the impact of exotic trout on native charr in a japanese stream

8/2/2019 The Impact of Exotic Trout on Native Charr in a Japanese Stream

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The Impact of Exotic Trout on Native Charr in a Japanese StreamAuthor(s): Kentaro Morita, Jun-Ichi Tsuboi, Hiroyuki MatsudaReviewed work(s):Source: Journal of Applied Ecology, Vol. 41, No. 5 (Oct., 2004), pp. 962-972Published by: British Ecological SocietyStable URL: http://www.jstor.org/stable/3505811 .

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Journalof AppliedEcology 200441,962-972

METHODOLOGICAL INSIGHTSTheimpactof exotictroutonnativecharr n a JapanesestreamKENTARO MORITA*j, JUN-ICHI TSUBOIt and HIROYUKI MATSUDA*?*Ocean ResearchInstitute, Universityof Tokyo,1-15-1 Minamidai, Nakano-ku, Tokyo164-8639, Japan,; ndt YamanashiFisheriesTechnologyCenter, Ushiku, Shikishima, Yamanashi400-0121, Japan

Summary1. Regressionandisodar methods developed by community ecologists providetools forevaluatingthe existence and magnitude of interspecificinteractionsin the field. In thisstudy,we examinedthe usefulness of both methods to assess the impact of exotic trouton native charr.2. Brown trout Salmo trutta and rainbow trout Oncorhynchusmykisshave been intro-duced world-wide. They are invading many streamsin Japan that also harbour nativesalmonids. We studied these species and the endemic Asian white-spotted charrSalvelinus leucomaenis in the Hekirichi River, south-western Hokkaido, Japan. Weestimated the densities of all three species in pools and riffles from 27 stream reachesover 2 successiveyears.Data were analysed by regressionand isodar methods to inferinterspecificinteractions.3. The regressionmethod identified a negative relationship between brown trout andwhite-spottedcharrdensities, mplying hat brown trout arereplacingwhite-spottedcharr.4. The isodar method identified significant competition for habitat between rainbowtrout and white-spotted charr. This method suggested that white-spotted charr pre-ferredpools to riffleswhen rainbow trout were scarce but moved frompools to riffles astrout density in the pools increased.5. Synthesisandapplications.Although they are based on limited data, regressionandisodar methods were able to evaluate the potential impact of exotic trout on nativewhite-spottedcharr.Fromtheseresults,we were able to hypothesizemechanisms of dis-placement of native charrby exotic trout. However,according to the two methods themechanisms underlyingthe negative impacts on charr differ between brown and rain-bow trout; in other words, limitations exist for both methods. From a more practicalviewpoint, the analyses conducted in this study may be useful tools for conservationbiologists who have limitations on their time and effort but must assess the impacts ofexotics on native species.Key-words:biological invasion, competition coefficient,habitat shift, ideal free distri-bution, introduced species, isodar, non-native troutJournalof Applied Ecology (2004) 41, 962-972

IntroductionInvasionby exoticspecies s thoughtby manyecolo-giststoplaya keyrole ndiminishinghe size of nativejPresent address and correspondence: Kentaro Morita,Hokkaido National Fisheries Research Institute, FisheriesResearch Agency, 116Katsuragoi, Kushiro 085-0802, Japan(e-mail [email protected]).?Present address: Graduate School of Environment andInformation Sciences, Yokohama National University,Hodogaya-ku, Yokohama 240-8501, Japan.

animaland plant populations,and much efforthasbeenputintodeterminingts existence ndmagnitude(Williamson 996;Ormerod 003).In freshwaterys-tems,salmonid ishesareamong hemostwidespreadintroducedpecies orcommercial ndsports isheries(Lever 996;Fuller,Nico&Williams 999).Brown routSalmo truttaL. and rainbow troutOncorhynchusmykissWalbaum,nparticular,avebecome stablishednfivecontinentsandseveralslands,andhaveconsequentlybeen listed among the most serious invasive alien spe-cies by the IUCN (the world conservationunion; Lowe? 2004British

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963Impacts of exotictrout on nativecharr

et al. 2001). Numerous studies have investigated theimpactof introduced routon nativebiota(Krueger& May 1991; Crowl, Townsend & McIntosh 1992;Townsend 1996;Dunham et al. 2002). However,moststudies have been conducted in only a few regions, pri-marily in North America and Australasia. Studiesfrom other geographical regions,under different bioticand environmental conditions, are needed for a moregeneral understanding of the impact of introducedbrown and rainbow trout.In Hokkaido Island, northern Japan, exotic brownand rainbow trout increasingly expanded their distri-butions in the last quarter of the 20th century. Thisongoing invasion is probably the result of intentionalintroductions for sport fishing and the lack of legalregulationsrestrictingtheir releaseinto naturalwaters.Brown trout were first introduced in Hokkaido Islandin 1978, and have since expanded theirdistribution;todate, they have been caught in 42 rivers (Takami &Aoyama 1999; Kudo 2001). Rainbow trout were firstintroduced in Hokkaido in 1920 but did not expandtheir distributionuntil sport fishingbecamepopular inthe 1970s Takami&Aoyama 1999).The numberof siteswhere rainbow trout have been caught has expandedfrom only five rivers in 1970 to 72 rivers in 1997(Takami& Aoyama 1999). Given this expansion, con-cerns have emerged over the impacts of brown andrainbow trout on endemic Asian salmonids, includingmasu salmon Oncorhynchusmasou Brevoort, white-spottedcharrSalvelinuseucomaenisPallasandSakhalintaimen Hucho perryi Brevoort (Kitano et al. 1993;Aoyama et al. 1999; Taniguchi et al. 2000; Takamiet al. 2002a;Taniguchi,Fausch & Nakano 2002). Con-sequently,in this study,we were interested in studyingthe potential for interspecific interactions betweenexotic trout and native salmonids under natural condi-tions in Japanesestreams.A variety of methods for evaluating the existenceand magnitude of interspecific interactions in thefield have been developed (Rosenzweig et al. 1985;Morris 1989;Pfister1995;Fox & Luo 1996;Shenbrot&Krasnov 2002). A traditionalapproachuses the regres-sionmethod,bywhichthedensityof a species sregressedagainst the densities of supposed competitors. Signi-ficantnegativerelationshipsmplythe existence of inter-specific interactions.This method has been applied instudies investigating interspecific interactions amongstream fishes (Townsend & Crowl 1991; Fausch,Nakano & Ishigaki 1994). However, because habitatheterogeneitycan also affect density, several modifiedregressionmethods incorporatingthe effects of habitatvariables have been proposed (Crowell& Pimm 1976;Rosenzweig, Abramsky & Brand 1984; Fox & Luo1996).Morris(1988,989,1990,1994,1999, 003)developedthe sodarmethod oinvestigatentra-and nterspecificcompetition from census data. This method models thedensities of multispecies communities in two types ofhabitat(e.g. pools and riffles) by adopting the ideal free

distribution theory (see the Materials and methods)proposedbyFretwell& Lucas(1970).The isodarmethodcan evaluatehabitat-dependent nterspecificnteractionsas well asqualitative ndquantitativedifferencesbetweentwo types of habitat, and overcomes the shortcomingsof traditional regressionmethods (Morris 1989).

Despite the development of the regressionand iso-darmethods, few studies haveappliedthesemethods toevaluate interspecificinteractions between exotic andnative species. Because both methods can be appliedwith limited data on density, they may be useful toolsfor conservation biologists who must rapidly assessthe impacts of exotics on native species. Our studydescribed an application of regression and isodarmethods to assess interspecific interactions amongthree salmonid fishes (browntrout, rainbow trout andwhite-spotted charr)in a Japanesestream.Specifically,our aims were to assess the impactsof exotic brown andrainbow trout on the endemic Asian white-spottedcharr,and to discuss the usefulness and limitations oftraditional regressionand isodar methods.

Materials andmethodsISODAR THEORYThe isodar method models the population densities ofmultispeciescommunitiesin two habitats.If travelcostsbetweenthe two habitats are negligibleand individualsare distributed to maximize their fitness, the realizedfitness should beequal betweenthe two habitats(i.e.anideal freedistribution;Fretwell& Lucas1970). Recently,Kawaguchi, Taniguchi & Nakano (2003) showed thatstream-dwellingsalmonids exhibited an ideal free dis-tribution in fieldexperiments n whichthe inputof foodwascontrolled.Theisodarequationthat definesdensitieswherefitness is equal betweentwo habitats is given by:

Wo NAI + XiN il=W -C -b NA +y Pi2eqn 1

where W0s the basic fitness n habitat1,andNi and Ni2representthe densities of species i in habitats 1 and 2,respectively.The left side of the equation denotes thefitnessof speciesA in habitat 1,and the rightside of theequation denotes the fitness of species A in habitat 2.The isodar intercept, C, indicates the quantitative dif-ference in fitness between the two habitats. The isodarslope, b, indicates the qualitative difference in fitnessbetween the two habitats,a and 3, re habitat-specificcompetition coefficients for each i species, i.e. the con-version factor for expressing species i in units of speciesA. Rearranging equation 1 gives:NAl = C + bNA2 + bPiNi - aN,, eqn 2i*A i+Awhich can be easily estimated by multiple linear re-gression. Morris (1989) further extended the isodar

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964K Morita,J-I. Tsuboi&H. Matsuda

equation by incorporating the interaction terms NA,x N,, and NA2 Ni2. He suggested that the additiveeffects represent exploitative competition and that theinteraction effects representinterferencecompetition.Morris et al. (2000), however,acknowledged that thisdistinction may not be perfect. Morris (1990) sug-gested that the isodar method could also apply to anideal despotic distribution and an ideal pre-emptivedistribution.

The isodar method has been applied and its validityhas been examinedin studies investigatingcompetitionamong small mammals (Ovadia & Abramsky 1995;Morris et al. 2000; Morris, Davidson & Krebs 2000).This method can also beapplied o stream ishes,becausestreams are easily classified into two habitats: poolsand riffles(Hawkinset al. 1993).Rodriguez (1995) firstexamined competitive interactions between Atlanticsalmon Salmo salar L. and brook charr Salvelinusfon-tinalis Mitchill using the isodar method, and the resultswere nagreementwithdata obtainedbyotherempiricalstudies.To ourknowledge,no other studies haveappliedthe isodar method to stream fishes.

STUDY SITEOur field study was conducted in 2002-03 in the head-water reaches of the Hekirichi River, south-westernHokkaido, Japan(Fig. 1).The river s about 25 kmlongand dischargesinto the Pacific Ocean. We established27 studyreaches(47 ? 13 m, mean? SD) upstreamof a

reservoir. Each study reach consisted of one pool andone riffle.For the isodarmethod, we assumednegligibletravelcosts betweenadjacentpools and riffleswithin thereaches,but not between the reaches.Thestudyareahadtwo obstructions to fish migration. A gorge betweenreaches 15 and 16 and a smalldam(1-5m high)betweenreaches25 and 26 inhibited upstream migration. How-ever,these obstructions did not completely preventfishfrom moving upstream.

Water emperaturemeasuredwith dataloggers(Stow-AwayTidbiT;OnsetComputer,Bourne,MA) from lateJulyto September2002 at reaches 1and 27 were 14-1 ?1-4oC and 11-6+ 0-9 'C (mean ? SD), respectively.Temperaturesn the studyarea weregenerallyhigheratupstreamreachesthanat downstreamreaches,probablydue to the stream being spring-fed around the middlereach.

Brown trout eyed eggs wereintroducedin 1990nearreach 26 by an angler (anonymous, personal commu-nication), and rainbow trouteyed eggswere introducedin 1994-98, primarily in a headwater tributary, byanotherangler(anonymous,personalcommunication).Although these personal communications lack inde-pendent verification,neither rainbow nor brown troutwere captured in the course of the Hekirichi Riverduring year-roundobservationsbetween 1971 and 1977(Goto et al. 1978). In 1995,no rainbow trout or browntrout were observed upstreamof the gorge, but browntrout were observed around reach 26 (K. Morita, per-sonal observation). In 2001, both rainbow and brown

1400E 1440EN The Hekirichi Rivers y s t e m 4 4 0 NHokkaidoS Island

Rainbow rout elease42N2 km StudyareaBrown rout elease

R e s e r v o i r

- - - - -

234 56

79 10 11 12c 13 14 c18

G o r g e

S m a l l dam P a c i f i c o c e a n

Fig. 1. Locationandmapof the HekirichiRiver, outh-westernHokkaido,Japan.Numbers ndicate helocationsof surveyed eaches.

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troutwereobserved,ndbrownroutwere hedominantsalmonidsrom he inlet of the reservoiro themouthof the HekirichiRiver Kanzawa 002).Therefore,t isreasonableo assume hatbrownroutwere stablishedroughly10 yearspreviouslyand that rainbow routwereestablishedoughly5yearspreviously.Native fishes inhabiting he study area includedwhite-spottedharr,wrinkleheadculpinCottusnoza-waeSnyder nd ar-easternrook ampreyLethenteronreissneriDybowski.Unfortunately ehaveno quanti-tative nformation n theabundance f white-spottedcharrprior o the introduction f brownand rainbowtrout.

FIELD OBSERVATIONSWeconductedishcounts neachpoolandriffleof the27 reachesby underwaterbservationswith snorkel-ling gear n July2002andJuly2003(Thurow1994).Oneauthor quippedwithawetsuit,maskandsnorkelentered he streamat thelowerendof each reachandcrawledlowlyupstreamnazigzagpatternduring hedaytime. almonidswere ounted,dentifiedospecies,andclassifiednto100-mmengthgroups < 100,100-199,200-299,> 300mm).Newlyemergedry 0+fish)werenotcounted.Recent tudieshaveconfirmedhatunderwater bservationsmade with snorkelling earprovideunbiased stimatesof the relativeabundanceand ize tructuref stream-dwellingalmonidsThurow& Schill1996;Mullner,Hubert&Wesche 998).Unfor-tunately,pools of two reacheswerechokedwith finesedimentn 2003andwere herefore xcludedrom he2003observations,esultingn data roma totalof 52pairsof adjacent oolsandriffles27and25reaches or2002 and2003,respectively). s mortalityand move-mentarebothsupposedo behigh,manyof the fishesin rifflesand pools could be different n successiveyears.Weassumed hatsamplesakenayearapartwererelativelyndependent.Wemeasuredhephysical haracteristicsf 27studyreachesnJuly2002.Thecentreengthof eachpoolandrifflewas measured. treamwidthandsubstrateweremeasuredat threeevenly spacedtransectsalongthelengthof eachpool and riffle 1/4, 1/2,3/4).Substratecompositionwas quantified ollowingBain, Finn &Booke(1985). Depth and velocitywere measured tthree venly pacedpoints 1/4,1/2,3/4)along hethree

transects(i.e. 3 x 3 points at each pool and riffle).Velocitywasmeasured t 60%of the depthfromthesurface obed(meanwater olumnvelocity;Gatz,Sale& Loar1987) sing propeller-typeeterCR-7;CosmoRiken,Osaka,Japan;Tanida,Yamashita& Rossiter1985).Physical haracteristicsf poolsandriffleswererelativelydiscrete(Table1). No significantgradientalongthewatercoursexisted oreachphysical harac-teristic (r2= 0-01-0-08, P = 0-156-0-926) except fordepthn rifflesr2= 0-16,P =0038).Thedepthofrifflesincreased ownstream.

STATISTICAL ANALYSESWeanalysed he relationshipsbetween he densitiesof brown rout,rainbowroutandwhite-spottedharrusing two differentmethods.First, the traditionalregressionmethodwas performed t the reach unitscale.The densitiesof pairedpools and riffleswereaveragedn eachreach,n eachsurvey ear. nadditionto simpleregression nalysis, he standardized rin-cipal componentanalysis(PCA)residualregressionsuggestedbyFox & Luo (1996)was used to estimatecompetition oefficients. ourphysical haracteristicsof eachpool and riffle Table1)wereused as habitatvariables. he set of eighthabitatvariables romeachreachwasreducedo threeprincipal omponents, ndthendensitieswerestandardizedsingthesevariables(PCAresidualmethod;Rosenzweig t al. 1985;Fox& Luo 1996).Secondly, he isodarmethod was per-formedat thepool/riffleunit scale.We used methodsestablishedby Morris et al. (2000) to estimatetheisodar quation s follows.Because he sodar quation(equation )assumes hat thedependent peciesoccu-piesbothhabitats,hesubsetof pairedpoolsandriffleswheretarget speciesoccurred n both habitatswasselected,resultingn 31pairsforwhite-spottedharr,20 pairs or brown routandonlythreepairs orrain-bow trout.Therefore,heisodarequation orrainbowtrout was not estimated, lthough he rainbow routwere ncludednthe sodarequationsor theother wospecies.Usingthedensityof eachspeciesneachhab-itatas thedependent ariable ndotherdensities s theindependentvariables,a model I stepwisemultipleregression asperformedoidentifya subsetof signif-icant sodarparametersP < 0.05to add and P > 0.10to remove).Beforecalculatinghe interactionerms,

Table1. Physical haracteristicsf poolsand riffles n thesurveyedeachesmean? SD)Pools (n = 27) Riffles (n = 27) t P

Width (m) 8-63? 1-54 11.40+ 3-30 3-95 < 0.001Depth (cm) 83-02? 16-47 38.64? 10-33 11-86 < 0.001Velocity (cm s-') 42-81 ? 9-39 81.33 ? 14-77 11-43 < 0.001Substrate code 3-51+ 0-43 3.92 + 0-39 3-67 < 0.001Substrate code followingBain, Finn & Booke (1985): 1,sand-silt (< 2 mm);2, gravel(2-16 mm);3, pebble(17-64 mm);4, cobble(65-256 mm); 5, boulder (> 256 mm); 6, irregularbedrock.

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the densities were centred and standardized (i.e. z-transformation) o removecollinearity(Rodriguez1995;Morris et al. 2000). Because all densities are subjecttomeasurement error, the values of isodar parametersmust be estimated by a model II regression (Morris1989; Rodriguez 1995; Morris et al. 2000). Model IIregression estimates were obtained by the reducedmajor axis or standard minor axis methods, followingMcArdle (1988). The bootstrap bias-correctedpercen-tile confidence limits were calculated for each isodarparameterfrom 1000bootstrap samples (Manly 1997).To address non-linear relationshipsbetween densityand fitness, log,(x + 1) transformations were used fordensities prior to statistical analyses (Morris 1994;Rodriguez 1995). Yearly data were pooled for thestatistical analyses, but year-specific symbols wereused in figuresto visualize year effects.

ResultsDISTRIBUTION PATTERNSThree species of salmonid fish co-occurred within thestudy area(Fig. 2). White-spotted charr were observedthroughout the study area, but were less abundantdownstreamof the gorge. Conversely,brown trout weredominant downstream of the gorge, while rainbowtrout were relatively abundant in the centre of study

area. Densities of all species were higher in poolsthan in riffles (Mann-Whitney U-test; white-spottedcharr P < 0-001;browntrout P < 0-001;rainbow troutP < 0-001). In particular,rainbow trout occurred onlyin pools, with the exception of three reaches in 2003.Similarly,upstreamof the gorge,wheretheywerescarce,brown trout were observed only in pools. Thus, exotictrout initiallyinvadedpools. Fish in pools tended to belarger than those in riffles, but significant differenceswere detected only for brown trout (Mann-Whitney U-test; white-spotted charr P = 0-155, n = 279; rainbowtroutP = 0-213,n = 114;brown routP = 0-049,n = 226).

REACH UNIT REGRESSION METHODAt the scale of thereach,white-spottedcharrdensitywassignificantly negatively related to brown trout densitybut not to rainbow trout density (Fig. 3; brown troutr = -0-711, P < 0-001; ainbow routr = 0-061,P = 0-670).Thedensityof charrdramatically ecreasedwith ncreasedbrown trout density. The relationship between charrdensityand rainbow routdensitywas stillnot significant,even after controlling for brown trout density (partialcorrelationanalysis,r = -0-160, P = 0-263).Competitioncoefficients of brown and rainbow trout on charr,esti-mated by standardizedPCA residualregression(Fox &Luo 1996), were -0-571 ? 0-113 (t = 5-065, P < 0-001)and -0-020 + 0-139 (t = 0-144, P = 0-886), respectively.

-0- White-spottedharr- 10 - --+- Brown troutJuly 2002 - Rainbow trout8 o

-0 ?+6 0o-2 - o O+o oo o0 0-2 0-o- 0 0-00o + 0) + --

+

0 5 10 15 20 250 -July 2003--+

_ +

/o0 000 o +-+-+-+ +-2o-o /0 0 ++ +4.-4

5 10 15 20 25Upstream DownstreamReachnumber

Fig.2. Densitiesof brown rout,rainbow rout andwhite-spotted harr n pools and rifflesof each surveyed each n theHekirichiRiver n 2002 and 2003. Boldgrey ines ndicate he locationsof imperfect arriers o fishmigration.

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2-0 2-0r = -0-711, P< 0001 r = 0-061, P = 0-670

? 0a c*I *,

o o

S? ? 00 nn

0-0E- S MEg0 0 0-- *gNEM0-0 * mu * * o-o mmmu0o0 1-0 2-0 0-0 1-0Brown trout density Rainbow trout density

Fig.3. Relationshipsmongbrown rout,rainbow routandwhite-spottedharrdensities mongreaches logscale).Filledcirclesandsquaresndicatedata rom2002 and2003,respectively.Table2. Summary f stepwisemultiple egressionor dentifying ignificantsodarparametersDependent ariable Predictor ariables Remainingariables nCP CR***,RP*** BP,BR, RR,CPx BP,CPx RP,CR x BR,CRx RR 31CR CP***,RP** BP,BR, RR, CPx BP,CPx RP,CRx BR,CRx RR 31BP BR** CP,CR, RP,BPx CP,BPx RP,BRx CR 20BR BP***,RP* CP,CR,BPx CP,BP x RP,BR x CR 20***P < 0-001, **P < 0-01, *P < 0-05.CP,white-spottedharrdensitiesnpools;CR,white-spottedharrdensitiesnriffles;BP,brown routdensitiesnpools;BR,brown routdensities nriffles;RP,rainbow routdensities npools;RR, rainbow routdensities nriffles.

POOL/RIFFLE UNIT ISODAR METHODIn contrast to the reach unit regression method, theisodar regressions identified significant competitiveinteractions between charr and rainbow trout, but notbetween charrand brown trout (Table 2). The model IIregressionestimates of the isodar equations for charrand brown trout were:CP= 4-753CR[3.1916.525] 0828 RP[0.289-1.483]

- 0-178[-1.415-1.218]CR = 0-210 CP[0O149-0.300] 0-174 RP[O.060-0.305] eqn 3+ 0-037[-0-229-0-247]andBP = 1-108BR[0757-1.496]+ 0-480[0.169-0.760] eqn4BR = 0-951BP[0718-1.568]0-479[1.193 (-0151)]where CP, RP and BP representthe pool densities ofwhite-spotted charr, rainbow trout and brown trout,respectively,and CR and BR are the riffledensities ofcharr and browntrout, respectively.Numbers inparen-theses indicate 95% confidence intervals. The effect ofRP on BR was not consideredherebecause it was onlymarginallysignificant(Table2).In pools, charr density decreased with increasingrainbow trout density but not with increasing browntrout density (Fig. 4). Charrdensity in riffles ncreased

with increasingcharrdensityin pools and with increas-ing rainbow trout densityin pools (Fig. 4). Brown troutdensity in riffles ncreased with increasingbrown troutdensity in pools (Fig. 5). The isodar slope for charr wassignificantly greater (or smaller) than 1 (equation 3),indicating that pools were qualitatively superior toriffles for this species. The isodar intercept for browntrout was significantly greater (or smaller) than 0(equation 4), indicating that pools were quantitativelysuperior to riffles for brown trout. Thus, the isodarmethod suggested that both white-spotted charr andbrown trout were density-dependent habitat selectorsthat showed a preferencefor pools. Moreover,the hab-itat suitability for white-spotted charr declined withincreased densities of conspecifics and rainbow trout,and habitat suitability for brown trout declined withincreaseddensity of conspecifics.

DiscussionBy examining the covariations in population densitiesamong and within pool/riffle units, we deduced inter-specificinteraction between exotic brownand rainbowtrout, and native white-spotted charr. The regressionmethod assessedcompetition at the landscape scale bydetectingdifferencesn densitiesamongreaches,whereasthe isodar method assessed habitat shifts driven bycompetition at the reach scale by detecting differencesin habitat use between two types of habitat (pool andriffle in this case). Although they are based on limiteddata, the regressionand isodar methods can, to some

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r = 0652, P < 0-001 10 r = -0-610, P < 0-0010 . . 0 t

m m0.o-00 0 U@. -0

..-5 0 05 1 . . .1"0 -0-5 0-0 0-5 1.0o-m5noCharr in pool Rainbow trout in pool

? O io

-0-5

r =

0,464,

P=

0.00..

r = 0109, P= 0

,558

-1-0 -0-5 0-0 0.5 1-0 1-5 -0.5 0.0 0-5Rainbow trout in pool Brown trout in pool

Fig.4. Fourpartialresidualplotsfor thesignificantsodarparameters P,CR, RP,BP and BR (Table ). Filledcirclesandsquaresndicate ata rom2002and2003,respectively.n theseplots, hedependentariable nd he ndependentariablewerebothregressedgainst he othervariables,nd the residualsoreachregression ereplottedagainst achother Montgomery,Peck&Vining2001).

1-5 - r=0-658, P = 0002

* E- 0.5

0.00-0 1-0 2.0Brown rout npool

Fig.5. Relationshipsetweenbrown routdensity n poolsandin riffles logscale).Filledcirclesandsquares epresentdata rom2002and2003,respectively.

extent, successfully and quantitatively evaluate theimpact of exotic trout on native white-spotted charr.An unexpectedoutcome fromthis studyhas been thecontrasting results that emerged from the regressionand isodarmethods. The traditionalregressionmethodidentifieda negative relationshipbetween brown troutandwhite-spottedcharrdensities,but theisodarmethodsuggestedno competitionfor habitat betweenthese twospecies. In contrast, the regression method identifiedno relationship between rainbow trout and white-

spottedcharrdensities,but the isodar method suggestedsignificant competition for habitat between rainbowtroutandcharr.Thesecontrastingresultswould suggestthat the mechanisms underlying the negative impactson charr differ between brown and rainbow trout; inother words, limitations exist for both methods.

DISTRIBUTION PATTERNSAll three fish species preferred pools to riffles. Thispattern is particularly pronounced among Japanesestream-dwellingalmonids Inoue,Nakano & Nakamura1997;Sagawa,Yamashita& Nakamura2002).Comparedwith riffles, pools are superior habitats energetically(Rosenfeld & Boss 2001), so fish should aggregate inpools. Our results suggest that brown and rainbowtrout first colonized pools and then moved towardsriffleswhen their densities in pools increased.The three study species showed longitudinal varia-tionin distribution: ativewhite-spotted harrdominatedupstream of the gorge; exotic brown trout dominateddownstreamof thegorge;and exotic rainbowtrout weredistributed around the gorge. Stocking locations mayexplain this longitudinal distribution of exotic trout inthe Hekirichi River. Generally, exotic trout colonizeareas downstream from the stocking location, ratherthan dispersing upstream against the flow and acrossphysical barriers (Adams, Frissell & Rieman 2001;Dunham et al. 2002), although upstream expansion

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does occur(Closs& Lake1996;Peterson& Fausch2003).Brown trout and rainbow trout might be abundant atdownstream and intermediatereaches,respectively, orthis reason (see stocking locations in Fig. 2). In con-trast, the longitudinal distribution of native white-spotted charrmay be indicative of theirreplacement bybrown trout.

Temperature gradient is also an important factoraffectingthe distribution of stream-dwellingsalmonids(Taniguchi et al. 1998; Taniguchi & Nakano 2000;Dunham et al.2002)butit could not explain ongitudinaldistribution in the Hekirichi River. Mean summertemperaturesat the most upstream and downstreamreachessurveyedwere 14 1 ?Cand 11 6 ?C,respectively(see the Materials and methods). On the other hand,summer temperaturewas near 20 'C downstream ofthe reservoir,where brown trout dominated (Kanzawa2002). Thus, brown trout dominated both the coldestand warmest areas in the Hekirichi River. Moreover,because both brown and rainbow trout were estab-lished after 1990 (i.e. less than c. five generations), thecurrent distributions do not represent he limitsof theircapabilities.

BROWN TROUT EFFECTSON WHITE-SPOTTEDCHARRThe reach unit regressionmethod identified anegativerelationship between brown trout and white-spottedcharrdensities,implyingthat brown trout had replacedcharr.However,the pool/riffle unit isodar method sug-gested no competition for habitat between brown troutand white-spotted charr. Previous diet analyses alsosuggestedlittleniche overlapbetween these two species.Most white-spotted charr are drift foragers, feedingmainly on terrestrial insects (Nakano & Furukawa-Tanaka 1994; Morita & Suzuki 1999), whereas manybrowntroutarebenthivorousorpiscivorous nJapanesestreams (Mayama 1999;Kanzawa 2002; Takami et al.2002b). Therefore,both the isodar method and previ-ous diet analyses suggest that competition for feedinghabitats is not very strong between brown trout andwhite-spotted charr.However,competition for feedinghabitats between the two species should not be ruledout (cf. Takami et al. 2002b).

There are two possible alternative mechanismsunderlying henegative mpactsof browntrout on charr.First, predation on fry could be important. Althoughpredation by brown trout on white-spotted charr fryhas not beenreported,brown trout arefrequentlypisci-vorous in Japanese streams (Mayama 1999; Kanzawa2002). Mayama (1999) reported that 24% of browntrout (54-189 mm in fork length) fed on masu salmonfry in the Chitose River, Hokkaido Island, Japan.Secondly,reddsuperimpositioncould be an importantmechanism.The mainspawningperiodsof white-spottedcharr and brown trout are October and December,respectively (Aoyama 2002; Morita & Morita 2002).Therefore,ater-spawningbrowntroutmay superimpose

their redds on those previously constructed by white-spotted charr, leading to increased mortality duringincubation of white-spotted charr embryos (cf.Taniguchi et al. 2000; Wakabayashiet al. 2002). Bothpredation on fry and redd superimposition by browntrout could substantially decrease recruitmentamongwhite-spotted charr; therefore, negative relationshipsbetween brown trout and white-spotted charrdensitiesmightbe identifiedby the reach unit regressionmethodrather than by the isodar method. This does not meanthat the isodar method failed to document competitionbut that the isodar method correctly documented nocompetition for habitats.

RAINBOW TROUT EFFECTS ON WHITE-SPOTTED CHARRThe reach unit regressionmethod did not identify anyrelationshipsbetween rainbowtroutand white-spottedcharr densities; however, the pool/riffle unit isodarmethod identified competition for habitat betweenthese two species.Previous diet analysesalso suggestedthatcompetitionforfoods could occur betweenrainbowtrout and white-spotted charr. Both fishes are driftforagers, feeding mainly on terrestrial nsects (Nakano& Furukawa-Tanaka1994;Nakano et al. 1999).There-fore,our isodar method andpreviousdiet analysescon-sistently suggest that competition for feeding habitatsoccursbetween rainbowtroutandwhite-spottedcharr.In fact, aggressiveinteractions between rainbow troutand charr were frequentlyobserved during the under-water observations in this study.An interesting findingof this studyis that charrden-sities in riffles increased with increasingrainbow troutdensities in pools. The isodar method suggested thatwhite-spotted charr preferred pools to riffles whenrainbow trout were scarce,but that charr moved frompools towardrifflesas rainbow trout densities in poolsincreased(see equation 3); in other words, charr werepossibly displacedfrompools to rifflesbyrainbow trout.This density-dependent behaviour would mitigate thedirectnegative impact of rainbow trout; therefore,thereach unit regression method might not identifyrelationshipsbetweenrainbow trout and white-spottedcharr densities. Similar habitat segregation has beendocumented previously (Hartman 1965; Glova 1986).Hartman(1965)showed that coho salmon and steelheadtrout occupied pools and riffles,respectively;however,both species preferredpools to riffles when the specieswere allopatric. Young (2001) experimentallyshowedthat a diverse habitat including both pool and rifflemitigated interspecific competition among juvenilesalmonids,and he suggested that habitatdiversity pro-motes species diversity.However,we speculatethat theimpactof rainbow routwill besubstantialwhen rainbowtrout increase in density and invade riffles as a resultof intraspecific competition. It is known that rainbowtrout can utilize high velocity riffles(Cunjak & Green1983; Bisson, Sullivan & Nielsen 1988).

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IMPLICATIONSWe found significant negative effects of exotic brownand rainbow trout on native white-spotted charr.Robust legislationthat is enforcedeffectively enough topreventexotic trout fromexpandingtheir distributionsis thereforeneededurgently.Both the regressionmethodand the isodar method could be alternative tools forinvestigating the impacts of exotics on native species,in addition to precise experimental manipulations.However, limitations were found for both methods.The traditional regression method may not identifyinterspecificnteractionswhen exotics are scarcebecauseniche shiftsbynativespecies might mitigate any negativeimpacts.Theisodarmethodmaynot identify nterspecificinteractions when exotics affect native species duringthe pre-recruitmentphase rather than competition forfeeding habitats, e.g. by predation on juveniles ordisturbance of breedinghabits. In addition, the isodarmethodcannot addressdistributionof thespecies nonlyone type of habitat (see the Statistical analyses). Wesuggest that, until the methods are furtherdeveloped,both are used to evaluate interspecificinteractions.

AcknowledgementsWe would like to thank J. B. Dunham, K. D. Fausch,D. W Morris andG. P Closs fortheirthoughtfulreview,H. Kishino,K. Shirakihara,T.Katsukawa,A. Moriyamaand H. Hakoyama for their helpful suggestions on thestatistical analyses, and A. Goto, Y. Kanzawa andD. Aoyama forproviding nvaluable nformationon theHekirichi River. This work was supported by a grant-in-aid for a Research Fellow of the Japan Society forthe Promotion of Science (No. 14-07512)to K. Moritafrom the Japanese Ministry of Education, Culture,Sports, Science and Technology.

ReferencesAdams,S.B.,Frissell,C.A.&Rieman,B.E. 2001)Geographyof invasionnmountain treams:onsequencesf headwaterlake fish introductions. Ecosystems,4, 296-307.Aoyama, D. (2002) Life historycharacteristicsof brown rout

artificially introduced nto the Hekirichi River of southernHokkaido.Graduate hesis. aculty f Fisheries, okkaidoUniversity,Hokkaido, Japan [in Japanese].Aoyama,T.,Takami, .,Fujiwara,M.&Kawamura, .(1999)Natural reproduction f rainbowtrout, Oncorhynchusmykiss, in the Shiribetsu River in Hokkaido, Japan.Scien-tific Reports of the Hokkaido Fish Hatchery, 53, 29-38 [inJapanesewith English summary].Bain,M.B., Finn,J.T.&Booke, H.E. (1985)Quantifying treamsubstratefor habitatanalysisstudies. North AmericanJour-nal of Fisheries Management,5, 499-506.Bisson, PA., Sullivan,K. &Nielsen,J.L. 1988)Channelhydrau-lics,habitatuse,andbodyform of juvenile oho salmon,steelhead, and cutthroat trout in streams. Transactionsofthe American FisheriesSociety, 117, 262-273.Closs, G.P. &Lake, P.S. 1996)Drought, differentialmortalityand the coexistence of a native and an introduced fishspecies in a south east Australian intermittent stream.EnvironmentalBiology of Fishes,47, 17-26.

Crowell,K.L. &Pimm,S.L.(1976)Competition ndnicheshiftsof mice introducedonto small islands. Oikos, 27, 251-258.Crowl, T.A., Townsend,C.R. & McIntosh, A.R. (1992) The

impact of introduced brown and rainbow trout on nativefish: the case of Australasia. Reviews in Fish Biology andFisheries, 2, 217-241.Cunjak,R.A. & Green,J.M.(1983)Habitatutilizationbybrookcharr(Salvelinusfontinalis) nd rainbow trout(Salmogairdneri) n Newfoundland streams. Canadian JournalofZoology, 61, 1214-1219.

Dunham, J.B.,Adams, S.B.,Schroeter,R.E. &Novinger,D.C.(2002) Alien invasions in aquatic ecosystems: toward anunderstanding of brook trout invasions and potentialimpactson inland cutthroat rout nwesternNorth America.ReviewsinFish Biology andFisheries, 12, 373-391.Fausch, K.D., Nakano, S. & Ishigaki, K. (1994) Distributionof two congeneric charrs in streams of Hokkaido Island,Japan:considering multiplefactors across scales. Oecologia,100, 1-12.

Fox, B.J. & Luo, J.(1996) Estimating competition coefficientsfromcensusdata:a re-examination f theregression echnique.Oikos, 77, 291-300.Fretwell, S.D. & Lucas, H.J. (1970) On territorial behaviorand other factors influencinghabitatdistributionin birds.Acta Biotheoretica, 19, 16-36.Fuller,PL.,Nico,L.G.&Williams,.D. 1999)NonindigenousFishes Introduced nto Inland Watersof the United States.

Special Publication No. 27. American Fisheries Society,Bethesda, MD.Gatz, A.J. Jr, Sale, M.J. & Loar, J.M. (1987) Habitat shiftsin rainbow trout: competitive influence of brown trout.

Oecologia, 74, 7-19.Glova, G.J. (1986) Interaction for food and space betweenexperimental populations of juvenile coho salmon (Onco-rhynchuskisutch)and coastal cutthroat trout(Salmo clarki)in a laboratory stream.Hydrobiologia, 132, 155-168.Goto, A., Nakanishi, T., Utoh, H. & Hamada, K. (1978) Apreliminary study of the freshwater fish fauna of riversinsouthern Hokkaido. Bulletin of the Faculty of Fisheries,Hokkaido University,29, 118-130 [inJapanesewithEnglishsummary].Hartman, G.F. (1965)The role of behavior in the ecology andinteraction of underyearling coho salmon (Oncorhynchuskisutch)and steelhead trout (Salmo gairdneri).JournaloftheFisheries ResearchBoardof Canada, 22, 1035-108 1.Hawkins, C.P., Kershner, J.L., Bisson, P.A., Bryant, M.D.,Decker, L.M., Gregory, S.V., McCullough, D.A.,Overton,C.K., Reeves,G.H., Steedman,R.J.&Young,M.K.(1993)A hierarchicalapproachto classifyingstreamhabitatfeatures.Fisheries, 18, 3-12.

Inoue, M., Nakano, S. &Nakamura, F.(1997) Juvenile masusalmon (Oncorhynchus masou) abundance and streamhabitat relationshipsin northern Japan. CanadianJournalof FisheriesandAquaticSciences, 54, 1331-1341.

Kanzawa, Y. (2002) Feeding habits of brown trout and itsimpacts on nativefishes in the Hekirichi River. GraduateThesis.Facultyof Fisheries,Hokkaido University,Hokkaido,Japan[in Japanese].

Kawaguchi, Y, Taniguchi,Y &Nakano, S. (2003) Terrestrialinvertebrate nputsdeterminethe localabundanceof streamfishes in a forested stream. Ecology, 84, 701-708.Kitano, S., Nakano, S., Inoue, M., Shimoda, K. &Yamamoto, S. (1993) Feeding and reproductiveecology ofexotic rainbow trout Oncorhynchusmykiss in the HoronaiStream n Hokkaido,northernJapan.NipponSuisanGakkai-shi, 59, 1837-1843 [in Japanesewith English summary].

Krueger,C.C.&May, B. (1991) Ecological and genetic effectsof salmonid introductions in North America. CanadianJournalof FisheriesandAquaticSciences,48 (Supplement1),66-77.

? 2004BritishEcologicalSociety,Journalof AppliedEcology, 41,962 -972


11/12

971Impactsof exotictrout on nativecharr

Kudo, S. (2001) Researches on the impact of exotic fishes inHokkaido. SodateruGyogyo, 336, 3-7 [in Japanese].Lever, C. (1996) Naturalized Fishes of the World.Academic

Press, San Diego, CA.Lowe, S.M., Browne, S., Boudjelas, M. & Poorter, M.D.

(2001) 100 of the World'sWorstInvasiveAlien Species: ASelectionfrom theGloballInvasivepeciesDatabase. IUCN-ISSG, Auckland, New Zealand.

McArdle, B.H. (1988) The structuralrelationship: regressionin biology. CanadianJournalof Zoology, 66, 2329-2339.Manly, B.F.J. (1997) Randomization, Bootstrap and Monte

Carlo Methods in Biology, 2nd edn. Chapman & Hall,London, UK.Mayama, H. (1999) Predation of juvenile masu salmon

(Oncorhynchusmasou) and brown trout (Salmo trutta) onnewly emerged masu salmon fry in the Chitose River.Bulletin of theNational Salmon Resource Centre,2, 21-27[in Japanesewith English summary].

Montgomery, D.C., Peck, E.A. & Vining, G.G. (2001) Intro-duction to Linear Regression Analysis, 3rd edn. WileyInterscience,New York,NY.

Morita, K. & Morita, S.H. (2002) Rule of age and size atmaturity:individualvariationin the maturation history ofresident white-spotted charr. Journalof Fish Biology, 61,1230-1238.

Morita, K. & Suzuki, T. (1999) Shifts of food habit and jawposition of white-spotted charr after damming. JournalofFish Biology, 55, 1156-1162.

Morris, D.W (1988) Habitat-dependentpopulationregulationand community structure. Evolutionary Ecology, 2, 253-269.Morris, D.W.(1989) Habitat-dependentestimates of compet-itive interaction. Oikos, 55, 111-120.Morris, D.W. (1990) Temporal variation, habitat selectionand community structure.Oikos, 59, 303-312.Morris, D.W (1994) Habitatmatching rules:alternatives and

implications to populationsand communities. EvolutionaryEcology, 8, 387-406.

Morris, D.W (1999) Has the ghost of competition passed?EvolutionaryEcology Research, 1, 3-20.Morris, D.W (2003)Towardanecological synthesis:acase forhabitat selection. Oecologia, 136, 1-13.Morris, D.W, Davidson,D.L. &Krebs, C.J.(2000)Measuringthe ghost of competition: insights from density-dependenthabitat selection on the co-existence and dynamics of lem-mings. EvolutionaryEcology Research, 2, 41-67.

Morris, D.W, Fox, B.J.,Luo, J.&Monamy, V.(2000)Habitat-dependent competition and coexistence of Australianheathlandrodents. Oikos, 91, 294-306.

Mullner,S.A., Hubert,WA. &Wesche,T.A. (1998) Snorkelingas an alternative to depletion electrofishing for estimatingabundance and length-class frequencies of trout in smallstreams. NorthAmericanJournalof FisheriesManagement,18, 947-953.

Nakano, S. & Furukawa-Tanaka,T. (1994) Intra- and inter-specific dominance hierarchies and variation in foragingtactics of two speciesof stream-dwellingcharrs.EcologicalResearch,9, 9-20.

Nakano, S., Kawaguchi, Y., Taniguchi, Y., Miyasaka, H.,Shibata,Y.,Urabe,H. &Kuhara,N. (1999)Selective oragingon terrestrial invertebratesby rainbow trout in a forestedheadwater stream in northern Japan. Ecological Research,14, 351-360.

Ormerod, S.J. (2003) Current issues with fish and fisheries:editor's overviewand introduction. Journalof AppliedEco-logy, 40, 204-213.Ovadia, O.&Abramsky,Z. (1995) Density-dependent habitatselection: evaluation of the isodar method. Oikos, 73, 86-94.

Peterson, D.P. &Fausch,K.D. (2003) Upstreammovement bynonnative brook trout (Salvelinusfontinalis)promotes inva-

sion of native cutthroattrout(Oncorhynchuslarki)habitat.Canadian Journal of Fisheries and Aquatic Sciences, 60,1502-1516.Pfister, C.A. (1995) Estimatingcompetition coefficients fromcensus data: a test with field manipulations of tidepoolfishes. AmericanNaturalist, 146, 271-291.Rodriguez, M.A. (1995) Habitat-specific estimates of com-

petition in streamsalmonids:a fieldtest of the isodar modelof habitat selection. EvolutionaryEcology, 9, 169-184.Rosenfeld, J.S. & Boss, S. (2001) Fitness consequences ofhabitat use forjuvenile cutthroat trout:energeticcosts andbenefits in pools and riffles. CanadianJournalof Fisheriesand AquaticSciences, 58, 585-593.

Rosenzweig,M.L., Abramsky,Z. &Brand,S. (1984) Estimatingspeciesinteractions in heterogeneous environments.Oikos,43, 329-340.

Rosenzweig, M.L., Abramsky, Z., Kotler, B. & Mitchell, W.(1985) Can interaction coefficients be determined fromcensus data? Oecologia, 66, 194-198.

Sagawa, S., Yamashita, S. & Nakamura, E (2002) Summerhabitat use of adult Sakhalin taimen in a tributaryof theTeshio River, Hokkaido, Japan:management implicationsfor habitatconservation. JapaneseJournalof Ecology, 52,167-176 [in Japanesewith English summary].Shenbrot,G. &Krasnov, B. (2002)Can interactioncoefficientsbe determined from census data? Testing two estimationmethods with Negev Desert rodents. Oikos, 99, 47-58.Takami, T.&Aoyama, T.(1999)Distributionof rainbow routand brown trout in Hokkaido, northern Japan. WildlifeConservation Japan, 4, 41-48 [in Japanese with Englishsummary].Takami,T., Yoshihara,T.,Aoyama, T.&Kuwabara,R. (2002b)Distribution and feedinghabitsof white-spottedcharr andbrown trout in a branch of the Chitose River. Uo to Mizu,38, 23-32 [in Japanese].

Takami, T., Yoshihara, T., Miyakoshi, Y. & Kuwabara, R.(2002a) Replacementof white-spottedcharr Salvelinus eu-comaenis by brown trout Salmo trutta in a branch of theChitose River, Hokkaido. Nippon Suisan Gakkaishi,68,24-28 [in Japanesewith English summary].

Tanida, K., Yamashita, K. & Rossiter, A. (1985) A portablecurrent meter for fielduse. JapaneseJournalof Limnology,46, 219-221.

Taniguchi, Y. & Nakano, S. (2000) Condition-specificcom-petition: implications for the altitudinal distribution ofstream fishes. Ecology, 81, 2027-2039.

Taniguchi, Y., Fausch, K.D. & Nakano, S. (2002) Size-structured interactions between native and introducedspecies: can intraguild predation facilitate invasion bystream salmonids?Biological Invasions,4, 223-233.

Taniguchi,Y., Miyake, Y, Saito, T., Urabe, H. & Nakano, S.(2000) Redd superimpositionby introduced rainbowtrout,Oncorhynchusmykiss,on native charrs n a Japanesestream.IchthyologicalResearch,47, 149-156.

Taniguchi, Y., Rahel, EJ., Novinger, D.C. & Gerow, K.G.(1998) Temperaturemediation of competitive interactionsamong three fish species that replace each other along lon-gitudinal stream gradients. CanadianJournalof FisheriesandAquaticSciences, 55, 1894-1901.

Thurow,R.E (1994) UnderwaterMethodsfor Studyof Salmo-nids in the IntermountainWest.General Technical ReportINT-GTR-307. US Department of Agriculture, ForestService, IntermountainResearch Station, Ogden, UT.Thurow, R.E & Schill, D.J. (1996) Comparison of day snor-

keling, night snorkeling,and electrofishing to estimate bulltrout abundanceand size structure n a second-order Idahostream.North American Journalof Fisheries Management,16, 314-323.

Townsend,C.R. (1996)Invasionbiologyandecological mpactsof brown trout Salmo trutta in New Zealand. BiologicalConservation,78, 13-22.

C 2004 BritishEcological Society,Journalof AppliedEcology, 41,962-972


12/12

972K. Morita,J.-I. Tsuboi &H. Matsuda

Townsend,C.R. &Crowl,T.A.(1991)Fragmentedpopulationstructuren anativeNew Zealand fish:an effectof introducedbrown trout? Oikos, 61, 347-354.

Wakabayashi,T., Nakamura, T., Kubota, H. &Maruyama,T.(2002) Comparisonof spawning ecology of three salmonidsin the inlet streams of Lake Chuzenji,central Japan. Japa-nese Journalof Ichthyology,49, 133-141 [in JapanesewithEnglish summary].

Williamson, M. (1996)BiologicallInvasions.Chapman&Hall,London.Young, K.A. (2001) Habitat diversityand species diversity:

testingthe competition hypothesiswithjuvenile salmonids.Oikos, 95, 87-93.Received 10 November 2003; final copy received 12 April2004

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