a short note on the terminal nerve in callorhinchus milii...

A short note on the terminal nerve in Callorhinchus milii (Callorhinchidae, Holocephali, Chondrichthyes)

by

Martin Licht† (1) & Peter Bartsch* (2)

Cybium 2015, 39(4): 317-320.

(1) Tannenweg6,D-32105BadSalzuflen,Germany.(2)MuseumfürNaturkundeBerlin,Invalidenstr.43,D-10115Berlin,Germany.* Correspondingauthor[peter.bartsch@mfn-berlin.de]

Ichthyological note – Note ichtyologique©

SFI

Received: 1st Sep. 2015Accepted: 29 Sep. 2015Editor: R. Causse

Résumé.–ÀproposdunerfterminaldeCallorhinchus milii (cal-lorhinchidae,Holocephali,Chondrichthyes)

Lenerfterminalaétédécritrécemmentendétailchezlesholocéphales.Cependant,cetteétudeportaituniquementsurdeuxespèces(Hydrolagus colliei et Chimaera monstrosa)deChimeri-dae,lafamillelaplusdérivéeparmilesholocéphalesactuels.Nouscomplétonsicileprécédenttravailendécrivant,pourlapremièrefois,lenerfterminalchezlachimèreéléphant(Callorhinchus milii) danssondernierstadeontogénétique,àpartirdecoupessériéesd’unspécimen.LetrajetdunerfterminaldeC. miliiressembleàceluidesautresholocéphales.Nousproposonsquelapositionplu-tôtventraleetmédianesoitlaconditiondebasepourlesholocépha-lesactuelsetpeut-êtrepourlesgnathostomes.

Keywords.–Chimaeriformes–Callorhinchidae-Callorhinchus milii-Neuroanatomy-Olfactoryepithelium-Nervus terminalis.

Extantholocephalanfishareanancientgroupamongrecentgnathostomesandareconsideredsister-grouptoElasmobranchii(sharks,batoids,andrays)(e.g.Zangerl,1981;Maisey,1986).Thankstotheirexceptionalmorphology,auniquecombinationofprimitivegnathostomeandspectacularderivedcharacters,theyhavebeenstudiedforalongtimeandmuchworkhasconcentratedontheircranium(e.g.Cole,1896;Dean,1906;Allis,1917;Keste-ven,1933;DeBeerandMoy-Thomas,1935;Stahl,1967;Didier,1995).Informationofmorphologyandbiologycomesmainlyfromtwospecies,Hydrolagus colliei(Lay&Bennett,1839)andCal-lorhinchus miliiBorydeSt.Vincent,1823.ParticularinterestonthemorphologyandgeneticsofC. milii arose during the last years, whichisnotonlybecausethisspeciesismoreeasilyaccessiblebutalsobecauseC. milii belongstoCallorhinchidae,thebasalsisterfamilyoftheothertwoextantfamiliesChimaeridaeandRhinochi-maeridae(e.g.Didier,1995;Licht et al.,2012;Pradelet al.2013;Jerveet al.,2014;Ryllet al.,2014;Venkateshet al.,2014).

Someinvestigationshavebeenperformedonthecranialnervesofholocephalans(e.g.Cole,1896;Liu,2001)andthecranialnervesofholocephalanfishstillconcealunknowninformationaboutgna-thostomeevolution(Pradelet al.2013).Thoughthecranialnerveshavebeenoftenexaminedunderdifferentaspects,thenervus ter-minaliswasdescribedforholocephalansonlyrecently,in2012byLichtandBartsch,therebycorrectingadoubtfulstatementthat

thisnerveisnotpresentinHolocephali(Liu,2001).Buttheter-minalnervehasneverbeendescribedforCallorhinchusandevenSchauinsland(1903)misseditinhisotherwiseveryinformative3-DreconstructionoftheheadandbrainofC. milii.

Thatthisnerveshouldnotbepresentinallholocephalanfami-lieswasparticularlysurprising,consideringthatitispresentandtosomeextentprominentintheElasmobranchii(e.g.Locy,1899,1905;NorrisandHughes,1920;Demskiet al.,1987).Neverthe-less,LichtandBartsch(2012)hadonlyaccesstotwospecies(Hydrolagus colliei and Chimaera monstrosaLinnaeus,1758),whichjustrepresentthemostderivedfamily(Chimaeridae)ofextantholocephalansandwerenotabletodemonstratethepres-enceoftheterminalnerveinCallorhinchidae.However,itwouldbeparticularlyinterestingifthepatternofthenervus terminalis in Callorhinchidae,wassimilartothatinChimaeridae(i.e.anentirelyventro-mesialpositionrelativetothebulbus and tractus olfacto-riusandelongateforebrainhemispheres),orshowedamoredorsalcourseasinelasmobranchs(e.g.Locy,1899,1905).Here,wenowsupplementourstudyanddemonstrateaganglionatedterminalnerve,well-separatedfromthefibrebundlesoftheolfactorynerveandtractintheholocephalanCallorhinchus milii.

MAteRiAl And MetHods

Thisstudyisbasedonaseriesofhistologicaltransversesec-tionsofapre-hatchlingofCallorhinchus milii(NMNZNo.1670),storedattheMuseumfürNaturkunde(Berlin).ThespecimenwascaughtinApril1955inDay’sBay(Wellington,NewZealand):totallength=72mm;headlength=19mm.TheheadwasembeddedinParaffin,andseriallycutinto10µm-thicksections,stainedinHeidenhain’sAZAN,examinedinaLeicaDMEmicroscope,andphotographedwithaZeissAxioCamMRc5.

Results

Thoughhistologicalpreservationofthespecimenisfarfromideal,itwaseasytofollowthecourseoftheterminalnervealongthetelencephalichemispheres.Thenervus terminalis has its anteri-ororiginattheolfactoryepitheliumandnasalcapsuleintheregionoftheanteriormostfibresofthenervus olfactorius.Thefollowing

† Note:MartinLicht,thefirstauthorofthisstudy,friend,colleagueandagiftedandenthusiasticyoungerresearcherinichthyologyandpaleontology,passedawayonFriday,September11,2015allofasudden.Sadly,hedidneitherseethisstudypublished,northeprintsofhisrecentworkonTetragonurus.Ourthoughtsarewithhim,andhisfamilyheleavesbehind.

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318 Cybium 2015, 39(4)

Figure1.-Histologicaltransversesectionsthroughnasalsacandforebrainofapre-hatchlingofCallorhinchus milii (NMNZNo1670),respectively.A:Anteriorganglionofthenervus terminalis,closetotheolfactoryepitheliumandnasalcapsuleintheregionofthefibresofthenervus olfactorius.B:Largermagnificationofsquaredregioninfigure1A.C:Relativepositionoftheterminalnerveclosetothenasalseptumonitscourseposterioralongthebulbus and tractus olfactorius.d:Largermagnificationofsquaredregioninfigure1C.e:Posteriorganglionofthenervus terminalisatthemedioventralpartofthetelencephaloninC. milii. F:Largermagnificationofsquaredregioninfigure1E.Abbreviations:(BO)bulbus olfactorius,(BV)bloodvessel,(GNTa)anteriorganglionofn. terminalis,(GNTp)posteriorganglionofn. terminalis,(NO)n. olfactorius,(NT)n. terminalis,(OE)olfactoryepithelium,(T)telencephalon,(TH)telencephalichemisphere.

Licht & Bartsch Nervusterminalis in Callorhinchusmilii

Cybium 2015, 39(4) 319

courseoftheterminalnerveinC. miliiisalsoconsistentwiththecourseinChimaera and Hydrolagus.LichtandBartsch(2012)describedthecourseasfollows:itsanteriorganglionliesontheinnerventralsideofthefirstcranialnerveclosetothenasalseptumandsendsafferentbranchestothenervus olfactoriusand/orclosetotheolfactoryepithelium(Fig.1A,B).Therelativepositionofthenervedoesnotchange,followingitscoursealongtheolfactorynerveposteriorlytowardsthebulbus and tractus olfactorius(Fig.1C,D).Asecondganglionissituatedatthemedioventralpartofthetelencephalichemisphere(Fig.1E,F).Finally,thenervus termi-nalisentersthetelencephalonmediodorsally(Fig.1E).Duringitscourse,theterminalnerveiscloselyassociatedwithbloodvessels,inparticularadistinctanteriorbranchoftheinnercarotidartery(Fig.1D,F).

disCussion

Itisgenerallyknownthattheterminalnerveispresentinmost,ifnotall,vertebrates(e.g.DemskiandSchwanzel-Fukuda,1987)andalsoinholocephalanfish(LichtandBartsch,2012).ButithasnotbeendetectedinthemostbasalextantfamilyCallorhinchidae.LichtandBartsch(2012)statedthequestionthatitwouldbeinter-estingwhetherthecourseoftheterminalnerveintheCallorhinchi-daeresemblesmorethoseoftherelatedelasmobranchs,orifitislikeinthemorederivedextantholocephalansH. colliei and C. monstrosa.Inelasmobranchfish,theterminalnerverestsontherostrodorsalsurfaceoftheolfactorybulbandrunsdorsalormedialto the bulbus olfactorius and tractus olfactorius(e.g.Locy,1905;Demski,1987),whileinC. miliitheterminalnervehasitsentirecourseventralandmedialtothebulbus and tractus olfactorius as in otherholocephalans(e.g.LichtandBartsch,2012)(Fig.2).Becauseofthesamepatternofthenervus terminalisinbothextantholo-cephalanfamilies,weconcludethatthismoreventralandmediancourseisbasicforextantHolocephali.However,theterminalnerveisstillundescribedforRhinochimaeridae,andalsoforfossilholo-cephalanswithadifferentcranialanatomy.Possibly,thecourseoftheterminalnervecoincideswiththespecialcranialmorphologyandfarventralpositionofnasalsacandcapsule,andtheelasmo-branchconditionisthemorebasalonealsofortheholocephalanclade.InDipnoiadultsandlarvae,asshowninPinkus(1895)andBartsch(1993),thecourseismoresimilartothatinelasmobranchfish.Butweassumethattheventralandmedianposition,aswellasthecoursetotheolfactorytractandbulb,isaplesiomorphicchar-

acterforgnathostomes,asalsoshowninActinopterygians(Allis,1897:plateXXXVIII,fig.64;Brookover,1910)orinextinctpla-coderms(e.g.Long,1988:fig.12;Dupretet al.,2014:Extendeddatafigs3e,f).Notsurprisingly,thisdelicatenerveisonlyknowninafewofthosefossiltaxainwhichanossifiedandwell-preservedendoskeletonoftheneurocraniumexactlymouldsnervebranches,vesselsandnasalcapsules.Nevertheless,thepotentialphyloge-neticanddevelopmentalimplicationsofitspresenceandcourseinholocephalansareyettobedetermined.But,ourfindingsfurtherconfirmitsgeneralpresenceinHolocephaliandthatthepatternofthenervus terminalisinextantHolocephalidiffersfromthatoftheirnextextantrelatives,theElasmobranchii.Certainly,thereissomecorrelationwiththetypeofdevelopmentandinvaginationofthetelencephalichemispheresinthesegroups.Theresultsforholocephalanfishmaythustriggernewquestionsandinterestinthecomparativeanatomicalstudyofthisstructure,itsdevelopmentandsignificanceinvertebrateevolution.

Acknowledgments.–WesincerelythanktheNationalMuseumofNewZealand(NMNZ,nowMuseumofNewZealandTePapaTongarewa),Wellington,theformer“DominionMuseumWellington”andHansBjer-ring(Stockholm),forthedonationandloanofholocephalanindividuals,respectively.Forlaboratoryhelpwiththehistologicaltransversesections,wethankJuttaZeller(Berlin)andPeterGiere(Berlin)foraccesstothemicroscopeequipmentandcamera. WearegreatlyindebtedtoIljaKogan(Freiberg)forthetranslationsandhelpwiththeFrenchlanguage.

ReFeRenCes

ALLISE.P.,1897.-ThecranialmusclesandcranialandfirstspinalnervesinAmia calva.J. Morphol.,12:487-770.

ALLISE.P.,Jr.,1917.-Theprechordalportionofthechondrocra-niumofChimaera colliei.Proc. Zool. Soc. Lond.,1917:105-143.

BARTSCHP.,1993.-DevelopmentofthesnoutoftheAustralianlungfishNeoceratodus forsteri(Krefft,1870),withspecialref-erencetocranialnerves.Acta Zool.-Stockholm,74:15-29.

BROOKOVERC.,1910.-Theolfactorynerve,thenervus termi-nalisandthepre-opticsympatheticsysteminAmia calva,L.J. Comp. Neurol.,20(2):49-118.

COLEF.J.,1896.-OnthecranialnervesofChimaera monstrosa (Linn.1754);withadiscussionofthelaterallinesystem,andofthemorphologyoftheChordatympani.Trans. R. Soc. Edinb.,38:631-680.

Figure2.-Sketchoftheforebrainandcourseoftheterminalnerveofthepre-hatchlingofCallorhinchus miliiinsagittalsectionshow-ingthelefthemisphere.Abbreviations:(BO)bulbus olfactorius,(CA)anteriorcom-missure,(Ep)epiphysis,(FV)ventricularforamen,(NT)nervus terminalis, (tc) tela choroidea(ofthemedianforebrainventri-cle),(TrO)tractus opticus.

Nervusterminalis in Callorhinchusmilii Licht & Bartsch

320 Cybium 2015, 39(4)

DEBEERG.R.&MOY-THOMASJ.A.,1935.-OntheskullofHolocephali.Phil. Trans. B,224:287-312.

DEANB.,1906.-ChimaeroidFishesandtheirDevelopment.194p.CarnegieInstitutionofWashingtonPublication,32.

DEMSKIL.S.,1987.-Phylogenyofluteinizinghormone-releasingsystemsinprotochordatesandvertebrates.In:TheTerminalNerve(Nervus terminalis)Structure,Function,andEvolution(DemskiL.S.&Schwanzel-FukudaM.,eds.),pp.1-14.AnnalsNewYorkAcademyofScience,519.

DEMSKIL.S.&SCHWANZEL-FUKUDAM.,1987.-Introduc-tion.In:TheTerminalNerve(Nervus terminalis)Structure,Function,andEvolution(DemskiL.S.&Schwanzel-FukudaM.,eds.),pp.ix-xi.AnnalsNewYorkAcademyofScience,519.

DEMSKIL.S.,FIELDSR.D.,BULLOCKT.H.,SCHREIBMANM.P.&MARGOLIS-NUNNOH.,1987.-Theterminalnerveofsharksandrays.Electronmicroscopic,immunocytochemi-cal,andelectrophysiologicalstudies.In:TheTerminalNerve(Nervus terminalis)Structure,Function,andEvolution(Dem-skiL.S.&Schwanzel-FukudaM.,eds.),pp.15-32.AnnalsNewYorkAcademyofScience,519.

DIDIERD.A.,1995.-Phylogeneticsystematicsofextantchimae-roidfishes(Holocephali,Chimaeroidei).Am. Mus. Novitates, 3119:1-86.

DUPRETV.,SANCHEZS.,GOUJETD.,TAFFOREAUP.&AHLBERGP.E.,2014.-Aprimitiveplacodermshedslightontheoriginofthejawedvertebrateface.Nature,507:500-503.

JERVEA.,JOHANSONZ.,AHLBERGP.&BOISVERTC.,2014.-EmbryonicdevelopmentoffinspinesinCallorhinchus milii (Holocephali);implicationsforchondrichthyanfinspineevolu-tion.Evol. Dev.,16(6):339-53.

KESTEVENH.L.,1933.-TheanatomyoftheheadofCallorhyn-chus antarticus.J. Anat.,67:449-454.

LICHTM.&BARTSCHP.,2012.-Noteontheterminalnerveinchimaeroidfishes(Holocephali;Chimaeridae).Cybium,36(4):539-543.

LICHTM.,SCHMUECKERK.,HUELSKENT.,HANELR.,BARTSCHP.&PAECKERTM.,2012.-Contributiontothemolecularphylogeneticanalysisofextantholocephalanfishes(Holocephali,Chimaeriformes).Org. Divers. Evol.,12(4):421-432.

LIUZ.,2001.-Phylogeneticrelationshipsofthelivingchimaeroidfishesbasedoncharactersofthebrainandcranialnerves.New Mex. J. Sci.,41:1-24.

LOCYW.A.,1899.-Newfactsregardingthedevelopmentoftheolfactorynerve.Anat. Anz.,16(12):273-290.

LOCYW.A.,1905.-Onanewlyrecognizednerveconnectedwiththeforebrainofse1achians.Anat. Anz.,26:33-63,111-123.

LONGJ.,1988.-Anewcamuropiscidarthrodire(Pisces:Placod-ermi)fromGogo,WesternAustralia.Zool. J. Linn. Soc.,94:233-258.

MAISEYJ.G.,1986.-Headsandtails:acordatephylogeny.Cla-distics,2:201-256.

NORRISH.W.&HUGHESS.P.,1920.-Thecranial,occipitalandanteriorspinalnervesofthedogfish,Squalus acanthias.J. Comp. Neurol.,31:293-402.

PINKUSF.,1895.-DieHirnnervendesProtopterus annectens.Morphol. Arbeit.,4:275-346.

PRADELA.,DIDIERD.,CASANED.,TAFFOREAUP.&MAI-SEYJ.G.,2013.-Holocephalanembryoprovidesnewinfor-mationontheevolutionoftheglossopharyngealnerve,metoticfissureandparachordalplateinGnathostomes.PLoS ONE, 8(6):e66988.

RYLLB.,SANCHEZS.,HAITINAT.,TAFFOREAUP.&AHL-BERGP.E.,2014.-ThegenomeofCallorhinchusandthefos-silrecord:anewperspectiveonSCPPgeneevolutioningnath-ostomes.Evol. Dev.,16:123-124.

SCHAUINSLANDH.H.,1903.-BeiträgezurEntwicklungsges-chichteundAnatomiederWirbelthiere,I.Sphenodon, Callo-rhynchus, Chamaeleo.Zoologica,39:1-98.

STAHLB.J.,1967.-MorphologyandrelationshipsoftheHolo-cephaliwithspecialreferencetothevenoussystem.Bull. Mus. Comp. Zool.,135:141-213.

VENKATESHB.,LEEA.P.,RAVIV.et al.[33authors],2014.-Elephantsharkgenomeprovidesuniqueinsightsintognathos-tomeevolution.Nature,505:174-179.

ZANGERLR.,1981.-HandbookofPaleoichthyology,vol.3AChondrichthyesI.PalaeozoicElasmobranchii.113p.München:VerlagDr.FriedrichPfeil.