ABriefDescriptionoftheSkullof

Spheniscusmegellanicus,theMegellanicpenguinBy

MatthewBorthsDepartmentofAnatomicalSciences

forHBA550:VertebrateEvolution

2

Introduction

TheMegellanicpenguin(Spheniscusmegellanicus)isfoundonthe

SouthAtlanticcoastofSouthAmericanearTierradelFuegoand

onthePacificcoastinthevicinityoftheFalklandIslands.Inthe

winterseasontheywillmigratenorthtothecoastsofBrazilor

Peru,followingthetemperateweathertheyprefer.

Megellanicpanguinsaremedium‐sizedforpenguins,averaging

70cminlengthandweighingbetween3.8kgand6.5kg.Likeall

penguins,theyhaverelativelyshortnecks,shortwedgedtailsandrigidwingssupportedby

fusedcarpelsthatactashydrofoilsratherthanairfoils.Thefusedwristpreventspenguins

fromfoldingtheirforelimbsasmostotherbirdsdo,buttheadditionalrigiditymakesthe

wingamoreeffectivepaddleformovingthroughthewater.Theyarecountershadedwith

whitestomachsandblackbacks,likelyservingthedualpurposeofcamouflagingthe

penguinfromitspredatorsandpreyasitdivesthroughthewaterwithothergroup

membersinpursuitofsquid,smallfish,andcrustaceans.TheMegellanicpenguin,likeall

speciesinthegenusSpheniscus,hasadistinctivewhitebandrunningfrombehindtheeye,

aroundthemandible,andacrosstheneck.Asecondwhitebandloopsaroundthestomach

andthorax(Wong2001).Thefeathersthatcreatethisdistinctivepatternarewater‐proof

andinsulatetheanimalinthecooldepthsoftheocean(Triche2005).

OtherextantspeciesinthegenusSpheniscus(meaning

“wedge‐shaped)includeother“bandedpenguins”suchasS.

humboldti(TheHumboldtPenguin,nativetoPeruandChile),

S.mendiculus(TheGalapagosPenguin),andS.demersus(The

African,orJackassPenguin).ThefirstspeciesofSpheniscus,S.

muizoni,occursinthelatestmiddle/earliestlateMiocene

(11‐13Ma)ofPeru(Göhlich,2007),suggestingaSouth

Americanoriginforthegenus.S.muizoniisalsotheoldest

occurrenceofcrownpenguins(KsepkaandClarke2010).

Fromtheanim

alfiles.com

http://www.theanimalfiles.com/birds/penguins/magellanic_penguin.html

3

ThemonophylyofSphenisciformes(penguins)iswell‐supportedbymolecularand

morphologicalevidence,butthesistergrouptoSphenisciformesremainscontroversial

witharecentanalysis(Livezey&Zusi,2007)recoveringGaviiformes(loons)and

Podicipediformes(grebes)assistergroupstoSphenisciformes,thoughtheauthorsnote

theremaybeconvergencedrivingthisplacementasallthreegroupsarecharacterizedby

aquaticadaptations.Molecularandfossilevidencesuggestspenguinsdivergedfromtheir

lastcommonancestorwithloonsorgrebesintheearliestPaleoceneortheLateCretaceous,

makingasatisfactorysisterrelationshipdifficulttorecover.Forfurtherdetailonthe

phylogenyofSphenisciformes,refertoAppendix1.

GeneralDescriptionoftheAvianSkull

Note:Forgreaterdetailonthediversityandosteologicalrelationshipsbetweenbonesoftheaviancranium,refertoZusi,1993.AnatomicalnomenclatureinthisdiscussionandinthefigurescomesfromZusi,1993,andBertellietal.,2010.TheAvianskullisahighlyderivedstructureconsistingofatightlysuturedneurocranium

surroundingarelativelylargebrainandlargeorbitsandamobilesplanchnocranium

formingthejaws.Theneurocraniumiscomposedoffrontal,parietal,occipital,squamosal,

lacrimal,pleurosphenoid,parasphenoid,ootic,andethmoidossificationregions.These

separateportionsoftheskullareusuallyonlyvisibleinjuveniles.Thecoelurosaur

ancestorsofbirdshadlessfirmlysuturedneurocraniaandpossessedseveralcranialbones

thathavebeenlostinthecourseofavianevolutionwhicharehighlightedintheadapted

figurebelowfromGöhlich&Chiappe2006.Theseincludethepostorbital(po,orange),the

postorbitalprocessofthejugal(red),thesquamosalprocessofthequadratojugal(qj,

yellow),theectopterygoid(notvisible),andcoronoidofthemandible(notshown).

4

Thesplanchnocranium,includingthepremaxilla,maxilla,nasals,jugal,quadratojugal,

palatines,pterygoids,quatrate,articular,splenial,supraangular,angular,articularand

prearticular,ismoremobilethantheneurocranium.Thesplanchnocraniumsupportsthe

keratinizedskinthatformsthebeak.Thewholeupperjawcanbeprotractedandretracted

independentlyoftheneurocranium.Thedegreeofcranialkinesisatthefrontonasalmargin

isvariable,butallbirdspossessomedegreeofmobilityatthequadrate.

NeurocraniumTheanteriorportionoftheneurocraniumisformedbytheroofingfrontalsthatarchover

theorbits.Anteriorly,thefrontalsmeetthemesethmoid,abonethatcontributestothe

anteriorportionoftheorbit.Posteriortothemesethmoidistheinterorbitalseptum,a

commonfeatureinbirdsthatvariesinextentanddensity.Theectethmoidslaterallyfuseto

themesethmoidandformaportionofthelacrimalcanal.Lateraltotheectethmoidsitsthe

lacrimal,abonethatrimsthelacrimalductandcontactsthejugalbar.Thelacrimalhasalso

beencalledthepreorbitalanditformstheposteriorborderoftheantorbitalfenestra.

Theposteriorportionofthefrontalcontactstheparietalsandsquamosals.Nearthis

junction,alateralprocessdescendsbehindtheorbitformingthepostorbitalprocesswhich

canbeformedfromthepleurosphenoid,squamosal,orfrontal.Thepostorbitalligament

continuesfromthetipoftheprocessandinsertsonthemandible,anteriortothe

quadrate/articulararticulation.Thelateralportionoftheparietalandsquamosalcanhave

ashallowfossaandrugosityassociatedwiththeoriginofthetemporalismuscle.The

squamosalalsohasacondylethatarticulateswiththequadrateatitsventral‐mostextent.

Theventralportionoftheneurocraniumisformedbythebasioccipitalattheposterior

marginoftheskull.Thebasiocciptialmayformaportionoftheoccipitalcondyleandin

somebirdssuchastherheaitformstheentireoccipitalcondyle.Theanteriormarginofthe

basiocciptialabutsthebasitemporalplate,astructurederivedfromtheparasphenoid.The

platesupportstheEustachiantubewhichopensattheanterioredgeoftheplatenearthe

rostralportionoftheparasphenoid,oneoftheposteriorsupportsfortheinterorbital

septum.

5

TheEustachiantubeitselfiscloselyassociatedwiththetightlyfusedprootic,opisthotic,

andepioticbonesthatformthemembranouslabyrinth.Theprootichasabeveledarticular

facetwherethequadratearticulatesnearthetympanicmembrane.

Ontheposteriorportionoftheskull,fouroccipitalbonesfusearoundtheforamen

magnum:thesupraocciptialwhichformsthesuperiormarginoftheocciputandcontacts

theparietals,thebasioccipitalwhichthenformstheventralportionoftheskull,andthe

exoccipitalswhichusuallyhousetheforaminaassociatedwithmanyofthecranialnerves

includingthehypoglossal(XII),theaccessory(XI),thevagus(X),andtheglossopharyngeal

(IX).

SplanchnocraniumModernbirdsareedentulous,relyingonspecializedkeratinizedskintocut,crack,and

speartheirfood.Thebeakissupportedinternallybythebonesofthemaxillaandmandible.

Inornithologicalliterature,themaxillaisthetightlysuturedcomplexofbonesassociated

withtheupperjaw.Itiscomposedoftheelongatepremaxillawhichformsmostofthe

dorsalandlateralportionsofthebill,thenasalwhichbeginposteriortotheexternalnares

andformstheproximal‐lateralportionofthebill,andthemaxillarywhichlimitedtothe

ventralmarginofthemaxillaandformsthedistal‐mostportionofthejugalbar.

Thejugalbarisastructurefoundinallbirds.Theanteriorportionofthebarisformedby

themaxillawhichsutureswiththejugal.Thejugalformsthemiddleportionofthebar,then

fuseswiththequadratojugalwhichinturncontactsthemobilequadrate.Thearticulation

ofthequadratetothejugalbarallowsmobilizationoftheupperjawatthecraniofacial

hingewhichisfrequentlydemarcatedbyatransverselineatthejunctureofthenasals,

premaxillaeandthefrontals.Thisiscalledprokinesis.Thelossofthecoelurosaurcranial

bonesmayberelatedtoanincreaseddegreeofprokinesisinthecourseofavianevolution,

freeingthejugalbartotransmitforcefromthequadratetothemaxilla.Somebirdspossesa

secondaryhingeattheintersectionofthepremaxillaandthenasals(rhynchokinesis)that

allowsevengreaterindependentmovementoftheupperjaw.

6

Alongwithajugalprocess,themaxillarieshaveapalatineprocessthatmayfusetocreate

thebonydesmognathoussecondarypalateofsomeneognathousbirdssuchasducksand

geese.However,mostbirdshaveakeratinizedpatentcleftpalate(schizognathouspalate).

Thepalatinescontactthemaxillopalatineprocessesanteriorlyandproceedposteriorly.At

theposterioredgeoftheircontactwiththesuperiorvomers,ventralprocessesprotrude

fromtheelongatepalatines.Attheposteriormarginofthepalatinestheflaredbones

articulatewiththepterygoidswhichvaryinformfromthin,strut‐likestructures(i.e.

Corvuscorax)towide,flaringbonesthatearntheirname(i.e.Spheniscusmegellanicus).The

posteriorportionofthepterygoidformsamobilearticulationwiththequadrate.

Thequadratethenhasanarticulationwiththepalate,thejugalbar,theprootic,andthe

articularbone.Thisfinalarticulationleadstothemandible,arigidstructurecomposedof

sixseparatebones.Posteriortothemandibularjointistheretroarticularprocessand

medialtothejointisoftenamedialprocess.Anteriorandinferiortothearticularisthe

angularbonewhichcontactsthesuperiorprearticular.Superiorandanteriortothe

prearticularisthesupraangular.Thesupraangularisperforatedlaterallybythecaudal

mandibularfenestra.Anteriorlythesupraangularcontactsthedentaryandformsthe

superiorborderoftherostralmandibularfenestra.Themedial,rostralportionofthe

mandibleissupportedbythesplenial,abonenotvisibleinlateralview.Thesplenialis

tightlyfusedtothedentarywhichformstherestofthedistalmandible.Atitstip,the

dentarymakesarigidsymphysiswiththeopposingdentary.

Somebirdspossesstreptognathicmandiblesthatcanflexlaterallyattheintersectionofthe

anteriorsplenialanddentarywiththeposteriorsupraangular,prearticular,andangular

neartherostralmandibularfenestra.Streptognathismisparticularlywelldevelopedin

birdsthatfeedtheirchicksbylettingthejuvenilessticktheirheadsintotheadult’smouth

(i.e.Larus,theseagull),andininsect‐eatingbirdsthatcaptureinsectsbyusingtheirmouths

asakindofnet(i.e.Nyctibius).Thiskindoflateralflexibilityrequiresaless‐rigid

mandibularsymphysisatthedentary.

7

ThePenguinSkullNote:Thespecimendescribedandillustratedhereismissingboththelacrimalboneswhichsitbetweenthefrontalandectethmoidsnearthejunctionofthebeakandneurocranium.Anteriortothelacrimalbonewouldbetheantorbitalfenestra.Thisparticularspecimenisalsomissingthequadratebone.Thisisnotsurprisingasthequadratedoesnotrigidlyfusewithanyportionoftheskull.RefertoAppendix2foraCT‐scannedJackassPenguinskull(Sheniscusdemersus)fromDigimorphthatpreservesboththesebonesandshowstheirarticulationwiththerestofthepenguin’scranium.AlsoonDigimorphisavarietyofotherpenguinskullsandawidediversityofotherbirdskulls.Relativetootherbirds,thepenguin’sskullisrobust(Zusi1993)withlimitedcranial

kinesis.Oneofthemostdistinctiveaspectsofthepenguin’sskullisthelargesupraorbital

fossa.Thisrugosedepressioninthefrontalbonearchesovertheorbit,stoppingshortof

thepostorbitalprocess.Thisfossahousesthesupraorbitalgland,alsocalledthesalt‐gland.

Thisparasympatheticallycontrolledglandisacommonstructureinmarinebirdsthat

ingestsalt‐waterwhenfeedingonsmallpreysuchaskrill.Theextremesaltaccumulation

inthebloodwouldoverwhelmthekidneys,andthesupraorbitalglandactsasanaccessory

kidney,filteringsaltfromthebird’sbloodstream.Theconcentratedsalt‐solutionisthen

drainedfromtheglandthroughductsthatopenintothevestibularconchaandfinally

emptyfromtheexternalnares.Interrestrialbirdsthisglandispresent,butmarinespecies

havesupraorbitalglands10to100timeslargerthantheirterrestrialcounterparts

(Schmidt‐Nielsen,K.1960).Enlargementofthesupraorbitalglandhasoccurredinmultiple

avianlineagesthatcontainspeciesthatexploitmarineresourcesincludingLaridae

(seagulls),Pelecanidae(pelicans)andeventhetoothedCretaceousdivingbirdHesperornis.

Spheniscusisalsonotableforthedeeptemporalfossaethatembaytheparietalbones,

raisingahighsagittalcrestthatmeetsthenuchalcrestataperpendicularangle.The

temporalmusclethatoriginatesatthetallsagittalcrestinsertsonthelong,narrow

retroarticularprocessofthemandible.Spheniscuspenguinscanalsobereadilyrecognized

bytheirdeep,triangularbeaksthatlackaventralcurvesuchasisseeninAptenodytes

forsteri(TheEmperorPenguin).

8

LateralView

Temporal Fossa

ParietalSupraorbital fossa for salt-gland

CN II

CN IV

Frontal

Nares

Jugal

Mesoethmoid

Parotic process

Tympanic cavity

Postorbital ProcessLacrimal duct

Olfactory nerve CN I

Nasal Premaxilla

Quadratojugal Palatine

Interorbital Septum

Squamosal

Maxilla

9

PosteriorView

Postorbital Process

Occipital Condyle Palatine

Posterior portion of the jugal bar

Squamosal

Supraoccipital

Nuchal Crest Temporal fossa

Foramen magnum

Cerebellar prominence

Hypoglossal foramen (CN XII)

Vagus foramen (CNX) Basilar tubercle

Parotic process

Foremen for the external occipital vein

Parietal

Exoccipital

10

DorsalView

NaresPremaxilla

Maxilla

Jugal

Frontal

Supraoccipital

Saggital crest

Nuchal crest

Parietal Supraorbital fossa

Palatines Nasals

Quadratojugal

Postorbital processParotic process

11

VentralView

Premaxilla

Vomer

Palatine

Pterygoid

Basioccipital

Parotic process

Postorbital process

Quadratojugal

Tympanic Cavity

Opening of the auditory tube (Eustachian tube)

Rostral portion of theparasphenoid

Basilar tubercle

Occipital Condyle

Foramen magnum

Maxilla

Open schizognathus palate

12

TheMandible

DentarySupraangularCoronoid Process

Rostral Mandibular FenestraCaudal Mandibular

FenestraRetroarticular Process

AngularArticular

Splenial

DentarySupraangular

Rostral Mandibular Fenestra

Caudal Mandibular FenestraArticularRetroarticular Process

PrearticularAngular

Mandibular symphysis

Lateral View

Medial View

13

ReferencesBertelli,S.,Giannini,N.P.&Ksepka,D.T.2006.RedescriptionandphylogeneticpositionoftheEarlyMiocenepenguinParaptenodytesantarcticusfromPatagonia.AmericanMuseumNovitates3525:1‐36.Göhlich,U.B.&Chiappe,L.M.2006.AnewcarnivorousdinosaurfromtheLateJurassicSolnhofenarchipelago.Nature440:329‐332.Göhlich,U.B.2007.TheoldestfossilrecordoftheextantpenguingenusSpheniscus–anewspeciesfromtheMioceneofPeru.ActaPalaeontologicaPolonica52(2):285‐298.Ksepka,D.T.&Clarke,J.A.2010.Thebasalpenguin(Aves:Sphenisciformes)Perudyptesdevriesiandaphylogeneticevalutionofthepenguinfossilrecord.BulletinoftheAmericanMuseumofNaturalHistory337:77p.Livezy,B.C.&Zusi,R.L.2007.Higher‐orderphylogenyofmodernbirds(Theropoda,Aves:Neorithes)basedoncomparativeanatomyII:Analysisanddiscussion.ZoologicalJournaloftheLinneanSociety.149,1:1‐95.Schmidt‐Nielsen,K.1960.“TheSalt‐SecretingGlandofMarineBirds.”Circulation21:955‐967.Triche,N.2005,“Spheniscusdemersus”(On‐line),DigitalMorphology.AccessedMarch7,2011athttp://digimorph.org/specimens/Spheniscus_demersus/.Wong,C.2001."Spheniscusmagellanicus"(On‐line),AnimalDiversityWeb.AccessedMarch10,2011http://animaldiversity.ummz.umich.edu/site/accounts/information/Spheniscus_magellanicus.html.ZusiRL.1993.Patternsofdiversityintheavianskull.In:Hanken,J.andHall,B.K.,eds.TheSkull,vol.2:PatternsofStructuralandSystematicDiversity.Chicago,IL:UniversityofChicagoPress,391–437.

14

Appendix1.AphylogenyofSphenisciformescalibratedtothestratigraphicrecordfromKsepkaandClarke2010.

15

Appendix2.AleftlateralviewofSpheniscusdemersusmodifiedfromhttp://digimorph.org/specimens/Spheniscus_demersus/.Notethepresenceofthelacrimalboneandquadrate,twoimportantbonesintheavianskullthatarenotpreservedinthespecimendescribedinthisdocument.