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First record of cestode cysts of Phyllobothrium delphini (Phyllobothriidae ) from dusky dolphins (Lagenorhynchus obscurus ) off Argentine coast

Primer registro de quistes de céstodos en delfines oscuros (Lagenorhynchus obscurus ) en la costa de Argentina

RocíoLoizagadeCastro,1DamiánG.Vales,1MarianaDegrati,1NéstorGarcía,1MercedesFernández,2andEnriqueA.Crespo1

1Centro Nacional Patagónico (CENPAT-CONICET), Bvd. Brown 2915, CPU9120ACV Puerto Madryn, Chubut, Argentina, CPU9120ACV Puerto Madryn, Chubut, Argentina

2Unidad de Zoología Marina, Instituto Cavanilles de Biodiversidad y Biología Evolutiva, Universitat de València, P.O. Box 22085, E-46071 Valencia, Spain

e-mail: rocio@cenpat-conicet.gob.ar

LoizagadeCastroR.,D.G.Vales,M.Degrati,N.García,M.FernándezandE.A.Crespo.2014.FirstrecordofcestodecystsofPhyllobothrium delphini (Phyllobo-thriidae)fromtheduskydolphins(Lagenorhynchus obscurus)offArgentinecoast.Hidrobiológica24(3):307-310.

ABSTRACTTheduskydolphin,Lagenorhynchus obscurus,isacoastalsmallcetaceanwidespreadinthesouthernhemisphere.Here,wepres-ent the first record of cestode parasites present in the blubberofduskydolphinoffArgentinecoast.Thehostexamined,corre-spondedtoa15yearsoldmaturefemaleandmeasured171cmlong.CystsofhelminthsbelongingtoCestodawerefoundonthesubcutaneousblubberoftheventralsurface;parasiteswerede-terminedasPhyllobothrium delphini (Phyllobothriidae).Probablythepresenceofthisparasiteisrelatedtodeeppelagicforaginghabitats where the most important prey are the squids. In thestomachcontents25TypeIIlarvaeofAnisakiswerefoundand12cephalopodbeaks,belongingtoargentineshortfinsquid,Illex ar-gentinus.Nematodeswerefoundintheintestines,TypeIIlarvaeofAnisakis,andanotherfromthegenusStenurus(family,Pseu-daliidae).Hereanewrecordofcestodescystsisdescribed,en-richingtheparasite-hostrecordforduskydolphins,enlargingthescarceparasitologicalinformationforcetaceansofArgentina.

Key words:Argentine,cestodes,duskydolphins,Phyllobothrium delphini.

RESUMENEl delfín oscuro, Lagenorhynchus obscurus, es un cetáceopequeñodehábitoscosterosquesedistribuyeampliamenteenelHemisferioSur.Enestetrabajo,sepresentaelprimerregistrode

cestodesparásitospresenteseneltejidoadiposodeldelfínoscu-ro en las costas de Argentina. El hospedero examinado corre-spondióaunahembramaduradeaprox.15añosdeedady171cmdelongitud.SeencontraronquistesdehelmintospertenecientesalaclaseCestoda:Phyllobothrium delphini(Phyllobothriidae),enlagrasasubcutáneadelasuperficieventraldelanimal.Esprob-ablequelapresenciadeesteparásitoserelacioneconloshábi-tatsdealimentaciónpelágicosdeldelfínyconlaprofundidadquehabita, donde las presas más importantes son los cefalópodos.Enelcontenidoestomacalseencontraron25larvasdeAnisakisTipoIIy12picosdecefalópodos,pertenecientesalcalamar,Illex argentinus.Losnemátodosfueronencontradosenlosintestinos,larvasTipoIIdeAnisakis,ydelgéneroStenurus (familia,Pseu-daliidae). En el presente estudio se presenta un nuevo registrodequistesdecestodos,enriqueciendoel registroparásito-hos-pedero para delfines oscuros. Además el trabajo contribuye yamplía la información parasitológica sobre los cetáceos de Ar-gentina.

Palabras claves:Argentina,céstodos,delfínoscuro,Phylloboth-rium delphini.

Duskydolphins(Lagenorhynchus obscurusGray,1828)arepelagicsmallpelagiccetaceanwithprimarydistributionintemperateandcold-temperatewatersintheSouthernHemisphere(Leatherwood&Reeves,1983).InthePatagoniancoastofArgentinathesedusky

Hidrobiológica2014,24(3):307-310 Diciembre2014NOTAS

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dolphinsrepresentthemostcommonspeciesofcetaceans.Sev-eralaspectsofitsbiologyhavebeenpreviouslystudied(Crespoet al., 1997;Danset al., 1997;Degrati et al., 2008;Garaffoet al., 2010;Würsig&Würsig,1980;Degratietal.,2012).Nevertheless,verylittleisknownaboutitsparasitefaunafromSouthwesternAtlanticOcean(Danset al., 1999;Berón-Veraet al.,2008).Theparasitesofmarinemammalscanprovidedataonthepopulationecologyoftheirhosts;especiallycanhelptoidentifyforaginghabitats,dietanddistribution.Parasitismisanecologicalconceptdealingwithonekindof thewiderangeof relationshipsbetweenorganismsandtheirenvironment.Thewayoflookingatparasitismandfind-ingitsplaceamongecologicalinteractionsisbasedontrophicre-lationships(Bushet al., 2001).Theyhavebeensuccessfullyusedasbiologicalstockindicatorsofhostpopulations,undertheas-sumptionthatdifferentparasitecommunitieswouldindicatethatthehostpopulationsareisolated(Perrin&Powers,1980;Dailey&Vogelbein,1991;Berón-Veraet al.,2001;Fernándezet al.,2003).On 24th January 2012, a dead female dusky dolphin was foundstrandedinPlayaBonita(43º21ºS,65º03ºW),ChubutProvince,Ar-gentina.Fortunately,thespecimenwasinfreshconditioninordertoperformparasitologicalanddietstudies.AcompletenecropsyofthespecimenwascarriedoutintheMarineMammalLaborato-ry(LAMAMA-CONICET).DuskydolphinspecimenwasdepositedandisnowavailablefromMarineMammalsScientificCollectionatCentroNacionalPatagónico (CENPAT-CONICET):MM-LO082;parasitespecimenshavebeendepositedinthehelminthcollec-tion of the Natural History Museum, London (NHM; accessionnos.:Phyllobothrium delphini (Bosc,1802), NHMUK2013.7.4.1-3.Stomach, intestines,skull, teeth,postcranialskeleton,andsam-plesofskin,blubber, kidneyand liverof theanimalwere takenand preserved. Age was determined counting the Growth layergroups(GLGs) indentine,assumingannualdeposition(Perrin&Myrick,1980).Agewasdeterminedindependentlybytwoobserv-ersinordertominimizecountingerrors.Theanimalagewas15yearsold.Standardmeasurementsofthespecimenweretakentothenearestcentimeter(Norris,1961)givingatotal lengthof171cm.Theanimalcorrespondedtoamaturefemale;ovariesweremeasured and weighed, the individual had signs of pregnancy(i.e.,enlargeuterinehorns).Danset al. (1997) found theyoung-estsexuallymaturefemaleandtheoldestimmaturefemalewere6and7yrold, respectively,also that thesmallestsexuallyma-ture female and the largest immature female were 161 and 172cmlong.Allstomachchamberswereobservedseparatelytoas-sessparasitedistribution.Parasiteswereisolatedfromfoodcon-tentsandrecoveredthemwitha0.5-mmmeshsieve. Intestineswere divided into 20 sections of equal length and washed thecontentsofeachsectionthrougha0.5-mmmeshsieve.Allpara-sitesfoundwerefixedin70%ethanolandidentifiedaccordingtoconventionalmethods,alsoasampleofparasiteswere fixed in100%ethanolformolecularanalysis.Inthestomachwefound12cephalopodbeaks,belongingtoArgentineshortfinsquid,Illex ar-gentinus (Castellanos,1960);thebeakswereidentifiedbymeans

of the reference collection of the LAMAMA. The prey found inthisstudyisconsistentwithpreviousstudiesthatreportedcom-prehensively theprey items forduskydolphins (KoenAlonsoet al.,1998;Romeroet al.,2012).Thegastrointestinalhelminthcom-munityinthisspecieshasbeenshowedtobedepauperate,withlowspeciesrichness(Danset al.,2010).NematodesfoundintheintestinescorrespondedtotheTypeII larvaeofAnisakis,sensuBerland (1961) and another from the genus Stenurus (family,Pseudaliidae).Inthestomachcontents25TypeIIlarvaeofAnisa-kiswerefound.Also,liverandlungswereexaminedforparasitesbutnonewerefound.HelminthsbelongingtoCestodawerefound:plerocercoids of Phyllobothrium delphini (Bosc, 1802) (Phyllo-bothriidae),fromthesubcutaneousblubberaroundtheabdominalsurface(Fig.1).Larvaeweremeasuredasfollows:cystlength:CL,cystwidth:CW,necklength:NL,neckwidth:NW,scolexlength:SL, scolex width: SW; all parasitological measurements in P. delphiniareexpressed inmm.Basicdescriptivestatisticswerecalculated: mean values on 5 cyst measured for size shown inTable1.Thegreatscatteringofourdatasuggesttheexistenceofhighmorphologicalandsizevariabilityinlarvaldevelopment,asFaillaandLeBas(2003)reportedbefore;alsothereisgreatvaria-tionbecauseofshrinkagedependsonthestateofthecystuponfixation.Howeverthemorphologyofthetetraphyllideanplerocer-coidspresentedhereagreeswellwiththeavailabledescriptionsofP. delphini(seeformoredetailAgustíet al.,2005).InArgentina,cestodescystshavenotbeenreportedforduskydolphinsbefore.However,cystsofcestodeshavebeenreportedinNewZealandduskydolphins(presumablyPhyllobothrium spp.)(Cipriano,1992)andduskydolphinsfromPeru(P. delphini)(VanWaerebeek,1992;VanWaerebeeket al.,1993).Bothofthemarepelagicforagers,theformerrelyingmainlyonmyctophidfishandthe latterprey-inguponanchoveta(VanWaerebeek,1992).InArgentinewaters,cysts of cestodes were recorded in several pelagic and deepfeeder cetaceans such as stripped dolphin (Stenella coeruleo-

Table 1. Mean values (mm) of the cyst of Phyllobothrium delphi-ni (Bosc, 1802), from the subcutaneous blubber of coastal duskydolphin(Lagenorhynchus obscurus)offArgentina.CL:cystlength,CW:cystwidth,NL:necklength,NW:neckwidth,SLandSW:sco-lexlengthandwidthrespectively.

CL CW NL NW SL SW

Mean 6.70 5.25 3.74 1.61 1.47 1.61

Median 6 5.25 3.64 1.56 1.63 1.69

Standarddeviation 1.60 0.98 0.66 0.50 0.54 0.35

Variance 2.56 0.96 0.43 0.25 0.29 0.12

Minimum 4.88 3.88 3.08 0.96 0.77 1.08

Maximum 8.63 6.5 4.75 2.31 2.15 2

N 5 5 5 5 5 5

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alba(Mellen,1833);LoizagadeCastroet al.,2011),spermwhales(Physeter macrocephalusLinnaeus,1758),Gray´sbeakedwhales(Mesoplodon grayi voonHaast,1876),Risso´sdolphins(Grampus griseus, (Cuvier,1812))andlong-finnedpilotwhales(Globicephala melas, Trail,1809),wherethemostimportantpreyinthisenviron-mentarethesquids,Kondakovia longimana Filippova,1972, Me-sonychotheutis hamiltoni Robson,1925andMegalochranchia sp.(Berón-Veraet al.,2008).Theabsenceofrecordingthisparasite,sofar,toduskydolphinsoffArgentinecoastwasdiscussedinac-cordancewithafeedingstrategybasedoninshorepreys(Danset al.,2010).Althoughweexamineasingleindividual,theoccur-renceofP. delphini induskydolphinsmaysuggesttheexploita-tionofmorepelagicgrounds. Inthesescenario,duskydolphinscouldprobablybeexploitingdifferentecologicalsystemsaspartofindividualforagingstrategiesormayindicatetheexistenceofduskydolphins’ecotypes(i.e.,inshoreandoffshore),inArgentinewaters.Analternativehypothesisthatwecannotdiscardisthatthehostexaminedinthepresentworkisamigrantindividualfromanotherstockpopulation.Thereisevidenceofmigrationamongstocks(Cassenset al.,2005).Additionaldataonthehost’shabitatandtrophicecologyandparasitefaunasareneededtoenhancetheknowledgeabouttheforagingareasorecotypesofduskydol-phinsinSouthwesternAtlanticOcean,aspotentiallyindicatedbycestodesparasites.Thisstudyisthefirstrecordforcestodesinacoastalcetaceanandenlargestheparasitologicalinformationwhichisscarce,particularlyforcetaceansofArgentina.

AKNOWLEDGEMENTS

TheauthorsareindebtedtoCentroNacionalPatagónico(Nation-al Research Council of Argentina) especially the Marine Mam-malLaboratoryforlogisticandinstitutionalsupport.Collectionofsamples was approved by Dirección de Fauna y Flora SilvestredelaProvinciadelChubut(ResearchpermitNo009-STyAP/12.-).ThanksareduetograntCGL2009-07465(MinisteriodeEconomíayCompetitividad,Spain).FundswerereceivedfromMohamedbinZayedSpeciesConservationFund.AlsoweliketothanktoPhDRossBarnettwhokindlyreviewedthemanuscript.Atthetimethismanuscriptwaswritten,R.L.C.,D.G.V.andM.D.weresupportedby a Fellowships from National Research Council of Argentina(CONICET).

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Recibido:19deoctubrede2012.

Aceptado:10dediciembrede2013.