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Influence of boat noises on escape behaviour of white-spotted eagle ray Aetobatus ocellatus at Moorea
Island (French Polynesia)
Cecile Berthe, David Lecchini
To cite this version:
Cecile Berthe, David Lecchini. Influence of boat noises on escape behaviour of white-spotted eagle ray Aetobatus ocellatus at Moorea Island (French Polynesia) . Comptes Rendus Biologies, Elsevier, 2016, 339 (2), p. 99-103. �10.1016/j.crvi.2016.01.001�. �hal-01297683�
Ethology/E´thologie
Influence of boat noises on escape behaviour of white-spotted eagle ray Aetobatus ocellatus at Moorea Island
(French Polynesia)
Influence des bruits de bateaux surle comportement de fuite
des raies-aigles Aetobatus ocellatus a` Moorea (Polyne´sie franc¸aise)
Cecile Berthea,David Lecchinia,b,*
aUSR3278CNRS–EPHE–UPVD,CRIOBE,98729Moorea,FrenchPolynesia
bLaboratoired’Excellence‘‘CORAIL’’,98729Moorea,FrenchPolynesia
ARTICLE INFO
Articlehistory:
Received7June2015
Acceptedafterrevision4January2016 Availableonline5February2016
Keywords:
Acousticcues Escapebehaviour Pearlfarming Predation
Motscle´s: Signauxacoustiques Comportementdefuite Culturedel’huıˆtreperlie`re Pre´dation
ABSTRACT
The present study tested different sounds that could disturb eagle rays (Aetobatus ocellatus)duringtheirforagingactivitiesatMoorea,FrenchPolynesia.Resultsshowedthat artificialwhitesoundandsingle-frequencytones(40Hz,600Hzor1kHz)didnothavean effectonrays(atleast90%ofrayscontinuedtoforageoversand),whileplaybacksofboat motorsoundsignificantlydisturbedraysduringforagingactivity(60%exhibitedanescape behaviour).Overall,ourstudyhighlightedthenegativeeffectofboatnoisesontheforaging activityofeaglerays.Thesenoisesproducedbyboattrafficcould,however,havesome positiveeffectsformarineaquacultureiftheycouldbeusedasadeterrenttorepelthe eaglerays,mainpredatorsofthepearloysters.
ß2016PublishedbyElsevierMassonSASonbehalfofAcade´miedessciences.Thisisan openaccessarticleundertheCCBY-NC-NDlicense(http://creativecommons.org/licenses/
by-nc-nd/4.0/).
RE´ SUME´
Notree´tudetestediffe´rentstypesdesonsquipourraientperturberlesraies-aigles(Aetobatus ocellatus)pendantleurprisedenourrituredanslelagondeMoorea,enPolyne´siefranc¸aise.
Lesre´sultatsmontrentquelebruitartificielblancoudesfre´quencesuniques(40Hz,600Hz ou1kHz)n’ontaucuneffetsurlesraies(aumoins90%desraiescontinuentdesenourrirdans lesable),tandisquel’enregistrementd’unmoteurdebateaulesperturbesignificativement danscetteactivite´ (60%desindividusontuncomportementdefuite).Notree´tudemetainsi ene´videncel’effetne´gatifdesbruitsanthropoge´niquessurlesactivite´sdenourrissagedes raies-aigles.Cesbruitsproduitsparlesbateauxpourraientne´anmoinsavoiruneffetpositif pourl’aquaculturemarines’ilspouvaienteˆtreutilise´scommere´pulsifsdesraies,principaux pre´dateursdel’huıˆtreperlie`re.
ß2016Publie´ parElsevierMassonSASpourl’Acade´miedessciences.Cetarticleestpublie´
enOpenAccesssouslicenceCCBY-NC-ND(http://creativecommons.org/licenses/by-nc- nd/4.0/).
* Correspondingauthor.BP1013,Papetoai,98729Moorea,FrenchPolynesia.
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.2016.01.001
1631-0691/ß2016PublishedbyElsevierMassonSASonbehalfofAcade´miedessciences.ThisisanopenaccessarticleundertheCCBY-NC-NDlicense (http://creativecommons.org/licenses/by-nc-nd/4.0/).
1. Introduction
Anthropogenic (human-made) noise is a form of pollution that is contributing increasingly to natural soundscapesonaglobalscale[1,2].Anthropogenicnoise causes physiological, neurological and endocrinological problems, increased risk of coronary disease, cognitive impairment and sleep disruption of many mammals, reptiles,fishesandinvertebratestaxa[3–6].Forexample, behaviouralimpactsonfishes(sharksandteleost)include lowerfeeding frequencies [7], increasedmovementand displacement[8,9],impairedorientationinlarvae[10],and slowerreactiontimes[7].However,anthropogenicnoises producedbyboattrafficcouldhavesomepositiveeffects formarineaquacultureifthesesoundscouldbeusedasa deterrent to repel the predators of oysters, mussels or otheraquaculturetaxa[11,12].
Formarineaquacultureindustries worldwide,depre- dation is an important and long-standing issue [11,13,14]. Farmers and researchers have been testing different techniques (e.g., magnetic or electric field, acousticbarrier,bubblecurtain,cages)toreducepredation onmarineaquaculture[11,14,15].For example,mussels areafavouritepreyitemfordivingducksinScotlandand Canada,andfarmersknowthattheycanuseboatstoscare thebirds.Rossetal.[12]reproducedtheboatmotorsound withanunderwaterplaybacksystemtoavoidusingreal boatsandtoreducecosts,thusdemonstratinganeffective alternativedeterrent when thefarmers wereabsent. In FrenchPolynesia,thepearlfarmingindustryisthesecond economic pillar of the country, representing 60% of all exports[16].However,theoysterfarmersconveythatthe industryhasbeenheavilyimpactedbypredationbyteleost fishes,raysandothertaxaforseveralyears.Althoughother animals,suchastriggerfish,turtles,andpufferfishpreyon the black-lipped pearl oyster Pinctada margaritifera in FrenchPolynesia,thewhite-spottedeagleray,Aetobatus ocellatus,isoneofthemostdetrimentalpredators[15].The eaglerayswerenotonlyeatingalargequantityofoysters, buttheywerealsodestroyingoysterlong-lines[15].
Asmanyoysterfarmersobservedthatthepresenceofa boatnearlong-linesdisturbedrays,inthepresentstudy, wefocussedontheuseofanacousticsystemtodetereagle raysfromoysterfarms.Specifically,ourfieldexperiments investigated behavioural responses of eagle rays to differentsounds: boat motor’s sound, white noise, and threesingle-frequencytones(40Hz,600Hz,1kHz).
2. Methods
Thepresentstudywas conducted onadultsofwhite- spotted eagle rays A. ocellatus (range size: 1.0 to1.3m) foragingunderanchoredboatsonthenorthcoastofMoorea Island, French Polynesia (17829023.0900S 14985106.0600W) fromOctober2012toNovember2013.Theacousticsystem usedinfieldexperimentsconsistedofa7Vbattery(Yuasa NP2.1-1)connectedtoanamplifier(FormulaF-102,CA,USA), connectedtoanmp3player(SansaClip1,SanDisk,Milpitas, CA,USA). All the equipment wasset up ina waterproof casing.Themp3playerwas connectedto anunderwater loudspeaker (UW-30, frequency response 0.1–10kHz,
UniversitySound,Columbus, USA)witha 4mlong cable toallowtheplacementofthespeakerasclosetotheraysas possible(about1mabovetheanimal–depthofsite:5m).
Theacousticsystemwassurroundedbyabuoy,forpositive buoyancy and pushed in the field by an observer. The observer playedsoundassoonasa raywas spotted.The soundswereplayedonlywhiletheraywasinfullviewand foragingoversand.Whenaneaglerayfinishedforaging,was waiting forprey,orwasresting, theexperimentwasnot conducted.Iftheraywasnotfeeding,itlefttheareaifan observerapproached[15,C.Berthe,unpublisheddata].
First, a control experiment was conducted on nine individualsinordertodetermineifthepresenceofthe acousticsystemand/orobserverelicitedflightbehaviour inwhite-spottedeaglerayswhentheyforagedoversand.
Thesystemwiththeloudspeakerswitchedoffwasplaced neartheray(about1mabovetheanimal)withoutplaying anysound,andtheobserverwaspositioned5mfromthe ray.Theray’sbehaviourwasnotedduring5minutes(i.e.
escapeorcontinuetoforage).Secondly,fivesoundswere tested: boat motor, white noise and three single- frequencytones(40Hz,600Hz,1kHzwhichcorrespond to, respectively, low, medium and high frequency perceivedbyelasmobranchfishes–[17,18]).Theartificial whitenoise(signalofwhichitsfrequenciesarerandomly distributedwithinaspecifiedfrequencyrangeresultingin a constant power spectral density – sound waves extending over a wide frequency range: 10 Hz to 22 kHz) and the three single-frequency tones were created withAvisoftSasLabPro[10,19].Ten 30-second replicateplaybackspersound(whitenoise,40Hz,600Hz, 1kHz)wereconstructed.
Fortheboatmotorsound,recordingsweremadeata depthof5moutsidethebarrierreefofMoorea(at2km awayfromthenearestreef)usingahydrophone(HiTech HTI-96-MINwithinbuiltpreamplifier;sensitivity–165dB re1V/mPa;frequencyrange2Hz–10kHz;HighTechInc., GulfportMS)andasolid-staterecorder(EdirolR-09HR16- bit recorder; sampling rate 44.1kHz; Roland Systems Group,Bellingham WA).A boat witha 25 horse power Yamaha engine started 50mfrom thehydrophone and drove past in a straight line for 100m; passing the hydrophoneataclosestdistanceof10m.Therecorderwas fullycalibratedusingpuresinewavesignalsgeneratedin SASLab(Avisoft,Germany),playedonanmp3player,and measured inlinewithanoscilloscope[6,10].Recordings were clippedinto 30-ssamples sothat whenboat was present a whole pass was sampled. Ten 30-s replicate playbackswerethenconstructed.
Asambientnoiseattheexperimental sitewasnever above80dBre1mPa(acrossallfrequencybandsbetween 10and2000Hz–[19]),thesoundlevelofourfivesound compositeswascalibratedat,atleast90dBre1mPaRMS byplacingahydrophoneat1mofhigh-speaker(Fig.1)to ensurethatitwasabovethelocalambientnoisefloor.To checkthequalityofboatsoundemittedbytheloudspeak- er, soundpressure and particle acceleration were mea- suredusingthehydrophone(describedabove)andaM30 accelerometer (sensitivity 0–3kHz, manufactured and calibrated by GeoSpectrum Technologies, Dartmouth, Canada; recorded on a laptop via a USB soundcard, C.Berthe,D.Lecchini/C.R.Biologies339(2016)99–103
100
MAYA44, ESI Audiotechnik GmbH,Leonberg, Germany).
Acoustic analyses performed in MATLAB v2010a were describedbyHollesetal.[10]andNedelecetal.[6].
Overall,59raysweretestedusingonlyonesoundper ray(i.e.10rayspersoundtypeand9raysforthecontrol experiment), and the duration of sound exposure was 5minutes.Twobehavioural responseswererecordedin real-timeforeacheagleray:noreaction(i.e.raycontinued toforageoversand)orescapebehaviour(i.e.swamaway fromtheforaging siteat,atleast,50m).Raysareeasily distinguishable due to the individual pattern on their dorsalside(C.Berthe,unpublisheddata).Thus,noraywas tested twice during theexperiment.A first x2 test was conductedonthefivesoundtypesinordertoassessifrays hada significanthomogeneousorheterogeneousbehav- iouraccordingtothetestedsounds.Then,asecondx2test wasconductedtocomparethenumberofraysshowing
escapebehaviourwithonesoundtypecomparedtothe control test (i.e. five x2 tests conducted) to determine whetheraparticularsoundhadasignificanteffect(escape behaviour) on the rays. The statistical analyses were conductedusingRsoftwarev2.11.1(RDevelopmentCore Team,2010).
3. Results
During the control experiment, rays did not exhibit escape behaviour. The 9 tested rays didnot moveand continuedto forage duringthe five-minute observation period(Fig.2).Thisresultconfirmedthatrayswerenot disturbedbythepresenceofanobserver.
During the sound tests, rays exhibited significant heterogeneousbehaviourdependingonthesoundtested (x20.05,4=18.2,P<0.001,Fig.2).Forexample,60%ofrays swamatleast50mawayfromtheforagingsitewhenthe boatmotorsoundwasplayed.Amongthesixraysthatfled, fourswanawayinthe10firstseconds,1between1and 4minand1duringthelastminuteofboatplayback.Onthe contrary, no ray exhibited escape behaviour when the 600Hzsound was played. Thus, none of thesounds at 40Hz,600Hz,1kHzorthewhitenoiseresultedinaltered raybehaviour(i.e.comparisonbetweensoundandcontrol tests–x20.05,1<3.84,P>0.05),andtherayscontinuedto forageoversand(Fig.2).Incontrast,thesoundsoftheboat motorelicitedsignificantlymoreescapebehavioursduring foragingactivity(x20.05,1=37.7,P<0.001).But,nosignifi- cant relationship was highlighted between the sound intensitiesofboat(between90and120dBre1mPaRMS) andthetimefortheeagleraystoescape(i.e.66%ofrays exhibitedanescapebehaviourduringthe10firstseconds, corresponding to the lowest sound intensities of boat noise–90and98dBre1mPaRMS,Fig.2).
Fig.2.Eaglerays(Aetobatusocellatus)behaviourrelatedtothecontroltest(withoutsound–switched-offloudspeaker)andthetestedsounds:aboatmotor sound,awhitenoiseandthreesingle-frequencytones(40Hz,600Hz,1kHz).Tenraysweretestedforeachsoundtypeandnineraysforcontroltest.Two possibleresponsesofeaglerayswereobserved:noreaction(i.e.continuetoforage)orescapebehaviour(i.e.swamawayfromtheforagingsiteat,atleast, 50m).Starsindicateasignificantdifferencebetweenthenumberofraysshowingescapebehaviourwithonesoundtypeandthecontroltest(x2test– P<0.05).
Fig.1.Soundenvelopeofboatplayback,whitenoiseandthethreesingle- frequencytones(40Hz,6000Hz,1000Hz)during30secondswithall soundcalibratedat,atleast90dBre1mPaRMS.
4. Discussion
Ourstudyshowedthenegativeeffectofboatnoiseson theforagingactivityofeaglerays.Thus,60%oftherays testedstoppedforagingandfledtheareawhentheboat motorsoundwasplayed(Fig.2).LocalfarmersinFrench Polynesia observed that eagle rays exhibited escape behaviour when a boat approached, and our findings confirmedthisobservation.Moreover,ourfieldobserva- tions allowed us toidentifythat 66% of eaglerays fled between1to10secondsafterthebeginningofboatsound (soundcharacterized by lowfrequencies – <350Hz–at thebeginningofrecording).Thesefieldobservationsare consistentwiththoseofCasper[17],whodemonstrated thatelasmobranchesmainlyperceivedtheparticlemotion, which is moreprevalent at low frequencies. Sharksare thought to be attracted to low frequencies because stressedpreysemitlowfrequencysounds[17,18,20].Eagle raysareafavouritepreyitemofthehammerheadshark [21]andcouldbemorereactivetolowfrequenciestoavoid shark’spredation.However,ourstudyshowednoescape behaviourwhenonlyasingle-frequencytonewasplayed (40Hz,600Hzor1kHz).Therefore,itmaynotbejusta specificlowfrequency(asthe40Hztestedinthepresent study)thatdisturbstheeagleraysduringtheirforaging activity,butratheracombinationofsoundlowfrequen- cies.Thishypothesisshouldbevalidatedbyfuturestudies onawholegroupofrays,asthebehavior,suchasescape,is oftendependentoftheschooldensity[22]andthatasocial organization was described in spotted eagle ray (same genusAetobatus)[23].
Worldwide, a lot of research has been done on aquaculturepredation[12,24–26],but asidefromuseof boatnoise,fewreliableandaffordablesolutionshavebeen found[12,27]. Our study confirmedthat anthropogenic noise, such as that produced by boat traffic could negatively affectthewhite-spotted eagleray, similarto othermarine speciesas indicated in earlier studies[1–
3,6].Thisnegativeeffectoneaglerayscouldbeusedby humanstobenefitmarineaquacultureifsuchsoundsdeter thepredatorsofpearloysters[11,12].Furtherexperiments mustbeconductedinsitu,nearoysterlong-linesandovera long-termperiodinordertodetermineifanunderwater playbacksystemcouldbeusedtoefficientlydetereagle rays fromoyster farmswithout negativeeffects on the growthofoystersandonthequalityoftheblackpearls.
Moreover,Newboroughetal.[28]showedtheproblemof habituation effects with acoustic repulse systems that removecetaceansfromfishnets.Toreducethelikelihood ofhabituationofeaglerays,localfarmerswouldneedto usedifferentrecordings,includingsounds fromdifferent boat types or by using irregular temporal and spatial patterns when playing back sounds. Overall, our study showed,forthefirsttime,thatboatnoiseisdetrimentalto theeaglerays,butthisnegativeeffectcouldbeusedby Humantodetertheraysfromoysterfarms.
Acknowledgements
This research was supported by a grant from the
‘‘Directiondesressourcesmarinesetminie`res’’ofFrench
Polynesia.TheauthorswouldliketoacknowledgeCe´drik Loforhishelptobuildthisstudy.
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