Chemical spying in coral reef fish larvae at recruitment

Ethology/E´thologie

Chemical

spying

in

coral

reef

fish

larvae

at

recruitment

Interception

de

l’information

chimique

lors

du

recrutement

larvaire

des

poissons

coralliens

?

Natacha

Roux

_,

_Rohan

_M.

_Brooker

_,

_Gae¨l

_Lecellier

_,

_Ce´cile

_Berthe

_,

Bruno

Fre´de´rich

,

Bernard

Banaigs

,

David

Lecchini

*

a

USR3278CNRS-EPHE-UPVD,CRIOBE,BP1013Papetoai,98729Moorea,FrenchPolynesia

b

SchoolofBiology,GeorgiaInstituteofTechnology,30318Atlanta,GA,USA

c

UniversityofVersailles–Saint-Quentin-en-Yvelines,75001Paris,France

d

Laboratoiredemorphologiefonctionnelleete´volutive,AppliedandFundamentalFishResearchCentre,Universite´ deLie`ge,4000Lie`ge, Belgium

e_{Laboratoired’excellence‘‘CORAIL’’,98729Moorea,FrenchPolynesia}

ARTICLE INFO Articlehistory:

Received19March2015

Acceptedafterrevision17May2015 Availableonline28August2015

Keywords:

Sensorymechanisms Communication Spying Chemicalcues Coralreeffishlarvae

Motscle´s:

Me´canismessensoriels Communication

Interceptiondel’information Stimulichimiques Larvesdepoissonscoralliens

ABSTRACT

Whenfishlarvaerecruitbacktoareef,chemicalcuesareoftenusedtofindsuitablehabitat ortofindjuvenileoradultconspecifics.Wetestedifthechemicalinformationusedby larvaewasintentionallyproducedbyjuvenileandadultconspecificsalreadyonthereef (communicationprocess)or whetherthe cues used resultfrom normal biochemical processeswithno active involvementby conspecifics(‘‘spying’’ behavior bylarvae). Conspecificchemicalcuesattractedthemajorityoflarvae(fouroutofthesevenspecies tested);althoughwhilesomespecieswereequallyattractedto cuesfromadultsand juveniles(Chromisviridis,Apogonnovemfasciatus),twoexhibitedgreatersensitivityto adultcues(Pomacentruspavo,Dascyllusaruanus).Ourresultsindicatealsothatspyingcues arethosemostcommonlyusedbysettlingfishes(C.viridis,P.pavo,A.novemfasciatus).Only onespecies(D.aruanus)preferredtheodourofconspecificsthathadhadvisualcontact withlarvae(communication).

ß2015Acade´miedessciences.PublishedbyElsevierMassonSAS.Allrightsreserved.

RE´ SUME´

Lespoissonscoralliensutilisentsouventlesstimulichimiqueslorsdurecrutementlarvaire pour trouver un habitat ou reconnaıˆtre les conspe´cifiques. Notre e´tude explore si l’information chimique perc¸ue par les larves est e´mise volontairement par les conspe´cifiques(processusdecommunication)ousilesstimulisonte´misinvolontairement etintercepte´sparleslarves(interceptiondel’information).Lesre´sultatsmontrentqueles larvessontchimiquementattire´esparlesconspe´cifiques(quatreespe`cessur lessept teste´es).Certainesespe`cessontplusre´ceptivesauxstimulie´misparlesconspe´cifiques adultes(Pomacentruspavo,Dascyllusaruanus),alorsqued’autressontattire´esa` lafoispar lesadultesetlesjuve´niles(Chromisviridis,Apogonnovemfasciatus).Enfin,troisespe`ces

* Correspondingauthor.

E-mailaddress:lecchini@univ-perp.fr(D.Lecchini).

ContentslistsavailableatScienceDirect

Comptes

Rendus

Biologies

w ww . sc i e nce d i re ct . co m

http://dx.doi.org/10.1016/j.crvi.2015.05.004

1. Introduction

Animals constantly make decisions: they choose mates, selectresources,anddecide whether toengage inactivitiesthatincreasepredationrisk.Thesedecisions areoftenbasedontheperceptionofchemicaloracoustic cues[1,2].WisendenandStacey[3]definedthreedistinct statesthatcharacterisetheevolutionofthesechemical andacousticsignals:ancestral,spying,and communica-tion. In the ancestral state, cues are released by an individual(thesender)butcannotbedetectedbyother individuals(i.e.noreceiver).Thespyingstateconsistsof theperception of a cue by a receiver with no specific response detected by the sender. For example, during matechoiceinfrogs[4],andfishes[5],satellitemalescan interceptacousticsignalsproducedbydominantmaleuse thesetotheirownadvantagetosuccessfullymatewith females. Similarly, bacteria in biofilms are known to releasesocalledquorum-sensingmolecules,whichare involvedinbacterialcell–cellcommunication.However, someseaweedsandmarineinvertebrates(e.g.,polychaete Hydroides elegans) can intercept these quorum-sensing moleculestodetectasuitablebiofilmforattachmentor settlement[6].Thecommunicationstatewasdefinedas cues that are actively used to transfer information between senders and receivers, and that are used by senders to manage the behaviour of receivers [2]. For example,socialinteractionsininsectsareprimarilythe result of chemical communication. For instance, dung beetlelarvaereleasechemicalsignalstoregulate mater-nalfoodprovisioning[7].Thoughlessunderstood,many vertebratesalsousechemicalstocommunicateandavoid aggressive conspecifics interactions [1]. For example, Tilapia fish use chemical cues to facilitate conspecific recognition,limitingunnecessaryconfrontations[8]. De-terminingwhetherthechemicalcuesthatanindividual producesareusedbyreceiversviaspyingor communica-tionisnecessarytounderstandtheimportanceofthese cuesinthedetectionoffood,predators,mates,orduring socialinteractions[1–3].Aquaticorganisms,suchasfish, oftenlive inenvironments wherevisualinformationis limitedbutwherechemicalinformationabounds. There-fore,fishes,giventheirlongevolutionaryhistory,havehad bothcauseandopportunitytodevelopsensitive chemo-sensorysystemsenabling individualsto respond adap-tivelytoconspecificandpredatorodours[3].Incoralreef fish,agoodsenseofsmellisalsoimportantfordetecting andorientating towardssuitable reef habitats prior to larvalrecruitment[9].However,despitetheimportance of chemical cues for many coral reef fishes, there is currently no information regarding the behavioural process underlyingchemical cue use, namely whether

theincorporationofcuesisa resultofeitherspyingor communication.

Most coral reef fishes have stage-structured life histories,withalargelysedentarybenthicstage(usually juvenilesandadults),precededbyapelagiclarvalstage duringwhichthereisoftenthecapacityforlong-distance dispersal [10]. At the conclusion of the pelagic phase, larvae must return and settle onto reef habitats to continuetheirdevelopmentintojuvenileandadultstages (i.e. recruitment). During recruitment, fish larvae are subjecttostrongselectivepressuretochoosehabitatsthat willpromotetheirsurvivalandgrowth[11].Manyspecies are highly selective between available habitats, basing thesechoicesontheavailabilityofspecificsubstrates,the presenceofjuvenileoradultconspecifics,andtherelative abundance of predators or direct competitors [12–14]. Several studies have highlighted the critical role that larval sensory mechanisms play in habitat selection, includingthedetectionofvisual,chemicalandauditory cues from conspecifics, habitats, or predators [9,15]. Chemicalcuesin particularmayplayanimportantrole inleadinglarvaebacktoareef[10,11].Chemicalcuesare usedbyfishlarvaetofindasuitablereefhabitat[16–20], tofindconspecificsatjuvenileoradultstage[17,21,22],or toavoidpredators[23].Unfortunately,noinformationis availableaboutthequestioninbehaviouralecology:the detectionofchemical cuesemittedbyconspecificsis it relatedtocommunicationorspyingincoralreeffish?Yet, determiningthenatureofchemicalcues,andthesocial recognition mechanisms used to integrate them into behavioural processes (spying or communication), will increase ourunderstandingof a widevariety oftopics, such as the evolution of social recognition, drivers of habitatselection,andcognitiveprocessinginlarvalfishes

[2,3,5].

Inthisstudy,weinvestigatedif(a)chemicalcuesare ‘‘passively’’receivedbylarvalfishes(‘‘spying’’)or if(b) thereisan‘‘active’’effortonthepartofthejuvenileor adult fishes tocommunicatethese cuesat recruitment (‘‘communication’’).Asitwasnotpossibletoanalyzeand identifythechemicalstructureofsignalsemittedintothe water, a series of three experiments were conducted using a two-chamberchoice flume. Theseexperiments testedwhether(1)larvalfishesareattractedtotheodour of conspecifics and if so, if they can (2) distinguish between‘‘communication’’and‘‘spying’’cues,and(3)if responses vary depending on if cues are produced by eitherjuvenileoradultconspecifics. Withourprotocol, thereisadifferenceinthecuesbetweenthetwochannels which is right onlyif significant differences are found between water containing ‘‘spying cues’’ and water containing potentialcommunicationcue (ifany).Thus, (C.viridis,P.pavo,A.novemfasciatus)sontattire´espardesconspe´cifiquesquin’ontjamais e´te´ en contact avec des larves (interception), tandis qu’une seule (D. aruanus) est re´ceptiveauxstimulie´mispardesconspe´cifiquesmisencontactvisuelavecdeslarves (communication).

acommunicationcuewouldbeonlyasignificantchoice comparedtounexposedones(spy).’

2. Methods

2.1. Studysiteandfishcapture

Larval fishwere collectedusingcrest nets[24,25] set off the west coast of Moorea Island (178300_58.8500_S, 1498550_26.7700_{W)inOctober2009andJanuary2010.Among} alllarvaecaptured,seventargetspecieswerecollectedin highabundance(60larvaeperspecies):fivepomacentrids (Stegastesfasciolatus,Chromisviridis,Chrysipteraleucopoma, Dascyllus aruanus, Pomacentrotus pavo), one apogonid (Apogonnovemfasciatus)andoneacanthurid(Ctenoachaetus Ctenoachaetusstriatus).Larvaewerecapturedatnight,just priortoenteringthelagoontorecruit[24]andthushadno priorexperienceofreefhabitats(i.e.naı¨velarvae).

Larvae were collected at dawn, transferred to the laboratory, and subsequently maintained in aquaria (0.30.20.2m) until 2100hours when experiments were begun [17,26]. Prior to initial experiments and between all subsequent experiments, each fish was maintained in individual aquaria supplied with flow-through seawaterfromtheadjacentlagoon, andfree of addedartificialornaturalhabitats.

Conspecifics,usedascuetransmitters,wereeither(a) larvae reared in aquaria for 15 days (juveniles) or (b) individualscapturedwithhandnetsintheMoorealagoon

(adults).Aquariacontainedlivecoralthroughoutthe 15-dayperiod,withjuveniles fed amixture ofrotifersand brineshrimpoverthisperiod.

2.2. Samplingprotocolofthechoiceflume

The responses of larvae to chemical cues from conspecifics were tested in a 2-channel choice flume (Fig.1).Twotankswereconnectedwiththechoiceflume bypipes, one perchannel,tocreate a constant gravity-drivenflow(1L/min).Dyetestsconfirmedlaminarwater flow in each channel, with water from both channels mixinginthedownstreamcompartment.

Foreachtest,asinglelarvawasplacedintothecentreof the downstream end of the choice flume (downstream compartment)for a 1minacclimatization period(a net prohibited thelarva from swimminginto theupstream channels).Attheendofacclimatizationperiod,thenetwas removed and a 4min test period began. The test was finished when the larva stayed more than 25s in an upstreamchannel(AorB,Fig.1)oraftera4minperiodin whichthelarva madenochoice(larvamovingbetween channelsorstayinginthedownstreamcompartment).This samplingprotocolwasvalidatedbypreviousexperiments conductedbyLecchini[18,26,27].Moreover,preliminary tests conducted on five toeight larvae of each species showedthatatleast80%ofthelarvaefromeachspecies swam between channels, and thus would come into contactwithbothodorsbeforemakingadecision.

Fig.1.Adiagramofthe2-channelchoiceflume(6010cm;waterdepth,5cm).Twotanks(2010cm;waterdepth:30cm)weresimultaneously connectedwiththetwoupstreamchannels(AandB)ofthechoiceflumebypipestocreateconstantgravity-drivenflowintoeachchannelat1L/min(flow rateandlaminarflowequalbetweenthetwochannels).Dyetestsshowedlaminarwaterflowineachchannelandshowedthatwaterwasmixed homogeneouslyinthedownstreamcompartment.Then,waterexitedtheflumebetweenthetwopanels,pastanetbarrierthatpreventedfishfrom escaping.Larvaewereinitiallyplacedinthedownstreamendofthechoiceflume,thencouldeitherstayinthedownstreamcompartmentormovetoward thetwoupstreamchannels.

2.3. Choiceflumeexperimentstodetectchemicalabilitiesof fishlarvae

Usingthisprotocol,threeexperimentswere conduc-ted using 20 larvae per species per experiment. Firstly, we determined the distribution of side choice exhibitedbylarvaewhenexposedtochemically identi-cal artificialseawaterin bothchannelstodiscount the presenceof aninnatesidepreference(i.e.,controltest) (Exp.1).Then,wetestedwhetherlarvaecandistinguish between, and exhibit a preference for, the odour of conspecificsthathadbeenexposedtolarvae(suggesting communication) or conspecifics that had not been exposedtolarvae(suggesting spying). Ifnopreference were observed, this would suggest that the chemical cues did not differ between treatments.This test was repeated twice, once using the odour of juvenile conspecifics(Exp.2)andagainwiththeodourofadult conspecifics(Exp.3).

Forspyingcues,5conspecifics(eitherjuvenileoradult) wereplacedfor3hina10-Laquarium(filledwithartificial seawater) without visual contact with fish larvae. For communicationcues,fiveconspecifics(eitherjuvenileor adultstage)wereplacedfor3hina10-Laquarium(filled withartificialseawater)withvisualcontactwith conspe-cific larvae in anotheraquarium setup one centimetre away.Thus,inexperiments2and3,larvaewereoffereda choicebetweenwatercontainingtheodourofconspecifics thathadobservedlarvaevs.watercontainingtheodourof conspecifics that had not. Observations of juvenile and adultconspecificsinaquariasuggestedthattheybehaved differently when they had visual contact with larvae, appearing to swim faster than when visual cues were absentandoftenswimmingclosetothelarvalaquarium. Differences in behavioral responses could alter the chemical signature produced by conspecifics. Thus, the ‘‘spying’’ and ‘‘communication’’ effect as defined in our experimental design is an indirect testing of these behavioralresponses.

Foreachindividualtrial,alarvacouldeitherstayinthe downstream compartment or swim in one of the two channels(Fig.1).Followingeachtrial,thechoiceflumewas emptiedandwashedwithfreshwater;andthepositionof channelsfilledwithspyingorcommunicationcueswere switched.

2.4. Statisticalanalysis

Foreachspecies,a

x

theobserveddistributionoflarvae(Exp.2orExp.3)toa baseline distribution (number of larvae in each com-partment during the Exp. 1) in order to determine if larvaewereattractedtoconspecificscuesfromjuveniles oradults. If was anattractionwas indicated,a second

x

testwithacorrectionofBonferronitestformultiple tests was conducted comparing the observed distribu-tion of fish larvae in the channel filled with spying cuesvs.thechannelfilledwithcommunicationcuesin ordertodetermineiflarvaeexhibitapreferenceforthe odour of water containing spying vs. communication cues.

3. Results

Inthecontrolexperiment(Exp.1),allspeciesexhibited either a homogenous distribution between all three choices in the flume (e.g., C. leucopoma: left channel: 6larvae;rightchannel:8;downstreamcompartment:6;

x

0.05,2=0.40,P=0.96),ortheydidnotmake adecision,

withthemajorityremaininginthedownstream compart-ment (e.g. S. fasciolatus, left channel: 4 larvae; right channel:2;downstreamcompartment:14)(Fig.1a).These resultsconfirmedthatthechoicesmadebylarvaewerenot influencedbyphysicalaspectsoftheflumesystem,most importantlyconfirmingthattherewasnoinnateleft/right channelpreferenceinanyspeciestested.

Whenjuvenile‘‘spying’’vs.‘‘communication’’cueswere compared (Exp. 2),only C. viridis and A. novemfasciatus showedasignificantattractiontothechannelscontaining the‘‘pure’’cuesources(Fig.1b).Forexample,60%ofC.viridis wereattractedbythechannelfilledwithcommunicationor spyingcues.C.viridislarvaewerethensignificantlyattracted byconspecificscues(

x

0.05,2=15.7,P<0.001),butdidnot

distinguish between communication and spying cues (

x

0.05,1=0.01,P=0.9).Similarly,A.novemfasciatus larvae

were attracted by conspecifics cues (

x

0.05,2=28.1,

P<0.001),butdidnotdistinguishbetweencommunication andspyingcues(

x

0.05,1=0.3,P=0.6).

Whenchannelswerefilledinwithwatercuesobtained from adults (Exp. 3), C. viridis, P. pavo, D. aruanus and A.novemfasciatusshowedasignificantattraction(Fig.1c). C.viridis,P.pavoandA.novemfasciatuswereattractedby conspecific cues (

x

0.05,2=54.6,P<0.001;

x

P<0.001;

x

0.05,2=49.8,P<0.001, respectively),but did

notdistinguishbetweencommunicationandspyingcues (

x

0.05,1<3.84, P>0.05). For example, 40% of C. viridis

larvaewereattractedbythechannelfilledwith commu-nicationcuesand 50%bythechannelfilledwithspying cues. In contrast, D. aruanus larvae were attracted by conspecific cues (

x

0.05,2=10.8, P=0.005) and preferred

communicationcues(

x

0.05,1=4.0,P=0.04).

4. Discussion

Thefindingsofthisstudysuggestthat,whilelarvaeare attractedtoconspecificchemicalcues(fouroftheseven species tested), theygenerally do differentiate between ‘‘spying’’ and ‘‘communication’’ cues. However, it does appear that some species have greater sensitivity to conspecificsatspecificlifestages.Whilethisstudyused a negative control(blankseawater), no positive control wasincluded(seawaterplusodorofheterospecificorodor of conspecific in the two channels). Therefore, any preferenceforunmixedcueinchannelsmaysimplyreflect the existence of an olfactory gradient or presence of ammonia or othergeneral physiological byproductsnot uniquetoconspecifics.Nevertheless,previouspapershave suggestedthatthefourspeciesattractedbyconspecifics cuesinthepresentstudy(C.viridis,P.pavo,D.aruanusand A. novemfasciatus)candifferentiatebetween theodor of conspecificsandheterospecifics[17,18].

Thelevelofsocialorganisationthataspeciesexhibits maydeterminewhetherornotthelarvaeareattractedto

conspecifics.Among the fivepomacentrid speciestested, C.viridis,P.pavo,andD.aruanusexhibitedanattractionto conspecifics cues. Yet, all three species are gregarious, generallyforminggroupterritorieswithbothjuvenilesand adults[28,29].Incontrast,C.leucopomaandS.fasciolatus larvaewerenotattractedtoanyconspecificcues.Juvenile andadultS.fasciolatusareaggressive,territorialandsolitary

[30] and adults will actively attack conspecifics [29]. Likewise, juvenile and adult C. leucopoma are generally solitary,occasionallyoccurringinpairsortrios[31].Social organisation may also explain the variable chemical

attraction to conspecific cues in the non-pomacentrids tested,namelytheattractiontocuesinA.novemfasciatus andthelackofanyattractioninC.striatus.Newlysettled A.novemfasciatusschoolwithjuvenilesandadultsonreefsat Moorea,whilenewlysettledC.striatusaresolitary[28].Fora settlinglarvaeofaspecieswithastrongsocialstructure, usingchemicalcuestolocateolderconspecificsmaybethe beststrategyfor quicklylocatingessential resourcesand reducing mortality risk while for non-schooling species alternative cues, i.e. those that originate directly from preferredhabitatsorfoodresources,maybeusedforthis

Fig.2.Olfactorycuepreferencesoflarvalreeffishesbasedontwochannelchoiceflumetrials.Inthecontrolexpriment(Exp1),thetwochannelswerefilled withcontrolseawater.Intheexperimentwithjuvenilecues(Exp2)oradultcues(Exp3),thetwochannelswerefilledwithwatercontainingeither ‘‘communication’’or‘‘spying’’cuesfromjuvenilleoradultconspecifics.Thedownstreamcompartmentrepresentsthepercentageoflarvaewhichshowed nopreferenceforeithercue: x2

testcomparingtheobserveddistribution(juvenilesoradultsexp.)toabaselinedistribution(controlexp.)identifieda significantdifferencebetweendistributions(Pvalue<0.05): x2

testcomparingtheobserveddistributionoflarvaeinchannelfilledwith‘‘spying’’cuesvs. inchannelfilledwith‘‘communication’’cuesidentifiedasignificantdifferencebetweendistributions.

purpose. However,the mostefficient chemical cues to locateolderconspecificswouldbeemittedbytheadults (Fig. 2). P. pavo and D. aruanus larvae were more sensitiveto adult cues.C. viridis andA.novemfasciatus larvaeweresensitivetobothadultsandjuvenilescues. Nofishspeciestestedwasonlysensitivetojuvenilecues. Theseresults suggest that chemical cues of immature individuals (juveniles) would be treated by perceivers (larvae)aslessinformativethanthoseofadults,possibly due to the greater vulnerability of juveniles to reef predators, their lack of experience onthe reef, and/or duetoincompletedevelopmentofphysiologicalprocess in juveniles that become more perceptible in adults. Similar hypotheses have also been used to explain ontogeneticvariationinmammalianalarmcue produc-tion, withalarm vocalizationsof immatureindividuals often treated by perceivers as less provocative than thoseof adults[32].

Whilethreeof thestudyspeciesdidnotdistinguish between cues, one species (D. aruanus) exhibited a preferencefortheodourofconspecificsthathadvisual contactwithlarvae(i.e.acommunicationcue).Thelarvae ofsomespecies(includingD.aruanus[33];Lecchini,pers. obs.) colonize the reef in successive waves of larval cohortsthatsettleduringthenight.Hypothetically,the first waveof larvalcohortscould recruit ontohabitats occupiedbyjuvenileandadultconspecificsusing habitat-specificcues[18].Settlinglarvaemayprovokeanactiveor passive behavioural modification in conspecifics that increases theattractiveness or potency of their odour, facilitating the recruitment of further larval cohorts. Nevertheless, this hypothesis needs both field and experimentalvalidationtodeterminewhether conspecif-icbehaviourchangesoncelarvaebegin settlementand whetherthisinturnaltersthemolecularstructureoftheir odourmolecules.

5. Conclusion

Theabilityofanimalstogatherinformationabouttheir social and physical environment is essential for their ecologicalfunction.Incoralreeffisheswithpelagiclarval stages, recruitment to appropriate habitats is essential

[34]. However, the unlikelihood of encountering these oftenrarehabitatsatrecruitmentbychance[11]means that the identification and incorporation of multiple sources of sensory information is essential for locating placestosettleandultimatelyresideasadults[15].While theadaptive benefits ofsocial recognition mechanisms, suchasspying orcommunication, atlarval recruitment remainunclear,theresultsofourstudysuggestconspecific chemicalcuescanbeusedbycoralreeffishlarvaetolocate appropriatehabitats. However,thenatureof thesecues mayvary,withoneofthesevenspeciestested(D.aruanus) potentiallymodifyingtheirodourtoincreaseitsattractive tofishlarvae.

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