*Author ([email protected]) for correspondence Oristano, Italy. Istituto perl’AmbienteMarinoCostiero, LocalitàSaMardini, Torregrande, 09072 Universidade Federal deSãoCarlos, SãoPaulo, 13565-905,Brasil. deCiênciasFisiológicas, Zoofisiologia eBioquímicaComparativa, Departamento Building, University of Glasgow,Building, GlasgowG128QQ, University of UK. © 2014.PublishedbyTheCompanyofBiologistsLtd|JournalExperimentalBiology(2014)217,4115-4118 doi:10.1242/jeb. Received 16July 2014; Accepted16October2014 2 1 organs, thusbrainsensitivity tohypoxiaislikelybehigh.Indeed, and schooling(Domenicietal.,2007;Richards2009). impaired performanceinreproductiveoutput,growth,swimming been intensivelystudied,showingnumerousinterferencessuch as Richards etal.,2009).Theeffects ofhypoxiaonfishbiologyhave agriculture anddischarge ofraw sewage(DiazandRosenberg, 2008; hypoxic eventsisexacerbatedbyhumanactivities,suchas because oftidalrhythms.Moreover, thenaturaloccurrenceof environments, fishareexposedtohypoxiaeventsdaily, mainly , behaviourandecology. Inmarineintertidal Oxygen availabilityisoneofthemainfactorsaffecting sculpin KEY WORDS:,Lateralization,Detourtest,Staghorn schooling. affect awiderrangeofbehaviours,suchassocialinteractionsand species, inwhichahypoxia-drivendisruptionoflateralizationcould Moreover, ourworkraisestheneedtostudythiseffect inother far-reaching implicationsforspeciesecologyandtrophicinteractions. expressed bystaghornsculpinsunderhypoxicconditionsmayhave from predatoryattacks.Thereforethealterationoflateralization predator–prey interactionsbyenhancingattacksuccessorsurvival population islikelytohaveanadaptivevalue,forexamplein specific turningpreferenceobservedinthestaghornsculpincontrol left afterexposuretohypoxiafor2 (>90% oxygensaturation),butanequalprobabilityofturningrightor showed adistinctpreferenceforrightturnsundernormoxicconditions lateralization atthepopulationlevel.Onaverage,staghornsculpins intertidal zone,wefoundthathypoxiaaffects behavioural ( role inseverallifehistoryaspectsoffish.Usingstaghornsculpin related tobrainfunctionalasymmetry, whichisthoughttoplayakey on lateralization(e.g.thetendencytoturnleftorright),abehaviour effects onecologicalinteractions.We assessedtheeffects ofhypoxia is oneofthemainfactorsaffecting fishbehaviour, causingbroad In intertidalenvironments,therecurringhypoxicconditionatlowtide Tyrone Lucon-Xiccato Severe hypoxiaimpairslateralizationinamarineteleostfish SHORT COMMUNICATION Paolo Domenici James CookUniversity, Townsville, QLD4811,Australia. MarineandTropical Studies, School Biology, of Excellence for CoralReef of Section, University of Copenhagen, Helsingør DK-3000, Denmark. Copenhagen,HelsingørDK-3000,Denmark. Section, University of INTRODUCTION ABSTRACT Institute of Biodiversity,Institute of AnimalHealthandComparative Medicine, GrahamKerr diPsicologiaGenerale, Università diPadova,Dipartimento Padova 35131,Italy. Leptocottus armatus),abenthicfishthattypicallyinhabitsthe The brainoxygenrequirementsareamongthehighestofall the 6 1, *, JulieJ.H.Nati

h (20%oxygensaturation).The 5 3 Marine Biological Laboratório de 2 , FelipeRoccoBlasco 6 4 CNR-IAMC, ARC Centre lateralization. We thencomparedthe population- andindividual- preference test(detourtest) toevaluatetheirbehavioural 2013), respectively, andweobservedthesubjectsinaturning (20% oxygensaturation)(Palsson etal.,2008;Speers-Roesch lethal levelsofhypoxiathatnaturally occurinthesamplingarea staghorn sculpinstonormoxia (>90% oxygensaturation)andnon- and tidepools(Palssonetal., 2008). We exposed two groupsof availability (<20%oxygensaturation)duringstrandinginmudflats intertidal environmentandmaythereforeexperiencelowoxygen armatus behavioural lateralizationinthestaghornsculpin( interactions (Yasugi andHori,2012). in non-gregariousspecies,itcouldbeinvolvedprey–predator greater coordinationinmovements(Bisazzaetal.,2000),whereas 2011). This biasappearstoberelevantinsocialspeciesachieve population islateralizedinthesamedirection(BisazzaandBrown, population level:aconspicuousproportionofindividuals ina bias foraspecificdirectionalityoflateralizationisobserved at the travelled inescaperesponses(Daddaetal.,2010).Insomecases,a have afasterreactiontime,higherturningratesandlongerdistance enhanced abilitytoescapefromapredator:stronglylateralizedfish Bisazza, 2006).Moreover, lateralizationisalsoassociatedwithan foraging andpredatorvigilance(Sovranoetal.,2005;Dadda spatial reorientationtasksorinsimultaneousactivities,suchas individual-level lateralization)outperformnon-lateralizedonesin example, highlylateralizedindividualfish(i.e.thosewithgreater information, resultingingreatercognitiveperformance.For hemisphere candevelophigherspecializationinprocessingspecific A lateralizedbrainallowsaseparation oftaskachievements:each of majorityevidencesuggeststhatitconfersseveraladvantages. cost ininformationprocessing(BisazzaandBrown,2011), thevast in somecaseshemisphericspecializationcouldrepresentanadded al., 2000;Daddaet2010;BisazzaandBrown,2011). Although social andsexualinteractions(e.g.Bisazzaetal.,1997; ecological settingssuchasfeeding,predatorescape,schooling, pressures andtobeimportantforthesurvivalofindividualsinmany patterns observedinapopulationarethoughttoreflectselective evolutionary processesinvolvedarestillnotclear, thelateralization (Bisazza andBrown,2011). Infish,eventhoughtheexact specialization ofthetwohemispheresinprocessinginformation expression ofbrainfunctionalasymmetrythatreflectsadifferential conditions infish,wefocusedonbehaviourallateralization,an such effects couldbeofgreatecologicalrelevance. fish remainsrelativelyunexplored,althougharguably, knowledgeof impact ofhypoxiaonbehavioursdirectlyrelatedtobrainfunctionin intra-specific level(ChapmanandHulen,2001).Bycontrast,the reduced brainsizeinchronichypoxichabitatsatboththeinter- and characterized byahugebrainoxygenuptake,areknowntoshow (e.g. Nilsson,1990;Nilssonetal.,1993).Furthermore,mormyridfish, near-lethal hypoxicconditionsareknowntoaffect brainphysiology In thisexperiment,weassessedtheeffect ofhypoxiaon In ordertoassessalterationsofbrainfunctioninginhypoxic 3 , JacobL.Johansen Girard 1854),abenthicfishthattypicallyinhabitsthe 4 , JohnF. Steffensen 111229 Leptocottus 5 4115 and

The Journal of Experimental Biology F * bars). N level lateralizationbias. reduction oftheindividual-levellateralizationand/orpopulation- al., 2012),wehypothesizedthatexposuretohypoxiamayinducea effects ofenvironmentalstressorsonlateralization(e.g.Nilssonet 1997; Daddaetal.,2010).Basedonpreviousworkthattestedthe strength oflateralizationirrespectivedirection(Bisazzaetal., at thepopulationlevel(mean contrast, thegroupexposedtohypoxiashowednolateralizationbias mean a left-turningbias(Bisazzaetal.,1997;Dadda2010).The 4116 armatus Fig. effect onlateralizationpattern( groups (seetheMaterialsandmethods).Groupinghadnosignificant Individuals weresubjectedtohypoxiaandcontrolwaterinsmall indicate aright-turningbias,whereasnegativevaluesof laterality index( level lateralizationofthetwoexperimentalgroupsusingrelative SHORT COMMUNICATION was significantlygreaterthanzero( population-level lateralization( specific directionatthepopulation-level:positivevaluesof groups exposedtonormoxiaandhypoxia( P fitness ofindividualsinthewild. functions, andcouldhavedirectimplicationsfortheecology changes inbrainhemispherefunctioningorneurotransmitter towards therightunderhypoxicconditionsislikelytobecausedby expression ofbrainasymmetry, thelossofturningpreference level lateralization(Fig. laterality index( control group(hypoxia:37.14±4.12;control:41.43±4.17; hypoxia-treated groupwasnotsignificantlydifferent fromthe under normoxicconditions;the preference forrightturnswhenfacingthebarrierindetourtest lateralization atthepopulationlevel,revealedbyadistinct 1).Onaverage,controlsubjectsexhibitedaright-biased (Fig. RESULTS ANDDISCUSSION individuals withleft-turningbias(Fig. preference towardstherightandanincreaseinfrequencyof P respectively. Themean P =0.384) showingtherewasnoeffect ofhypoxiaontheindividual- 10,73 =0.085). Thisindicatesareductionoftheaverageturning <0.05; n.s.,notsignificant.

1. Population-levellateralizationof staghornsculpin( =0.725, L =42 forcontroland A ) islostunderhypoxia. refers toindividual-levellateralizationanddescribesthe Laterality index (mean ± s.e.) L P A 10 20 30 40 50 =0.698). Therewasasignificantdifference inthe ) offishexposedtonormoxia(black bars)orhypoxia(grey 0 L R ) andtheabsolutelateralityindex( L

N 1). Becausebehaviourallateralizationisan R =42 forhypoxia.Results aremeans±s.e. L allows ustoassesstheturningbiasfora * R Relative lateralityindex( L L R L R L R index (31.91±5.87,mean±s.e.) R t index: 12.38±6.85; 41 : index) ofstaghornsculpins =5.413, F 10,73

2). TheL =1.278, t n.s. P 82 L 001 Fg 2).In <0.001) (Fig. A =2.259, L A R ) andabsolute P Leptocottus index ofthe =0.259; L t t R P 41 82 =0.027) indicate =1.767, =0.876, L L A L A ), R : lateralization ofcoralreeffishlarvaemaintainedinhigh CO whereas othersshow brainprotectionagainsthypoxia asanincrease resulting inabreakdownofbrain functioning(Nilssonetal.,1993), brain: mostfishspeciesrapidly loseionhomeostasisintheirbrain hypoxia exposuretriggersseveral physiologicalchangesinthefish neuronal transmitterfunctions (Nilssonetal.,2012).Extreme thought tobemediatedbychanges inbrainphysiologythatalter concentration isimpaired(Domenici etal.,2012)andtheeffect is Fig. to normallevelsofoyxgen(blackbars)orhypoxia(greybars). previously beenreportedforCO within thebrainfollowinghypoxiaexposure.Suchchanges have caused byaphysiologicalchangeinneuraltransmitterfunctions hypoxia. lateralization aremoreintenseinindividualswithlowtolerance to relevant todeterminewhethertheeffects ofhypoxiaonbehavioural sensitivity tohypoxia(Killenetal.,2012).Therefore,itmay be hypoxic conditions,probablybecauseofindividualvariation in juvenile seabassdifferentially altertherisk-takingbehaviourin situation hasbeenreported.Forexample,different individualsof bias. Infish,alarge within-speciesvariationincopingwithastress al., 1997),resultinginalossoftheoriginalpopulationright-turning hemisphere wouldimplymorefrequentturnstotheleft(Bisazzaet Using ourdetourtest,anincreaseinthecontrolbyright hypoxia causedtreatedsubjectstoincreaseright-hemispherecontrol. with Rogers(Rogers,2010),itispossiblethatthestressdueto left torightcontrol)(Rogers,2010;Domenicietal.,2014).Inline of informationprocessingbetweenthetwohemispheres(i.e.from theoretical worksuggeststhatstressfulsituationscouldcauseashift controls emergency responses(Rogers,2010).Someevidenceand behaviours innon-stressfulsituations,whereastherighthemisphere lateralization. Inseveralspecies,thelefthemispherecontrols could explaintheeffect ofhypoxiaexposureonpopulation-level Relative frequencydistributionofrelativelateralityindex( control and The effect onthepopulation-level lateralizationmayalsobe A shiftininformationprocessing betweenbrainhemispheres

.Responseofstaghornsculpin(Leptocottusarmatus 2. Relative frequency (%) 10 15 20 25 10 15 20 25 30 0 5 0 5 N =42 forhypoxia. The JournalofExperimentalBiology(2014)doi:10.1242/jeb.111229 –100

–80

–60 Relative lateralityindex(

–40

–20

0

2 20 exposure: behavioural

40 L R

60 80 ) L R ) infishexposed N ) tohypoxia. =42 for

100 2

The Journal of Experimental Biology an effect ofexposuretoelevatedCO (Domenici etal.,2014).Incontrast, studiesonotherspeciesreported affected population-levelbutnotindividual-levellateralization incongruence of theresults.Onepossibility is thatthedifferent current stageofresearch,it is notclearwhatdeterminesthis population-level lateralization (e.g.Nilssonetal.,2012).Atthe SHORT COMMUNICATION found inacoralreeffish,where exposuretoelevatedCO individual-level lateralizationasinnormoxia.A similareffect was side biasinthewholepopulationwhilemaintainingasimilar lateralized (seepeakatLR= hypoxia mightcauseright-lateralizedindividualstobecome left- results insomeindividualsbeingleft-biased.Hence,exposure to non-lateralized orright-lateralized,whereashypoxiaexposure individual level.Innormoxia,sculpinsaremainly either has aneffect onlateralization atthepopulationlevelbutnot (Fig. by hypoxiaexposure.Inspectionofthefrequencydistribution plots effect ofhypoxiaonlateralization ingregariousspecies. their schoolingactivity. Therefore,itmaybeworthwhiletotestthe including thoseinvolvedinsocialbehaviours,possiblyaffecting level lateralizationmaysubsistinotherfishspeciesaswell, do notschool.However, similareffects ofhypoxiaonpopulation- (Bisazza andBrown,2011). Staghornsculpinsaresolitaryandthus lateralization givesadvantagesforcoordinationduringschooling in predationsuccessorsurvivalfrompredatorattacks. staghorn sculpinscouldsuffer theseverefitnesscostsofadecrease right-biased toleft-biased.Therefore,inhypoxicconditions, individuals exposedtohypoxiashifttheirturningpreferencefrom subjects inpopulation-levellateralizationsuggeststhatsomeofthe Rogers, 2005).Thedifference betweencontrolandhypoxia-treated alternatively tosurvivefrompredatoryattacks(Vallortigara and prey lateralizationpatternsinordertoenhanceattacksuccess,or turning preferenceinthedetourtest)maybeadaptedtomatchtheir population usedinthisstudy(i.e.mostoftheindividualshadaright a similarfashion,thelateralizationpatternofstaghornsculpin or left)ofthetwoindividualsinvolved(Yasugi andHori,2012).In lateralization (e.g.thepreferenceforapproachpreyfromright prey–predator interactionsisrelatedtothespecificdirectionalityof and attackingpreyshowlateralizedbehaviourstheoutcomeof environment. Forinstance,insomefishspecies,escapingpredator patterns arelikelytohaveanadaptivevalueintheirnatural study werewild-caughtfish,theirpopulation-levellateralization lateralization; however, becausetheindividualsobservedinour known regardingtheecologicalmeaningofpopulation-levelbiasin repercussions forthespeciesitself,aswellotherspecies.Littleis in hypoxia-treatedstaghornsculpinsmighthavecriticalecological consequence, thelossofpopulation-levelright-turningbiasobserved by humans(DiazandRosenberg, 2008;Richardsetal.,2009).Asa with anincreasingoccurrence/intensitybecauseofpollutioncaused even moresevere(<20%oxygensaturation)(Palssonetal.,2008), hypoxic conditionssimilartotheonerecreatedinourexperimentor variation ofthereportedeffect. one prospectivefieldofinvestigationisthebetween-species environments couldshowdifferent sensitivitiestohypoxicstress, exposed tohypoxia.Becausespeciesadapteddifferent population-level right-turningbiasobservedinstaghornsculpin physiological changesinthebraincouldexplainlossof functioning andlimitoxygenrequirements(Nilsson,1990).Similar or aredistributionofinhibitoryneurotransmittersthatsuppressbrain In ourexperiment,individual-levellateralizationwasnotaffected Additionally, ingregariousfishspecies,population-levelbias Fish communitiesinoursamplingareamaydailyexperience 2) offers apossibleinterpretation forthefindingthathypoxia − 60), resultinginthelossoforiginal 2 in individual-levelbutnot 2 levels external sump(40 of transparentsyntheticglass.Thetreatmenttankwasconnectedtoan respiration ofthesubjects,watersurfacewascoveredwithapanelmade temperature ontheoxygenconsumptionofsubjects.To avoidaerial treatment (11.48±0.06°C) inordertoavoidanyconfoundingeffect of Fig. implications oftheincreasingworldwideincidencehypoxiczones. understand theunderlyingphysiologicalprocessesandecological factors onawiderangeofspecieswouldbegreatvalueto investigations onthesynergistic effect ofdifferent environmental hypoxia toalterbehaviourallateralization.Therefore,broader (Domenici etal.,2014),hencetheycouldpotentiallyinteractwith known toaffect lateralization(temperatureandelevatedCO light conditionsandatatemperatureof11.64±0.52°C. tanks (130×60×26 Harbor Laboratories(UniversityofWashington) for24hours.Maintenance in August2013.Beforetheexperiments,fishweremaintainedatFriday Jackson beach(48°31′ tested onlyonce.Staghornsculpinsweresampledbybeachseiningatthe exposed tohypoxia,andforty-twowereusedascontrol.Eachsubjectwas (standard length123.54±2.91 permit number4208-3).Eighty-fourstaghornsculpinswereusedoverall Animal CareandUseCommitteeattheUniversityofWashington (IACUC care andexperimentalprotocolsfollowedtheguidelinesofInstitutional No physicalinvasivemanipulationwasperformedonthefish.Allanimal temperature, elevatedCO exposed tootherstressorsinadditionhypoxia,suchasincreased 2009). Moreover, incoastalareasveryoftenfisharesimultaneously sediment loadingandpollutionfromhumanactivities(Richardsetal., areas arespreadingworldwidebecauseofincreasedeutrophication, found acrossmostoftheworld’s aquaticecosystems,andhypoxic suggest broadimplicationsforwildpopulations,becausehypoxiais in theeffect sizeslimitthestatisticalinference. both individual-andpopulation-levellateralization,butdifferences possibility thattheenvironmentalstressorssimultaneouslyaffect level ineachspecies.However, oneshouldalsoconsiderthe stressors affect lateralizationonlyattheindividualorpopulation (Bisazzaet al.,2000).Theapparatusconsisted ofatank(120×50 al., 1997),aprocedurepreviouslyadopted tostudylateralizationinbenthic were testedfortheirbehaviourallateralization usingadetourtest(Bisazzaet Immediately aftertheendoftreatment (normoxiaorhypoxia),subjects and keptoxygensaturationconstantfor120 (>90% oxygensaturation)to20%saturationovera20 group, wedecreasedoxygensaturationinthetreatmenttankfromnormoxia saturation inthesump,andindirectlytreatmenttank.Forhypoxia nitrogen flowthroughtheairstones,allowingregulationofoxygen 5714, PRElectronics,Roende,Denmark)andasolenoidvalvecontrolled International, Birkeroed,Denmark)connectedtoanoxygenregulator (PR the sump.A galvanicoxygenprobe(OxyguardHandy, Oxyguard to anairpumpandfourconnectedanitrogentankproviding to bottom ofthesump,fivestandardairstoneswereinstalled,oneconnected which allowedconstantrecirculationofthewaterintosystem. In the tank (45×50 Subjects weretransferredinsmallgroups(7–8individuals)toatreatment was injectedinthesumpviaair stones. (98.34±1.02% oxygensaturation) for140 saturation). Forthecontrolgroup,oxygensaturationwaskeptatnormoxia Experimental subjects MATERIALS ANDMETHODS Lateralization assessment Experimental treatment Our resultsshowthathypoxiacandisruptlateralizationinfishand S1). Water temperaturewasmaintainednearconstantduringthe cm) filledwith25 The JournalofExperimentalBiology(2014)doi:10.1242/jeb.111229 cm indiameter, 60 cm) werekeptataconstantseawaterflow, undernatural 11 ″ N, 123°00′ 2 or ammonia.Someofthesestressorsare

mm, mean±s.e.).Forty-twosubjectswere

cm ofseawater(supplementarymaterial 40″

cm high)filledwith50 W) onSanJuanIsland(WA, USA)

min andairinsteadofnitrogen

min (20.29±0.74%oxygen

cm ofseawater

min period 4117

cm, 2 )

The Journal of Experimental Biology the barrierwasrecorded. ends oftherunway(Domenicietal.,2014).Thedirectionturnsinfront procedure wasrepeatedtentimesalternatingbetweenthetwosymmetrical order toencourageitswimtowardthebarrier. Foreachsubjectthe small fishnets,thesubjectwasgentlyconducteduptohalfofrunway, in become accustomedtotheenvironment.Subsequently, byusingapairof random wasintroducedintotheexperimentalarenaandleftfor1 orientation oftherunway. Atthestartofeachtrial,asinglefishchosenat white opaquebarrier(20×20 the negative root transformationbeforeanalysis(SokalandRohlf,1995).To dealwith L sample using aone-samplet respectively. − left)/(turns totheright+turnsleft)]*100,withvaluesrangingfrom A mean L 4118 from FridayHarborLaboratories. T.L.-X., J.J.H.N.andF.R.B werepartiallysupportedbyaStudentFinancialAid P.D. wrotethepaper. J.J.H.N. andF.R.B. analysedthedata;T.L.-X., J.J.H.N.,F.R.B., J.L.J.,J.F.S. and experiments; T.L.-X., J.J.H.N.andF.R.B. performedtheexperiments.T.L.-X., T.L.-X., J.J.H.N.,F.R.B., J.L.J.,J.F.S. andP.D. conceived anddesignedthe The authorsdeclarenocompetingfinancialinterests. and AngeloBisazzaforcommentsontheearlierversionofmanuscript. support, the2013FishSwimmingclassforfishcollectionandhelpfuldiscussions The authorswouldliketothankstheFridayHarborLaboratoriesstaff forlogistical Because water depth15 SHORT COMMUNICATION material Fig. statistical software(version3.0.2,RFoundationforStatisticalComputing). group andhypoxia-treatedgroup.AllanalyseswerecarriedoutusingR Therefore, themean neither left-norright-biasedinitsturningtendency(Bisazzaetal.,1997). formula: had asignificanteffect onthe small groups,weconductedapreliminaryanalysistotestwhetherthegroup literature. Becausethesubjectswereexposedtohypoxiaorcontrolwaterin the maintext,untransformeddataarereportedforconsistencywithprevious and subsequentlyweaddedthecorrespondingsigntoeachobservation.In Funding Author contributions Competing interests Acknowledgements Statistical analysis R 100 to+100,indicatingcompletepreferenceforleftandrightturning, For eachsubject,wecomputedthe was computedusingtheformula: t -test tocomparemeansof L L R R A =|L and near zeroindicatesthatagivensampleofthepopulationis

S2). Atbothendsoftherunway(6 L L R R A

L | (Bisazzaetal.,1997). values, wetransformedtheabsolutevalueofthisvariable cm) withacentralrunaway(75×10 , rangingfrom0to100,wascomputedaccordingthe A indices arepercentagedata,weperformedarcsinesquare L -test (Bisazzaetal.,1997).We usedtheindependent R of eachgroupwascomparedwithatheoreticalzero L

cm) waspositionedperpendiculartothe R and L R L L L A and R R indices usingaone-wayANOVA. =[(turns totheright and theL L A indices betweenthecontrol

cm aheadoftherunway),a A (Bisazza etal.,1997).

cm) (supplementary − turns tothe

min to aui .adHr,M. Hori, and M. Yasugi, alriaa .adRgr,L.J. Rogers, and G. Vallortigara, pesRec,B,Mni,M,Gom .J n ihrs J.G. Richards, and D.J. Groom, M., Mandic, B., Speers-Roesch, J.(1995).Biometry:ThePrinciplesandPracticeof F. Rohlf, and R. Sokal, L.J. Rogers, J. Beam, and T. R. Parra, R.E., Pacunski, W. A., Palsson, ad,M n iaz,A. Bisazza, and M. Dadda, K.G. Hulen, and L.J. Chapman, orn,V . ad,M n iaz,A. Bisazza, and M. Dadda, V. A., Sovrano, C., Sørensen, M.I., McCormick, P., Domenici, D.L., Dixson, G.E., Nilsson, ihrs .G,Frel .P n rue,C.J. Brauner, and A.P. Farrell, J.G., Richards, iaz,A,Cnauo . aocin,M n alriaa G. Vallortigara, and M. Capocchiano, C., Cantalupo, A., Bisazza, ad,M,Koha,W .adDmnc,P. Domenici, and W. H. Koolhaas, M., Dadda, iso,G . ée-izn . ibr,K n ibr,S. Winberg, and K. Dimberg, M., Pérez-Pinzón, G.E., Nilsson, iso,G.E. D.J. Nilsson, McKenzie, and P. Domenici, M.R., Ryan, S., Marras, S.S., Killen, http://jeb.biologists.org/lookup/suppl/doi:10.1242/jeb.111229/-/DC1 Supplementary materialavailableonlineat iaz,A,Pgat,R n alriaa G. Vallortigara, and R. Pignatti, A., Bisazza, C. Brown, and A. Bisazza, iz .J n oebr,R. Rosenberg, and R.J. Diaz, References Supplementary material oeii . la,B,MCrik .I n udy P. L. Munday, and M.I. McCormick, B., Allan, P., Domenici, A. Shingles, and C. Lefrancois, P., Domenici, oeii . la,B . asn .A,MCrik .I n udy P. L. Munday, and M.I. McCormick, S.A., Watson, B.J., Allan, P., Domenici, on 589, discussion589-633. Biol. advantages anddisadvantagesofcerebrallateralization. during hypoxiaexposureinfishes. oxygen tensionsaspredictorsofhypoxiatoleranceandtissuemetabolicresponses 127. than nonlateralizedfishinspatialreorientationtasks. Statistics inBiologicalResearch welfare. Press. Vol. 27(ed.A.P. FarrellandC.J.Brauner),pp.528.SanDiego,CA:Academic SocietySymposiumSeries hypoxia onmarinefishpopulationsinsouthernHoodCanal,Washington. of simultaneoustasks? morphometryofmormyridfishes. 284. behaviour byinterferingwithneurotransmitterfunction. P. L. Munday, and S.A. Watson, Physiol. sensitivity toanoxiainfishasreflectedbychangesextracellularK+activity. chromaffin tissue,andliver . amino acidandmonoamineneurotransmittersinthebrain, interspecific variationinpoeciliidfish. lateralisation andsocialbehaviour:astudywith16speciesoffish. escape performanceinateleostfish. hypoxia injuvenileEuropeanseabass. relationship betweenmetabolicrateandrisk-takingbehaviourisrevealedduring e87969. temperature onbehaviourallateralizationinacoralreeffish. Cambridge: BlackwellPublishing. Cognition andBehaviour marine ecosystems. dioxide affects behaviourallateralizationinacoralreeffish. behaviours offishes. (2014). Shiftingfromrighttoleft:thecombinedeffect ofelevatedCO Rhinogobius gobies 215 Appl. Anim.Behav. Sci. 264 , 2390-2398. , R250-R253. The JournalofExperimentalBiology(2014)doi:10.1242/jeb.111229 (2010). Relevanceofbrainandbehaviourallateralizationtoanimal (1990). Long-termanoxiaincruciancarp:changesthelevelsof Science Philos. Trans. R.Soc.B (2012). Lateralizedbehaviorintheattacksoflargemouthbass Anim. Behav. corresponding totheirmorphologicalantisymmetry. (2006). Doesbrainasymmetryallowefficient performance (2011). Lateralizationofcognitivefunctionsinfish.In (ed. C.Brown,K.LalandandJ.Krause),pp.298-324. 321 (2008). Spreadingdeadzonesandconsequencesfor . NewYork, NY: W.H. FreemanandCompany. (2001). Implicationsofhypoxiaforthebrainsizeand 127 , 926-929. (2012). Near-futurecarbondioxidelevelsalterfish J. Exp.Mar. Biol.Ecol. , 1-11. J. Zool.(Lond.) 64, 255-280. (2005). Survivalwithanasymmetricalbrain: 72, 523-529. Biol. Lett. Anim. Behav. J. Exp.Biol. Funct. Ecol. (2005). Lateralizedfishperformbetter 362 (2010). Behaviouralasymmetryaffects (1997). Lateralityindetourbehaviour: (2007). Hypoxiaandtheantipredator 6 (2009). Hypoxia.In , 414-417. , 2105-2121. 150 54, 1273-1281. 26, 134-143. 254 Nat. Clim.Chang. , 295-320. Behav. BrainRes. , 461-472. 449 Behav. BrainSci. Biol. Lett. (2012). Elevatedcarbon , 239-249. (2008). Theeffects of (2000). Population Laterality PLoS ONE 8 (2013). Critical , 78-81. (1993). Brain 2 , 201-204. 163 American (2012). A 28, 575- J. Exp. 5 Am. J. 2 , 122- , 269- Fish and 9 , ,

The Journal of Experimental Biology