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Hawaii, POBox 1106,Kailua, HI96734,USA. MarineBiology, Research Program,Hawaii Instituteof University of MA 02543,USA. *Author ([email protected]) for correspondence Sciences, 62Fenghuang Road, Sanya 572000,. theChineseAcademy of Deep-seaScienceandEngineeringof Institute of Received 11 July2013;Accepted1October 2013 attributed. use, distribution andreproductioninany mediumprovided that isproperly theoriginalwork Attribution License(http://creativecommons.org/licenses/by/3.0), unrestricted permits which theCreative Commons of distributed undertheterms This isanOpenAccessarticle ‡ 1 444 1901; Roffler andButler, 1968).Theshapeoftheouterearinfluences serve toconductsoundthemiddleandinnerear(Angell Fite, In terrestrialmammals,structuressuchasthepinnaeandear canal Marine mammal,Odontocete,Communication KEY WORDS:Sensory, Auditorybrainstemresponse,Noise, mayhaverelativelylessacoustic‘shadowing’. odontocetes intheanatomyrelatedtoreceivingsound,and head. Theresultssuggestthattherearedifferences among interrelated whenconsideringsoundreceptionacrosstheodontocete amplitudes, whichsuggeststhatlatencyandsensitivityare heads. Responselatenciesincreasedwithdecreasingresponse which 30–40 contrasts withtestsbottlenosedolphinsandbelugawhales,in different atlocationsfromtherostrumtiptoear(11.6 overlaying theauditorybulla.Meanthresholdswerenotsubstantially thresholds werefoundadjacenttoamandibularfatpadand the samesubspecies.Thebesthearinglocationswithminimum using computedtomography(CT)imagingofdeceasedanimals frequencies andlocations,referencedtotheunderlyinganatomy cup transducer. Thresholddifferences werecomparedbetween presented atninelocationsontheheadandbodyusingasuction- potentials (AEPs).Clickandtonestimuli(8,54120 across thehead.Hearingwasmeasuredusingauditoryevoked broadband clicks,comparingsoundspresentedatdifferent locations asiaeorientalis finlessporpoise( reception. Here,weaddresshowadivergentsubspecies,the morphology amongodontocetessuggestsvariationinsound representative species.Thesubstantialvariationinjawandhead sound isreceivedacrosstheheadhasbeenlimitedtoafew ‘jaw hearing’ iswellsupportedforodontocetes, workexamininghow How ananimalreceivessoundmayinfluenceitsuseofsound.While T. AranMooney asiaeorientalis Hearing pathwaysintheYangtze finlessporpoise, RESEARCH ARTICLE © 2014.PublishedbyTheCompanyofBiologistsLtd|JournalExperimentalBiology(2014)217,444-452doi:10.1242/jeb.093773 Academy of Sciences, China. Wuhan 430072,People’sAcademy Republic of of theChinese Hydrobiology of Sciences, Instituteof Chinese Academy of Laryngology, MedicalSchool, Boston,MA02114,USA. Harvard INTRODUCTION ABSTRACT Biology Department, Woods HoleOceanographicInstitution,WoodsBiology Department, Hole, Present address:MarineMammalandBioacousticsLaboratory, Sanya

dB thresholddifferences werefoundacrosstheanimals’ ) hearslow-,mid-andhigh-frequencytones,aswell 2 Key Laboratory of Aquatic Biodiversity and Conservation of the of Aquatic Biodiversity andConservation Key of Laboratory 1, *, SonghaiLi Neophocaena asiaeorientalis 2,3,‡ 4 Department of Otologyand of Department , DarleneR.Ketten 3 Marine

kHz) were

dB). This 1,4 , KexiongWang of ‘acoustic’ fats. while providingacomparisonto auditoryanatomyandthelocation yet tocomprehensivelyexamine head/jawreceivedsensitivity al., 2008).Despitethesephysiological differences, nostudy has in dolphinsbutratheratthetip ofthelowerrostrum(Mooneyet demonstrates lowesthearingthresholds notfromthelowerjawas (Kastelein etal.,2005).The beluga( significantly widerreceivingbeamthanthebottlenosedolphin example, theharborporpoise( despite indicationsthattheyreceivesounddifferently. For cetacean species,withvariedjawmorphologies,receivesounds sound isreceived.Littleattentionhasbeenpaidtohowdivergent odontocete speciessuggestingatleastsubtlevariationin how Yet, thereare clearvariationsinthejawandheadmorphologiesof species, particularlyonbottlenosedolphins( of ‘jawhearing’,previousresearchhastendedtofocusona few receives lowerfrequencysounds(Popovetal.,2008). concept ofanadditionalpathwaynearthebulla,whichpreferentially hypothesis issupportedbyphysiologicaldata,particularlyforthe in eachspecies(Ketten,1994).Themandibularfathearing fat lobesassociatedwiththelowerjawthatvaryinsizeandshape 1989; Møhletal.,1999).Anatomicalstudieshaveshowndiscrete physiological studiesofdolphinreceivedsensitivity(Brilletal., by psychophysicalecholocationresearchanddetailed,non-invasive (Norris andHarvey, 1974).Odontocetejawhearingisalsosupported indicated aconcentrationofsoundthroughthethroatandjaws Sound transmissionmeasurementsthroughheadtissuesamples lowerjaw(Bullocketal.,1968;McCormick1970). studies, whichdemonstratedgoodhearingsensitivityfromthe intracranial-recorded evokedpotentialandcochlearaction Zahorodny, 2008).Thejawhearinghypothesisissupportedby incoming soundtotheears(Koopmanetal.,2006;Koopmanand within thelowerjaw, perhapsaffecting soundspeedtochannel that the‘acousticfats’ haveaspecifictopographicalarrangement Biochemical analysesofthelipidswithinodontoceteheadsshow conduct soundtotheinnerear(Varanasi andMalins,1972). acoustic impedance,suggestingthesefatbodiespreferentially Fats withintheodontocetemandiblearesimilartoseawaterin an acousticwindowofthepanbonetolowerjaw(Norris,1968). anatomical studiesproposedthatsoundpreferentiallytravelsthrough specialized adaptationsaroundthelowerjaw. Forexample,early external pinnae.Mostevidenceindicatestheyreceivesoundusing received levelsofnoisomesounds(Heffner andHeffner, 1992). of noiseexposurebyturningawayfromsoundsourcestodecrease mayalsousedirectionalitycuestolimittheadverseimpacts predators andprey, navigating andcommunicatingwithconspecifics. consequently importantbiologicalactivities,includinglocating Variations inthesecuesaidanimalssoundsourcelocalizationand the spectra,amplitudeandarrivaltimeofsounds(Müller, 2004). While thepropensityofevidenceclearlysupportsfoundation Odontocetes (toothedwhales,dolphinsandporpoises)lack 2 and DingWang Neophocaena phocoena 2 Delphinapterus leucas Tursiops truncatus). ) hasa )

The Journal of Experimental Biology Mandibular fatpad Lower jaw Flipper Back Overlying bulla Meatus Throat the lowermelon(one-way ANOVA, *Thresholds fromstimulipresented at thebackaresignificantlygreaterthanallothers; 1).Thethroatlocationwasslightly, but significantly different (Fig. jaw. Themeanthresholdsfromalltheselocationswerenot similarly lowoverlayingthebulla,atmeatusandlower 1).Thresholdswere tip andmandibular(cheek)fatpad(Table both animalswerelowestandnearlyidenticalattheporpoisejaw sensitivities. Themeanhearingthresholdsforallfrequenciesand Materials andmethods).Bothanimalsshowedgoodhearing This workexaminedthehearingoftwofinlessporpoises(see RESEARCH ARTICLE and themeanofallthresholds,relativetolocationsuction-cup transducer-presentedstimuli Table potential impactsofanthropogenicnoise. The resultsarethenviewedinlightoflocalizationcapabilitiesandthe sensitivity offinlessporpoisehearingacrossitsheadandlowerjaw. receive sound.Thegoalofthisworkwastoexaminetherelative subspecies (Popovetal.,2005),therearenodataregardinghowthey construction. Whilehearingrangeshavebeenestablishedforthis acoustic sourcesincludingshipping,dredgingandunderwater are ofconcernbecausetheseanimalsinhabitwaterswithsubstantial (Mei etal.,2012;Zhao2008).Noiseimpactsonthissubspecies (Turvey etal.,2007).Porpoisepopulationsare alsodecliningrapidly same busywatersasthenowlikelyextinctbaiji( population. Theyareaparticularconservationissueastheyinhabitthe is asubspeciesofthefinlessporpoiseandonlyfreshwater (Pilleri andGihr, 1972)]receivessound.TheYangtze finless Yangtze finlessporpoise[Neophocaenaasiaeorientalis groups orevendeterminetheapplicabilityofsuchactions. data onhearingdiversityitisunclearhowtoidentifyrepresentative species (NationalAcademyofSciences,2005).However, withlittle panels oftenstresstheneedfordatafromagreaternumberof and Hastings,2009).Regulatoryagenciesresearchreview influence directionality, localization andfrequencysensitivity(Au may besignificantastheshapeofsoundreceiverscangreatly Relative thresholds RESULTS Lower melon Jaw tip Here, weaddresshowadivergent speciesofodontocete,the Differences inhoweachspeciesofodontocetereceivessound P soundpressurelevel sinusoidallyamplitudemodulated V fast-Fouriertransform peak-equivalentrootmeansquare SPL envelopefollowingresponse SAM computedtomography peRMS auditoryevokedpotential FFT EFR CT AEP List of abbreviations List of p–p 1. Thresholdsforbothfinlessporpoises(Neophocaenaasiaeorientalis peak-to-peak voltage 5 4 9 7 8 6 3 oain Mean±s.d. Location 1 2 F 7,58 =12.34, P 55.7±9.8 61.1±6.6 orsos orsos orsos orsos Noresponse Noresponse Noresponse Noresponse No response 57.7±8.9 97.0±11.2* 59.3±8.1 67.0±12.3 Threshold (dB) 76.8±12.2 55.4±8.9 <0.001 andsubsequent Tukey’s pairwisecomparison). Lipotes vexillifer ‡ ‡ ‡ ‡ ,‡ 68.5 70.4 Click 82.3 99.1 68.3 70.2 65.7 65.3 ) (15–25 melon resultedinsubstantiallyhigherhearingthresholds mandibular fatpadorjawtipforallfrequenciesexcept8 frequency showlowestthresholdswhensoundenteredthe their hearingabilities. and femaleporpoisedidnotdemonstratesubstantialdifferences in when thetransducerwasplacedonanimals’ flippers.Themale animals’ backs(acontrollocation).Noresponsescouldbedetected thresholds werehighestwhenthetransducerwasplacedon tip, mandibularfatpad,meatusandoverlayingthebulla).Mean substantially higher(>20 Thresholds acquiredfromlowermelonstimulationwere frequencies except120 overlaying thebullaandatmandibularfatpad.Forall thresholds for8 most frequenciesandsubstantially(by20 2).Stimulationatthethroatlocationwasslightlyelevatedfor (Fig. The maximumsoundlevelpresentedwasdeemed0 increasing delays)werethenplottedrelativetothestimuluslevel. latencies assoundlevelsdecreased(Fig. waves I–IV. Thislineshowsacleartrendinlongerresponse visible withalinedrawnbetweentherespectivepeakvaluesof 4,5).Thiswasclearly to increaseassoundlevelsdecreased(Figs back. increased withstimulipresentedatthejawtip,lowermelonand or fasterthan,meatalstimulation.Relativeresponselatencies response regions(lowerjaw, cheek,overbulla),butonaparwith, tended tohaveresponselatencieslongerthanthoseofthemostrapid using soundpresentedatthemeatus.Throat-presentedstimuli bullae, valueswereoftensimilarlylow. Latenciesincreasedslightly 3).Whenthetransducerwasoverlayinganimals’ lower jaw(Fig. when transducerstimulationwasatthemandibularfatpadand potential (AEP)wavesI–IV. Thelatenciesweregenerallylowest Mean responselatenciesweremeasuredusingauditoryevoked F significantly, elevatedrelative totheselocations(one-wayANOVA, increasing soundattenuationandphysiological AEP relatively high,therewasasignificantpositiverelationshipbetween or 20 original peakvalueswasplottedforeachattenuationstep(5,10,15 and 0 Relative latencies 7,58 Responses fromtheindividuallocationsbrokendownbystimulus Response latenciesweredependentuponsoundlevelsandtended ‡ =12.34, thresholds aresignificantlydifferent fromthoseforstimulipresented at dB). ThiswasdoneforwavesII–IV. Whilethespreadis ms timedelay. Thedifference intimefromthoseofthe dB). The JournalofExperimentalBiology(2014)doi:10.1242/jeb.093773 P 56.7 62.0 120 61.9 85.4 54.8 59.1 53.7 50.9 <0.001 andsubsequentTukey’s pairwisecomparison).

kHz werefoundatthesidelocations:meatus,

kHz ) providedbyindividualstimulusfrequencies

kHz, stimulationatthelowerportionof

dB) thantheareasofbestsensitivity(jaw 60.3 59.5 86.3 107.6 49.0 53.3 42.5 49.0 54

kHz

4). Theselatencies(or dB) for8

dB attenuation kHz. Lowest 58.8 76.4 No response No response 58.7 54.6 61.0 56.5 8 kHz

kHz 445

The Journal of Experimental Biology locations andforbothanimals. physiological delaysincreased.Thiswastrueacrossallstimulus pairwise comparison). 446 RESEARCH ARTICLE overlaying thethin panboneregionofeachlower jaw. melon and,bilaterally, anintramandibularandalateralovoid pad (Fig. data fromcomputedtomography (CT)assessmentsanddissections dimensions wereuncertainbecause ofthisoverlap.Thecombined The mainjawfatbodieswere distinctbutexactedgesand which ledtosome‘fogging’ ofthefatbodies inautosegmentations. layers insomeareashadsimilarattenuationstothemandibular fats, part becauseoftheconditionstrandedspecimens,blubber an anatomicalrelationshipforthephysiologicalmeasurements. In scanned strandedpost-mortemspecimens(Figs the scansandthree-dimensionalreconstructionsofheads the The sensitivitiesfromthetransducerplacementswereplotted over delays (r locations (one-wayANOVA, *The backlocationhadsignificantlyhigherthresholdvaluesthanallother response wasdetectedfromstimulipresentedatthecontrolflipperlocation. (box), and±50%(whiskers).(B)Mean±1s.d.ofthethresholds.No (A) Boxplotsofthresholds,showingmeanvalue(dot),medianand±25% both finlessporpoises(Neophocaenaasiaeorientalis Fig. and female(gray)porpoises.SPL,soundpressurelevel. overlaying thebullaandback.(C)Thresholdcomparisonofmale(black) significantly different fromthoseatthejawtip,mandibularfatpad,meatus, AEP comparisonstoanatomy

1. Thresholdstoallsuction-cuptransducer-presentedstimulifrom SPL (dB re. 1 µPa) 100 7A) revealedthreefattyregions distinctfromblubber:the 100 120 100 80 40 60 40 60 80 40 60 80 2 =0.21; B A C melon melon Lower lower 123456789 P Jaw tip jaw tipgularlower <0.05). Inotherwords,assoundlevelsdecreased, ‡ ‡ Female Male Thresholds fromstimuliatthelowermelonwere

Throat F 7,58

=12.34, P Lower jaw jaw fat pad fat pad Cheek cheek ‡ <0.001 andsubsequentTukey’s Over bulla ‡

Meatus Back

6, 7).Thisprovided ‡ * ,‡

Flipper No response No response No response ). were notplotted.SAM,sinusoidallyamplitudemodulated. response wasdetectedfromsoundspresentedattheflipperandthosedata respective stimuluslocations. Fig. threshold fluctuation acrossmostofthehead(except fromthemelon some datascatter, althoughthebroadbandclicksshowedless sounds andorientationwithinthe localsoundscape. Lateral lowfrequencyhearing mayfacilitatelocalizationofthese porpoises alsoproducelowfrequency sounds(Lietal.,2008). important lowfrequencysoundscape cues,andneonatefinless porpoises, theambientenvironmentisfilledwithpotentially directionality (LammersandAu,2003;Popovetal.,2008).Yet, for frequencies wellfromtheside,presumablyforevaluatingwhistle of soundsincludinglowerfrequencywhistlesandhear be heardbestfromthefront.,incontrast,producea range echolocation sounds(Auetal.,1999;Li2005),whichwould as theyareconsideredtomainlyproducehighfrequency et al.,1999).A double-acousticwindowisintriguingforporpoises shows considerable(near40 sensitivity arelessspecificthaninthebottlenosedolphin,which frequency-dependent generalregionsoflowandhighfrequency for thebottlenosedolphin(Popovetal.,2008).Theporpoise’s investigations. Suchadouble-acousticwindowhasbeenproposed anterior positions;andatleastsuggesttheneedforfurther frequencies betterfromthesideandhigherat for thefinlessporpoise,theydoindicatetheseporpoiseshearlow these datamaynotconclusivelysupportadoubleacousticwindow was detectedbestusinglateral,meatalpresentedstimuli.While and atthemandibularfatpadlocation.Thelowerfrequency, 8 and click)werefoundwithstimulationtowardsthefrontofhead The bestresponsesforthehigherfrequencies(54,120 hearing thresholdswerenotparticularlysensitivefromthislocation. The lowermelonplacementwasnearthefatofbody, but of themandibularfats,particularlyintramandibularfatbodies. location wasnear, butnotdirectlyoverlaying,theanteriorportions produced thelowestthresholdsfor8 visualized acousticfatregions.However, themeatuslocation The jawtipandmeatusdidnotappeardirectlyassociatedwith shown intheVRT visualizationsoftheacousticfatsmandible. location overlayingthebullawasalsoneighboringthesetissuesas area. Thelowerjawlocationwasjustadjacenttothisfatregion. thresholds (greatestsensitivity),overlaidthefatbodyatpanbone Relative hearing DISCUSSION Examining relativesensitivities basedonfrequencydoesreflect The mandibularplacement,whichprovidedlowestclick

.Meanthresholdsofbothanimalsbystimulusfrequencyat 2. SPL (dB re. 1 µPa) 40 60 80 melon Lower The JournalofExperimentalBiology(2014)doi:10.1242/jeb.093773 Jaw tip Throat Lower

Data fromthebackwereexcluded.No dB) differences acrossthehead (Møhl jaw Cheek fat pad

kHz tone.Thethroat 8 kHzSAM 54 kHzSAM 120 kHzSAM 100 kHzclick Over bulla

Meatus kHz tones,

kHz,

The Journal of Experimental Biology signals presentedindBpeakto(dB expected forbriefsignalsandconsideringthedifference between generated elevatedthresholdscomparedwiththetones,whichis tones presentedindBrootmeansquare(dB respective waves(I,II,III,IV)arelabeledtotheright. the fourwavesfromallstimuluslocationswithadetectableresponse.The four ‘positive’ inflections ofthefirstclickareindicated(I–IV).(B)Latencies site, whichdidnotconductsoundswell)(Figs presented atthe‘lowerjaw’ locationat135 location. (A)Auditoryevokedpotential(AEP)waveformtoaclickstimulus Fig. RESEARCH ARTICLE studies havesuggested goodhearingfrom head pathwaysnot al., 1999;Mooneyet2008) and modeling(Cranfordetal.,2008) transmitted throughthebody’s tissues.Similarempirical(Møhlet from thebackisquiteunusual andsimplyreflectsthatsoundis Responses wereevengenerated fromtheanimal’s back.Hearing includes thejawtip,throat, meatusandoverlayingthebulla. associated withacousticfatswere particularlystriking(Fig. transmitted throughtheimpedancemismatchofboneisuncertain. investigating (Norris,1968).Howsoundcouldbeeffectively intramandibular fatandthentotheear, as Norrisalsoproposed adjacent fatbodyoristransmittedthroughthepanboneto the fat, suggestingthat,likeindolphins,soundiseitherconducted to the 1968). Thelowerjawoftheseporpoiseshaslimitedextramandibular preferentially conductsoundtotheear(Bullocketal.,1968;Norris, jaw, whichreinforcesprevioushypothesessuggestingacousticfats pathway forthefinlessporpoise. odontocetes (Cranfordetal.,2008),thisisnotapreferentialauditory were alsoelevated,suggestingthat,despitepredictionsinother echoes, butinanattenuatedmanner. Thresholdsfromthroatstimuli 2005). Thissuggestsapotentialmeanstoheartheirownclicksor near thecenterfrequencyofporpoiseecholocationsignals(Lietal., elevated relativetotheotherfrequencies.The120 system. Interestingly, the120 stimulation probablyreflectitsacousticisolationfromtheauditory was negligible.Thegenerallyhigherthresholdsformelon If thetoneswerecomparedindB The responsesandsensitivitiesfromlocationsthatare not Lowest thresholdswerefoundatthemandibularfatpadandlower

Latency (ms) Amplitude (µV) .RepresentativeAEP waveformandrespectivelatenciesby 3. 1.5 2.5 3.5 4.5 –2 –1 1 2 3 4 5 0 1 2 0 melon Lower B A I II III Jaw tip

IV 5 10

Throat

kHz thresholdatthemelonwasleast

Lower Time (ms) jaw p–p

15

, thisdifference inthresholds dB peakto(dB fat pad Cheek p–p ; clicks)andthoseofthe

20 25 RMS

Over bulla 2, 6,7).Theseclicks ) (Auetal.,2002). Meatus Back

kHz tonewas p–p IV III II II I I ). Thefirst

7). This

30 values. the regressionsslopetowardsincreasingdelaysforcorrespondingpeak in A.RegressionsofthepeakpositivewavesIIIandIVareoverlaid.Notethat 75 (A) AEP responsestoa100 Fig. regression. Allstimulus frequenciesarecombined. Response delaysincreasewithdecreasing sensationlevels,indicatedbythe Fig. by accessingbothears.Thesameisprobablytrueforthethroat is likelythatsoundpresentedatthislocationinfluencedresponses signals. a large roleinsoundprocessingandproperlyutilizingacoustic preferential acousticpathways.Thesesmalldifferences likelyplay conduction totheearmaybeinfluencedbysubtledifferences in free-field planewaveacrosstheheadandbody. Soundreceptionand 1988). Inwater, soundsaremoreoftenreceivedbyporpoisesina a fixeddifference, whichisvitalinnear-field experiments(Kalmijn, and Houser, 2006).Thismethodalsoprovidesconsistentstimuliat a consistenthearingmechanismbetweenthetwomethods(Finneran produces thresholdsthataresimilartofree-fieldstimuli,suggesting Further, priorworkhasshownusingasuction-cuptransducer parsimonious entrywayintothebulla(Cranfordetal.,2010). bone conduction).Yet, softtissuepathwaysoffer themost means notconsideredprimaryodontoceteauditorymechanisms(e.g. suction-cup transducermayhavegeneratedresponsesthrough necessarily associatedwithacousticfat.Oneconcernhereisthatthe While hearingthresholdswereprimarilylowestatthejawtip, it Delay (ms) dB Amplitude (µV)

–0.5 .Waveforms andlatencieswithrespecttostimulusamplitude. 4. .Delay ofwavesII,IIIandIVrelativetostimulusattenuation(dB). 5. 0 3 6 9 0 3 6 9 0.5 1.5 p–p 0 1 2 0 0 A . (B)Close-upoftheAEP waveformsillustratedbytheboxedregion B 0 510 1520 The JournalofExperimentalBiology(2014)doi:10.1242/jeb.093773

5 101520

2

kHz centeredclickat105,95,85,80and

Attenuation (dB) 4 Time (ms)

6 Wave IV Wave III Wave II

8 10

25 30 447

The Journal of Experimental Biology 448 RESEARCH ARTICLE from thejawtiptoear(~12 bulla, thissuggeststhatthesewereparticularlysensitivelocations. locations ofthemandibularfatpadandoverlayingporpoise measured.) Becauseminimumthresholdswerefromipsiliateral the contra-lateralside,althoughthesedifferences werenot primarily bytheipsilateralear. (They alsomayhavebeenshadedon on thesideofhead(lowerjawtoear)werelikelyreceived thresholds werecomparativelylow. Soundspresentedfromlocations response amplitudesrelativetoipsilateralstimulations,and et al.,2008).Soundreachingbothearslikelyincreasesevoked beluga whaleandthebottlenosedolphin(Møhletal.,1999;Mooney midline. Similarlow‘midline’ thresholdshavebeenshowninthe measurements. Inbothsituationsthetransducerwasplacedon C A Yet, meanthresholdswerenotsubstantiallydifferent atlocations click click 8 kHz 8 kHz SAM 8 kHzSAM C A +45 NR +18 NR +3 +4 +0 +7 +5 0 +4 +3 +3 0 NR NR

dB), suggestingthattheporpoise D B D B +0 +5 +4 +3 +7 0 +4 +3 receive sound. substantial differences canbefoundinhowdivergent odontocetes suggests thatwhilethereareconsistenciesinlowerjawhearing, animals’ heads (Møhletal.,1999;Mooney2008).This beluga ,forwhich30–40 porpoise headisincontrasttofindingsthebottlenosedolphinand separations. Therelativesimilarityofsensitivitiesacrossthefinless similarities (e.g.Popovetal.,2006)despitethesubstantialniche angles (Kasteleinetal.,2005),andmayreflectconservedauditory the harborporpoise’s ( receiving beamanddirectivityindex.Ifso,thiswouldbesimilarto in thresholdsacrossthefinlessporpoiseheadsuggestabroad may bequitesubtleforthefinlessporpoise.Theslightdifferences receives soundsimilarlyfrommultiplelocationsandsensitivitycues +3 0 +18 NR

The JournalofExperimentalBiology(2014)doi:10.1242/jeb.093773 click thresholds.CandDarefromthe8 no responsewasmeasured.A andBreflecthigh-frequency numbers reflecttherelativelyhigherthresholds;NRindicates thresholds, wherezerowasthelowestthreshold.Higher Circles reflectthesoundlevels(indB)ofrelative specimens showingthehead,boneandbodystructure. Fig. and 2,respectively. modulated tone.A,CandB,Dcorrespondtospecimens1

.Computedtomographytopogramsofboth 6. Phocoena phocoean

dB differences occuracrossthe these frequencies. off-axis viewsarepresented for the 8 broadband clicks.(D–F)Values for Relative thresholdvaluesforthe was thelowestthreshold.(A–C) the relativethresholds,wherezero reflect thesoundlevels(indB)of Circles bone; green,fatbodies. tomography images. reconstruction ofthecomputed Fig.

.Three-dimensional 7. kHz tone.Side,bottomand a) auditoryreceiving

kHz amplitude White,

The Journal of Experimental Biology 1984; Popovet al., 2008).We seefrom priorworkthatsoundlevels terrestrial mammalsaswell inotherodontocetes(Donetal., sound level(Figs from someanthropogenicsources. disadvantageous fordetectingintense impulsesounds,suchasthose duration, lowamplitudesounds, suchasecholocationechoes,but responses tosound.Thismaybeadvantageousfordetecting short help coordinatesoundtothebulla,increasingphysiological latencies guidingtheplanewaveacrosshead,i.e.anatomy may same time,mightbeeffectively enhancedbyanatomicallyinduced But aplanewave,whichdoesnotreachallpartsofthehead at the plane wave)wouldbedifficult todetectifreceivedasapointsource. example, lowamplitudereturningechoes(whichareeffectively a sound receivedatdifferent locations couldbesummatedintime.For reception andconductionfrommultiplepointsonthehead.Rather, bulla. Inthismanner, aplanewaveisnot entirely dissipatedbyits deceased odontocetes(NorrisandHarvey, 1974). These dataagreewithsoundspeedmeasurementscollectedfrom be lowestinimpedanceandpreferentialforsoundconduction. the shortestroutestoear, suggestingsoundpathwaysthatmay animals’ lower jawandmandibularfatpadlocations.Thesewerenot lower melon.Minimumresponselatencieswerefoundatthe were presentedfartherfromtheear, attheanimals’ backandatthe distance totheear. Thegreatestlatencies werefoundwhenstimuli Response latenciesvariedaccordingtostimuluslocationandrelative RESEARCH ARTICLE be affected bylowersignal-to-noiseratios. particular fishprey(Lietal.,2008;Luczkovich2000),may lower frequencycommunicationsignals,andthesoundsof echolocation signalsmaynotmaskedbymostnoise,detectionof may bedifficult forthefinlessporpoise.Whilehighfrequency the Yangtze River, detectingcertainimportantsignals fromnoise biologically importantcues.Inahighnoiseenvironment,suchas be substantiallyshaded.Thismayaidindetectinglowamplitude confounding signals.Soundsatoff-the-midline axisanglesmaynot to agreaterproportionofbothbiologicallyimportantsoundsand they receivesoundwellatmultiplelocations.Theymaybesensitive there arecorrelatesofdivergent auditorycapabilities. results seemtosuggestthatwithspeciesanatomicaldifferences, system. Thisisreflectedinvariationsreceivedsensitivity. These major roleinhowsoundsaregatheredandutilizedbytheauditory Hastings, 2009),complexmandibularanatomyseeminglyplaysa contributes substantiallytotransducerperformance(Auand influence jawmorphology. Yet, astheshapeandsizeofareceiver species isexpected.Inaddition,factorsotherthanhearingalso 2009), findingauditorydifferences amongdivergent odontocete or otherfactorsrequiresfurtherinvestigation. differences resultfromspeciesmorphology, simplesizedifferences years) (McGowenetal.,2009).Determiningwhetherthese porpoises themselvesareevenfartherremoved(5.60–11.60 million phylogenetically divergent fromotherodontocetes,andfinless surprising whenconsideringthatporpoisesarequite the riverineenvironment.Ingeneral,thesedifferences arenotvery not needahighdirectivityindexiftheirsonarisrangelimitedby river porpoise(themayrestrictranges).Coastalporpoises dolphins probablyuselong-rangeecholocationcomparedwitha Relative latencies There wasaslightincreasein response latencywithdecreasing Latencies mightalsoreflecttheorientationofsoundentering the Signal-to-noise ratiosmaybelowforfinlessporpoisesbecause With over70speciesinvaryingaquaticniches(Perrinetal., Differences maybeduetonicheseparations.Forone,bottlenose 4, 5).Suchfindingshavebeen establishedin studies. comparisons betweenspeciesandpotentialapplicationsofhearing filter shapesandform–functionstudies)willbetterinform audiograms, temporalresolution,receivedsensitivityparameters, auditory adaptations.Thus,multiplecharacteristics(e.g. differ notonlybaseduponaudiogramsbutalsoinmoresubtle divergent species.Thesedifferences alsosuggestthatspecies may for carewhenapplyinghearingdatafromrepresentativeanimalsto among taxonomicgroups.Thisconsiderationunderscorestheneed indicate thatadditionalauditoryvariationsarelikelytobefound porpoise andthebottlenosedolphinbelugawhalehearingdata consistencies thatcompriseodontoceteauditorysystems. investigations inotherspecieswilladdressthedifferences and amplitudes andincreasedlatencies.Comparativeformfunction locations maybesomewhatlimitedbydecreasedresponse role intheuseofsound.Conversely, soundsreceivedatother amplitudes ofpreferentialsoundpathwaysmayplayanimportant to soundreception.Thedecreasedlatenciesandincreasedresponse et al.,1988),asthesedifferences inlatenciesmayalsoprovideclues perhaps inparttohelpdiscriminatetheseacousticdifferences (Au are robust.Notably, odontocetes haverapidintegrationtimes, multiple animalsanddistinctodontocetespeciessuggeststhatthey have multiplemeanstodirectandshadesoundwithinthehead. al., 1995).Thus,finlessporpoises,andlikelyotherodontocetes, differences ofanaquaticmedium(Mooneyetal.,2012;Moore air), compensatingfortheminimalintra-auraltimeandloudness may beinpartadaptionstosoundspeedwater(~5×fasterthan left (contra-lateral)sideofthehead.Thesephysiologicalmechanism also faster, comparedwiththosetoloweramplitudesoundsonthe physiological responseamplitudesintherighteararehigher, but higher inamplitudeatone(inthiscasetheright)ear. Thus, sound fromoneside,forthisexampletheright,wouldlikelybe localization intwomanners:responseamplitudeandlatency. A imply thatsoundlevelscanaffect responsesforsoundsource often bedifferent atipsilateralandcontralateralears,theseresults to responselatency(Popovetal.,2008).Becausesoundlevelswill are directlytiedtoresponsemagnitude,andthismagnitudeislinked on themats. experiments andtheporpoisewithin thepoolwasgentlyliftedandplaced mats onthetopledgeofatieredpool. Water wasdrainedjustprior tothe obtained outofthewater. Thetestsubject porpoisesrestedontwofoam (Mooney etal.,2011). Allreceivedsensitivityhearingexaminationswere related tothisstudyreflectednormal odontocetehearingcapabilities years priortothisresearch(Popov etal.,2005)andprobehearingtests were collectedfromthefemale. male overthreeconsecutivedays.Therewasthena3 from thenearbyYangtze River. Hearingdatawere firstcollectedfromthe pools withfourotherconspecifics.Poolswerefilledfilteredfreshwater and wasestimatedtobeofasimilarage.Thetwowerehousedincement in length.Thefemale(Ying Ying) weighed41.8 (Abao) wasestimatedtobe15 and 14 Hydrobiology, ChineseAcademyofSciences,Wuhan, China,forthepast6 female, wereoriginallyfromthewild,buthaveresidedatInstitute of et al.,2007;Supin2001).Theanimalsubjects,onemaleand one invasively investigatehearing(reviewedinMooneyetal.,2012;Nachtigall utilized inmarinemammalsasameanstorapidly, passivelyandnon- porpoises usingAEP methodology. TheAEP techniqueisincreasingly Hearing measurementsweremadeinApril2010ontwoYangtze finless MATERIALS ANDMETHODS The basicaudiogramsoftheseanimals weremeasuredinwaterseveral The differences inrelativehearingsensitivitiesbetweenthefinless These differences inlatenciesaresmallbuttheirdescription years, respectively. Atthetimeofexperiments,adultmale The JournalofExperimentalBiology(2014)doi:10.1242/jeb.093773

years old,weighed47.8

kg, was142

day breakbeforedata

kg andwas145 cm inlength, 449 cm

The Journal of Experimental Biology 54 and120 sinusoidally amplitudemodulated(SAM)tonesatcarrierfrequencies of8, broadband clickscenteredat100 used ascontrols.Thresholdsweremeasuredusingfourdifferent stimuli: thresholds oftheanimalacrossitshead.Thebackandflipperpositions were 8).Thefirstsevenlocations wereusedtomaptherelative flipper (Fig. fat pad,overlaying(outwardfrom)theauditorybulla,meatus,backand body. Thesewerethelowermelon,jawtip,throat,jaw, mandibular transducer wasattachedatninespecificlocationsontheanimal’s headand to eliminatereflectiveairgapsbetweenthecupandanimals’ skin. suction cup.Thetransducerwasattachedtotheanimalusingelectrogel transducer (Slangerup,Denmark)implantedinacustom-builtsilicone ‘jawphone’ orsuction-cuptransducer. ThisconsistedofaReson4013 350D attenuatorandprojectedtotheanimalthroughacustom-built at a512 program, laptop,anddataacquisitioncard.Outgoingsignalswereproduced 16 the dataacquisitioncardconvertedanalogsignaltoadigitalrecordat computer. Usingacustom-writtenLabView program(NationalInstruments), USA) andaPCMCIA-6062Edataacquisitioncardimplementedinlaptop BNC breakoutbox(2110, NationalInstrumentsCorporation,Austin,TX, filtered themfrom300to3000 Technologies), whichamplifiedallresponses10,000-foldandbandpass electrodes wereconnectedtoabiologicalamplifier(CP511, Grass peduncle, andagroundelectrodewasplacedontheanimal’s tailfin.The behind theblowhole.Thereferenceelectrodewasplacedondorsal is thenacquiredin50 (Nachtigall etal.,2007).A recordforaparticular frequencyandsoundlevel response whileaveragingdownbackground noisetoarelativelylowlevel sweeps isrelativelystandardforodontocetes becauseitestablishesarobust software andstoredforlaterdataanalyses.Thistotalnumberofstimuli and presentation. These1000responseswereaveragedusingthecustom-written sound levelandacorrespondingresponsewascollectedforeach sound with stimuluspresentation.Stimuliwerepresented1000timesfor each Evoked responserecordingswereof30 at arateof1 Carrier signalswithintheboutweremodulated(tones)orpresented(clicks) 450 RESEARCH ARTICLE facility beforethe experimentusingthesamesounds asinthehearingtests. Suction-cup transducer stimuliwerecalibratedinthe waterattheresearch (non-inverting) electrodewasplacedalongthemidlineofanimal3-4 electrode gel(Signagel,ParkerLaboratories,Fairfield,NJ,USA).Anactive (Grass Technologies, Warwick, RI,USA)wereattachedusingconductive cups (KE1300T, Shin-Etsu,Tokyo, )withembeddedgoldelectrodes Once theanimalwasproperlystationed,threecustom-builtsiliconesuction (protocol numberDRKno.3). Oceanographic Institution’s AnimalCareandUtilizationCommittee Hydrobiology oftheChineseAcademySciencesandWoods Hole Calibrations anddata analysis Stimulus presentation andevoked potentialrecording 9 To measurelocation-basedreceivingsensitivity, thesuction-cup Acoustic stimuliwerecreatedusingthesamecustom-writtenLabView This studywasconductedwiththeapprovalofInstitute kHz samplingrate.Thedatawerestoredonthelaptop. 8

A kHz updaterate.SignalamplitudeswerecontrolledusingaHP kHz. Allstimuliwerepresentedin20

kHz. Theindividualclickstimuliwere20 6

s andthresholdsareobtainedinjust afewminutes. 7 5

Hz. Thisbioamplifierwasconnectedtoa 4

kHz (seeMooneyetal.,2011), and 3 ms durationandbegancoincident 2 1

ms boutsata20 B 9 5 μs induration. 4 3 s − 1 rate. 2 1 8

cm dB levelsofclickSPLsarepresentedin intensities duetotheinherentbrevityofsignals(Au,1993).Hereafter, were measuredusing al., 2010;Nachtigallet2008;2005).SPLsoftheclicks most easilyinitiallyquantifiedbytheirpeak-to-peakvalues(e.g.Mooneyet used forcalculatingthemodulatingamplitudeofthesestimuli,whichare pressure level(SPL)forthatfrequency(dBre.1 peRMS wastakenastheRMSvoltageandusedtocalculatesound equivalent rootmeansquarevoltage(peRMS)bysubtracting15 projector andreceiverwereplaced1 Received measurementsweremadeusingaReson4040transducer. The are presentedindB SPLs startedatanestimated20–30 positions. ThesecondwasthelatencyofAEP responses.Forthresholds, were analyzed.Thefirstwastherelativethresholdofresponseatvarying minimal (FinneranandHouser, 2006). (Cook etal.,2006).Actualhearingdifferences betweenmethodsappear be differences betweenfree-fieldandcontacttransducermeasurements comparisons tohearinginthefree-field,butwithcaveatthattheremay this mannerareinherentlynear-field stimuli.Thus,thismethodprovides the free-andfar-fields, itshouldbeacknowledgedthatstimulipresentedin ( (Tektronix TPS2014,Beaverton,OR,USA)andthepeak-to-peakvoltages the calibration.Thereceivedsignalswereviewedonanoscilloscope path) reducedtheinterferenceofoverlappingstandingwavesandfacilitated levels (i.e.reflectionsweresignificantlyattenuatedrelativetothedirect1 short-duration SAMtonesweeps(i.e.severalms)andrelativelylowsound detectable fortwotothreetrials.Eachthresholdtook5–10 5–10 (Supin andPopov, 1995).Soundlevelswerethendecreasedinstepsof the EFRwasreflectedbyapeakinFFT atthe1 (FFT; 256points)andviewedinthefrequencyspectrum.Themagnitudeof AEP program.A 16 envelope followingresponse(EFR)wasvisibleaspartofthecustom-written of thefinlessporpoise(Popovetal.,2005).With adetectablestimulus,an stimulus onsetand thepointofmaximalchangein neuronalfiring;thus, Yuen etal.,2005),whichareconsidered astandardforsounddetection. similar tobehavioraltechniques(Supin etal.,2001;Szymanski1999; method iswellestablished,rapid and,importantly, producesthresholds calculate thresholds(Finneranet al., 2009;Hall,2007).ThisFFT-based presented totheanimal.ForAEPs, multiplemethodscanbeusedto to predictthethresholdforeach frequencyandtransducerplacement the actualzeropoint.Byestimatingresponselevelitwaspossible low levelofbiologicalelectricalnoisealwayspresentintherecords masks response tothestimulus.Thiszeropointhadbeextrapolatedbecause the extrapolated tozero,thehypotheticalpointwheretherewould be no al., 2005).A linearregressionaddressingthedatapointsobtainedwas stimulus intensitywasafunctionoftheSPL ofthestimulus(Nachtigallet frequencies andprojectingtransducerplacements,theFFT peakateach per day. and 5–10thresholdswerecollectedpersession.Two sessionswere collected V p–p In ordertodeterminetheregionsof‘best’ response,twoprimaryvariables Response latencies weremeasuredbyestablishingthe time(ms)between Actual thresholdestimateswerecalculatedoffline. Foreachofthe ) weremeasured.FortheSAMtones,thisV dB untilresponses(EFRsandFFT peaks)werenolongervisually The JournalofExperimentalBiology(2014)doi:10.1242/jeb.093773 peRMS ms portionoftheresponsewasfast-Fouriertransformed flipper. overlaying theauditorybulla;7,meatus;8,back;9, throat; 4,lowerjaw;5,mandibularfatpad;6, by thenumberedcircles.1,lowermelon;2,jawtip;3, front (B)viewpoints. asiaeorientalis Fig. V p–p re. 1 μPa.Whilecalibrationmeasurementswerein

8. Finlessporpoise(Neophocaena as isstandardformeasuringodontoceteclick

dB abovepreviousaudiogramthresholds

m apartat1 p–p Stimulus locationsareindicated re. 1 μPaandSAMtonedB μPa). Thismethodisoften p–p

m depth.Theuseofthe was convertedtopeak- ) fromside(A)and

kHz modulationrate

min tocollect

dB. The

m

The Journal of Experimental Biology dimensions ofanatomicalstructuresdelineatedinthereconstructions. Dissections ofthespecimenswereperformedtoverifypositionand visual inspectionofthesegmentedfieldstocorrectanycontourerrors. each ofthesetissues.Thisauto-segmentationprocedurewasfollowedby Unit readingsconsistentwiththecharacteristicX-rayattenuationvaluesfor mandibular fatbodyandintra-mandibularbasedonHounsfield were completedfortheskull,mandibles,tympanoperioticcomplex,outer were obtainedusingSiemensproprietaryVRT software.Reconstructions widths anda512matrixinbonesofttissuekernels. tones andclicksweremeasuredatalocationduringonesession). the variables(forexample,multiplethresholdsfromoneanimaland was usedbecauseitassumesthereperhapssomerelationshipbetween from whichmeasurementsweretakenwasrandom,therepeatedmeasures measures ANOVA andaTukey’s Threshold differences betweenlocationswereevaluatedwitharepeated analyses wereconductedusingExcel,MatlabandMinitabsoftware. lower stimuluslevels.Datawerepooledacrossfrequenciesandanimals.All were notincludedintheseanalysesastheyalwaysdetectableat each decreasingstimuluslevel.Wave I(usuallyofsmallestamplitude)data u .W .adHsig,M.C. Hastings, and W. W. L. Au, u .W . or,P .B n alsi D.A. Pawloski, and P. W. B. Moore, W. W. L., Au, immediate release. [grant no.31170501], andwethankthemfortheirsupport.DepositedinPMC [grant no.KSCX2-EW-Z-4] andtheNationalNaturalScienceFoundationofChina Award, theKnowledgeInnovationProgramofChineseAcademySciences The workwasfundedbytheOffice ofNavalResearch,aMellonJointInitiatives interpretation ofthefindingsbeingpublished,anddraftingrevisingarticle. revising thearticle.K.W. and D.W. assistedwithexecutionoftheexperiment(s), experiment(s), interpretationofthefindingsbeingpublished,anddrafting T.A.M., S.L.andD.R.K.participatedintheconception,designexecutionof The authorsdeclarenocompetingfinancialinterests. discussions withManoloCastelloteandAudePacini. providing theAEP software. Theinspirationforthisresearchstemsfrommany collection. We alsothank Alexander SupinandPaulNachtigallforconsultation Aquarium,InstituteofHydrobiology, fortheirsupportandassistanceindata The authorswouldliketoexpresstheirgratitudethestaff andstudentsatthe of 120 16. Bothscanswereobtainedinthetransaxialplaneusingaspiralprotocol Zhongnan Hospital,Wuhan University, onaSiemensSomatom Sensation head wasavailableforimaging.Thespecimenswerescannedatthe frozen andweregraduallythawedforscanning.Foronespecimen,onlythe in themonthpriortohearingtestexperiments.Theanimalshadbeen CT scanswereacquiredfromtwofinlessporpoisespecimensthatstranded 0 from maximumstimuluslevel.Thelevelwasconsidered case, timevaluesofwaveII–IV peakswerecomparedwiththeattenuation were pooledbetweenanimalsandcalculatedusingallfrequencies. significant AEP waveintheEFR.Latenciesrelative tostimuluslocations back 20individualwaves(fromstimuli)fromthelast (Mooney etal.,2006;Supin2001).Thiswasconfirmedbycounting These waveswerelikelytheresponsetofirstclickorSAMstimulus AEP waves,whichweredesignatedaswaveI, II,IIIandIV, respectively. latencies weremeasuredasthetimevalueofpositivepeakfirstfour RESEARCH ARTICLE nel .R n ie W. Fite, and J.R. Angell, Author contributions Competing interests Acknowledgements CT measures References Funding

dB and0 13, 775-777. echoes innoisebyan echolocatingdolphin. York, NY: Springer. Attenuation-based segmentationsandthree-dimensionalreconstructions Latencies relativetostimulusamplitudewerecomparedseparately. Inthis kV and118 effective mAS.Imageswereformattedat1 ms delay. Theincreaseinresponselatencywasthenplottedfor (1901). Themonaurallocalizationofsound. (2009). post hoc Principles ofMarineBioacoustics J. Acoust.Soc.Am. test. Whiletheorderoflocations (1988). Detectionof complex 83, 662-668. Psychol. Rev.

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