey-axis,n=samplesize.
https://doi.org/10.1371/journal.pone.0183769.g002
Tubenosegobieswererecordedbetween1and1621individualsperday(mean±standard
deviationSD:20.1±516.5)on631studydays(48.5%ofallstudydays).Theyappearedmainly
duringApril,MayandearlyJuneandagaininSeptemberandOctober(Fig4).Bigheadgoby
werefoundon598studydays(45.7%),mainlyduringsummer(Fig4)between1and1968
individualsperday(mean±SD:49.2±612.0).Roundgobieswererecordedon998days
(76.3%)indensitiesbetween1and14193individualsperday(mean±SD:90.4±591.5),
mainlyduringsummerorautumn(Fig4).
Allthreespeciesofinvasivegobyexhibitedpulsedswarmingbehaviour,withmorethan
1000individualsdetectedwithinaonetotwohourperiodonafewdaysinsummer(Fig5)
and,inthecaseofroundgobyalsoduringautumn.Swarmingbehaviourwasparticularlyobvi-
ousfortubenosegobyonthreedaysin2011,forbigheadgobiesontwodaysin2013andfor
roundgobiesonfivedaysin2012,fivedaysin2013andtwodaysin2014(Fig4).Theexcep-
tionallyhighoccurrencesrecordedatthesetimesweremainlylimitedtothesecondhalfofthe
night(Fig5),butonthe18thand24thofAugust2013morethan1000roundgobiesperhour
werecaughtinthemorningbetween5:00–9:00amandononedayinOctober2012asimilar
captureratewasobservedarounddusk(17:00–18:00pm).Themeanbodylengthsof
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Invasionstrategyandactivitytriggersforgobiids
Fig3.Relativefrequenciesofadultnon-nativegobiidsinanaverage24hourperiodbasedonindividualsdetected
inthesamplingcontainerduringthestudyperiod;notethediscontinuityofthey-axis,n=samplesize.
https://doi.org/10.1371/journal.pone.0183769.g003
individualsrecordedduringswarmingeventswere5.1cmTL±0.9SDfortubenosesand4.3
cmTL±1.1SDforbighead,withnoindividuals>7cmTL.Bycontrast,TLsofswarming
roundgobiesrangedupto14cm(mean±SD:4.4cm±2.5).
Mostgobiidsdetectedinthesamplingtankduring2011(Table1)weretubenosegoby
(n=10466),withbigheadgobyadistantsecond(n=4303).Roundgobyaccountingforonly
8.9%ofallgobiidrecordsfortheyear2011(n=1458,Table1).Adrasticshiftwasrecordedin
2012whennearly93%ofallgobiidrecordsreferredtoroundgoby(n=43033,Table1).In
2013recordsofbigheadgobypeakedatupto8047individuals,representing25%ofallgobiids
(Table1).However,roundgobyremainedthemostabundantgobiidin2013(n=26888)and
by2014,bigheadandtubenosegobyhadalmostdisappeared,withroundgobymakingup
97.2%ofallgobiidrecords(n=18899,Table1).
Intermsofmonthlycatchcomposition,tubenosegobydominatedthenon-nativegobiids
untilJuly2011(Fig6),atwhichpointasharpincreaseofbigheadgobywasobservedresulting
inashiftofrelativeshare(Fig6).However,fromautumn2011,occurrencesofroundgoby
alsoincreasedandbyJuly2012thisspeciesbegantodominatethecatchofnon-nativegobiids
andcontinuedtodosofortheremainderofthestudyperiod(Fig6).Theexceptionwas
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Invasionstrategyandactivitytriggersforgobiids
Fig4.Absolutedailyoccurrence(n)ofgobiidindividualsinthesamplingcontainerbetween1stofApriland31stof
Octoberinthefourstudyyears;notethediscontinuityofthey-axis.
https://doi.org/10.1371/journal.pone.0183769.g004
summer2012(June),whenduringaphaseofgenerallylowgobiidactivity,largernumbersof
tubenosegobieswerefound(Figs4and6).Afinalpeakofbigheadgobyrecordsoccurredin
July2013duringnightswithover1000individualsdetectedinthesamplingtankonsome
nights(Fig4),butafterthatbothbigheadandtubenosegobyrecordsdwindledtoalmostnoth-
ing(Fig6).
Lookingintothemodelstatistics,studyyearwasrelevant(P<0.0001)fortheconsecutive
appearanceofround,bighead,andtubenosegoby(Tables2and3).Watertemperaturecorre-
latedpositively(P<0.01)withtheoccurrenceofjuvenilesofallthreespecies(Table2)and
adultsofbigheadandroundgoby(Table3).Incontrast,theoccurrenceofadulttubenosegoby
showsasignificant(P<0.0001)negativeinfluenceofwatertemperature(Table3).Fluvialdis-
chargewaspositivelycorrelated(P<0.0001)withtheoccurrenceofjuvenilebigheadgoby
(Table2)andnegatively(P<0.0001)withadulttubenosegobyrecords(Table3).Timeofday
appearedtobeofminorimportancebutcorrelatedsignificantlywiththeoccurrenceofjuve-
nile(Table2)andadulttubenoseandroundgoby(Table3),thoughratesdiffered.Thevolume
ofcoolingwaterintakecorrelatedpositivelywiththeoccurrenceofjuvenilebighead(P<0.01)
androundgoby(P<0.0001)(Table2)andcorrelatednegativelywithrecordsofadultbighead
goby(P<0.01)(Table3).Themodelshowednosignificanteffectsofthemeteorological
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Invasionstrategyandactivitytriggersforgobiids
Fig5.ExamplesofpulsedswarmingbehaviourofP.semilunarisonthe13thofJune2011andofP.kessleriandN.
melanostomusonthe26thofJuly2013;notethediscontinuityofthey-axis.
https://doi.org/10.1371/journal.pone.0183769.g005
factorsprecipitation,sunshinedurationorchangeinairpressurefortubenosegoby,butrec-
ordsofjuvenileroundgobywerenegativelyaffected(P<0.05)bychangingairpressure
(Table2),occurrenceofadultroundgobiesincreasedwithprecipitation(P<0.01)(Table3)
andthedetectionofadultbigheadgobywasnegativelyinfluencedbyincreasingsunshine
hours(P<0.0001)(Table3).Theinteractionofthetwoparametersdischargeandwatertem-
peraturehadaninfluenceonthedetectionrateofjuvenileroundgoby(P<0.0001)(Table2)
andadulttubenosegoby(P<0.0001)(Table3).Overall,themodelstatisticsexplained15–
20%ofobservedvariationingobyrecords(Tables2and3).
ElectricfishingsurveysintheRiverRhinein2008yieldednogobiidrecords.Thefirsttube-
nosegobieswerecaughtupstreamoftheNPPP(Table4)in2009.Bigheadgobiesbegantobe
recordedin2010,bothup-anddownstreamoftheNPPP,thoughtubenosegobystilldomi-
natedthecatch(Table4).In2011thefirstroundgobieswerefoundandbigheadgobieshad
increasedasaproportionofcatch(Table4).From2012onwardsroundgobiesincreasedenor-
mouslyandbigheadandtubenosegobiesnearlydisappeared(Table4).Intherecentpast
(2015)roundgobiescontinuedtobefoundinhighdensities(0.3–0.5individualsm-2)and
tubenoseandbigheadgobiesarecomparablyrare(Table4).Anotherspeciesofgobyrecently
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Invasionstrategyandactivitytriggersforgobiids
Fig6.Changesinrelativeshareofthenon-nativegobiidsinthemonthlycatchduringthestudyperiod.
https://doi.org/10.1371/journal.pone.0183769.g006
detectedapproximately250kmdownstream(monkeygobyNeogobiusfluviatilis,Borcherding
etal.2011),wasnotrecordedinthisstudy.
Discussion
ResultsfromthemonitoringofthecoolingwaterintakeofNPPPagreewiththoseoftheelec-
tricfishingsurveys,andbothtechniquesrecordthesametrendsingeneralabundanceofthree
non-nativegobiids,includingtherapiddeclineoftubenoseandbigheadgobyaftertheappear-
anceofroundgoby.However,thevolumeandexceptionallyhightimeresolutionofdatafrom
thecoolingwaterintakeandtheinterpretationoffishrecordsthereinasaproxyforfishactiv-
ityoffersauniqueopportunitytoinvestigatepotentialmechanismsunderlyingtheparallel
invasionsoftubenose,roundandbigheadgoby.
Borcherdingetal.(2013)[10]pointedouttheimportanceofcircadianfactorsinforming
theecologicalnichesoftheRhine’sthreeinvasivegobiids.Informationpertainingtothe24
houractivityofthesespeciesisscarce,especiallyoutsidetheirnativerange.Dopazoetal.
(2008)[13]reportedthattheproportionofroundgobyinnighttimecatcheswasdoublethat
recordedduringtheday.Borcherdingetal.(2013)[10]recordedsignificantlygreaterdensities
ofroundgobyinsurveysconductedtwohoursaftersunsetthaninsamplestakendirectlyafter
sunsetorduringthedaytime.Jana´četal.(2013)[21]reportedthatthedriftoflarvaltubenose
androundgobyoccurredalmostcompletelyduringhoursofdarknessandthatinbothspecies
PLOSONE|https://doi.org/10.1371/journal.pone.0183769 September15,2017 10/16