Osteology Supports a Stem-Galliform Affinity for the Giant Extinct Flightless Bird Sylviornis

62 Pages·2016·23.07 MB·English

RESEARCHARTICLE
Osteology Supports a Stem-Galliform Affinity
Sylviornis
for the Giant Extinct Flightless Bird
neocaledoniae
(Sylviornithidae, Galloanseres)
TrevorH.Worthy1*,MiyessMitri1,WarrenD.Handley1,MichaelS.Y.Lee2,3,
AthollAnderson4,ChristopheSand5
1 SchoolofBiologicalSciences,FlindersUniversity,Adelaide,SouthAustralia,Australia,2 EarthSciences
Section,SouthAustralianMuseum,NorthTerrace,Adelaide,SouthAustralia,Australia,3 Schoolof
BiologicalSciences,UniversityofAdelaide,SouthAustralia,Australia,4 ArchaeologyandNaturalHistory,
CollegeofAsiaandthePacific,AustralianNationalUniversity,Canberra,AustralianCapitalTerritory,
Australia,5 Institutd’ArchéologiedelaNouvelle-CalédonieetduPacifique,BP11423,98802Nouméa
Cedex,NewCaledonia
*[email protected]
Abstract
OPENACCESS
Citation:WorthyTH,MitriM,HandleyWD,LeeMSY,
ThegiantflightlessbirdSylviornisneocaledoniae(Aves:Sylviornithidae)existedonLa
AndersonA,SandC(2016)OsteologySupportsa
GrandeTerreandIledesPins,NewCaledonia,untilthelateHolocenewhenitwentextinct
Stem-GalliformAffinityfortheGiantExtinctFlightless
BirdSylviornisneocaledoniae(Sylviornithidae, shortlyafterhumanarrivalontheseislands.Thespecieswasgenerallyconsideredtobea
Galloanseres).PLoSONE11(3):e0150871. megapode(Megapodiidae)untilthefamilySylviornithidaewaserectedforitin2005to
doi:10.1371/journal.pone.0150871
reflectmultiplecranialautapomorphies.However,despitethousandsofboneshavingbeen
Editor:AlistairRobertEvans,MonashUniversity, reportedforthisuniqueandenigmatictaxon,thepostcranialanatomyhasremainedlargely
AUSTRALIA
unknown.WerectifythisdeficiencyanddescribethepostcranialskeletonofS.neocaledo-
Received:November5,2015 niaebasedon~600fossilsandusedatafromthisanditscranialanatomytomakeacom-
Accepted:February19,2016 prehensiveassessmentofitsphylogeneticaffinities.Sylviornisneocaledoniaeisfoundto
beastemgalliform,distantfrommegapodiids,andthesistertaxontotheextinctflightless
Published:March30,2016
MegavitiornisaltirostrisfromFiji,whichwetransfertothefamilySylviornithidae.Thesetwo
Copyright:©2016Worthyetal.Thisisanopen
speciesformthesistergrouptoextantcrown-groupgalliforms.Severalotherfossilgalloan-
accessarticledistributedunderthetermsofthe
CreativeCommonsAttributionLicense,whichpermits seresalsoincludedinthephylogeneticanalysisrevealnovelhypothesesoftheirrelation-
unrestricteduse,distribution,andreproductioninany shipsasfollows:Dromornisplanei(Dromornithidae)isrecoveredasastemgalliformrather
medium,providedtheoriginalauthorandsourceare
thanastemanseriform;Presbyornispervetus(Presbyornithidae)isthesistergroupto
credited.
Anseranatidae,nottoAnatidae;Vegavisiaaiisacrownanseriformbutremainsunresolved
DataAvailabilityStatement:Allrelevantdataare
relativetoPresbyornispervetus,AnseranatidaeandAnatidae.Sylviornisneocaledoniae
withinthepaperanditsSupportingInformationfiles.
wasreconstructedhereintobe0.8mtallinarestingstanceandweigh27–34kg.Thepost-
Funding:ThisresearchwasfundedbytheAustralian
cranialanatomyofS.neocaledoniaeshowsnoindicationofthespecialisedadaptationto
ResearchCouncilDECRAprojectDE130101133to
THW.TheNationalGeographicSociety,theService diggingseeninmegapodiids,withforexample,itsungualmorphologydifferinglittlefrom
desMuséesetduPatrimoine(Département thatofchickenGallusgallus.Theseobservationsanditsphylogeneticplacementasstem
Archéologie)andtheAustralianNationalUniversity
galliformsmakesitimprobablethatthisspeciesemployedectothermicincubationorwasa
(ANU,Canberra)providedfinancialandmaterial
mound-builder.Sylviornisneocaledoniaecanthereforebeexcludedastheconstructorof
assistancefortheexpeditionthatcollectedthe
material.Thefundershadnoroleinstudydesign, tumuliinNewCaledonia.
datacollectionandanalysis,decisiontopublish,or
preparationofthemanuscript.
PLOSONE|DOI:10.1371/journal.pone.0150871 March30,2016 1/62
OsteologyandRelationshipsofSylviornis(Aves:Sylviornithidae)
CompetingInterests:Theauthorshavedeclared Introduction
thatnocompetinginterestsexist.
Avianevolutiononislandshasresultedintheevolutionoflargeflightlessformsinmultiple
Abbreviations:AM,AustralianMuseum,Sydney,
groups[1,2],suchastheninespeciesofratitemoa(Dinornithiformes)ofNewZealand[3],
NewSouthWales,Australia;AMNH,American,
giantwaterfowl(Anatidae)includingmoa-nalosinHawaii[4]andgeeseinNewZealand[3],
MuseumofNaturalHistory,NewYork,U.S.A.;
pigeons(Columbidae)intheMascarenes[5,6]andFiji[7],andenigmaticgruiforms(Aptor-
ANWC,AustralianNationalWildlifeCollection,
Canberra,Australia;IANCP,Institutd'Archéologiede nithidae)inNewZealand(e.g.,[8,9]).Galliformshavealsospawnedgiantflightlessformsin
laNouvelle-CalédonieetduPacifique,Nouméa,New thePacific,withthebestknownbeingSylviornisneocaledoniaePoplin,1980fromNew
Caledonia;KU,OrnithologyCollection,Universityof Caledonia.
KansasBiodiversityInstitute,Lawrence,Kansas,U.S.
Sylviornisneocaledoniaewasoriginallydescribedasaratite[10],butitsaffinitiesweresoon
A;LACM,VertebrateZoology,NaturalHistory
consideredtoliewithmegapodegalliforms[11–15].Despitethousandsofbonesbeingknown
MuseumofLosAngelesCounty,LosAngeles,
California,U.S.A.;NHMUK,NaturalHistoryMuseum, [14],itsosteologyisincompletelyknownexceptfortheskull,whichwasdescribedindetailby
London,UnitedKingdom;NMNZ,MuseumofNew Mourer-ChauviréandBalouet[16],whoconvincinglyshowedthatS.neocaledoniaewasagalli-
ZealandTePapaTongarewa,Wellington,New form.However,theyconsideredthesharedfeatureswithmegapodestobesymplesiomorphic
Zealand;NMV,NationalMuseumofVictoria,
andonthebasisofitsmanyautapomorphies,theyestablishedthemonotypicSylviornithidae
Melbourne,Victoria,Australia;QM,Queensland
forS.neocaledoniae.Notablefeaturestheseauthorshighlightedincluded:thebroadflattened
Museum,Brisbane,Queensland,Australia;SAM,
cranium;amassive,dorsoventrallydeep,laterallycompressedrostrumwithalargebonyorna-
SouthAustraliaMuseum,Adelaide,SouthAustralia,
Australia;USNM,UnitedStatesNationalMuseum, ment;mandiblewithanelongatedsymphysis;andazonaflexoriacraniofacialisthatformsa
SmithsonianInstitution,WashingtonD.C.,USA;ant, synovialjoint,hereaftertermedacraniofacialhinge,thattransectsthenasalsearlyinontogeny.
anterior;cmc,carpometacarpus;cor,coracoid;cran However,suchautapomorphiesmightnotprecludethistaxonfrombeingembeddedwithinan
pt,cranialpart;hum,humerus;fem,femur;fib,fibula;
establishedfamilyas,forexample,someratites(e.g.,Casuariussp.)andgalliforms(e.g.Numi-
fur,furcula;juv,juvenile;mand,mandible;pt,part;
didae)havebonyornamentontheirskull,andsomegalliformshavesuchontheirrostrum
rad,radius;scap,scapula;stern,sternum;tib,
tibiotarsus;tmt,tarsometatarsus;L,left;R,right;DW, (e.g.some,butnotall,cracids).Billshapeandsizecanberemarkablyvariablewithingroups,as
maximumdistalwidth;PW,maximumproximalwidth; wellshownwithinAnatidae,forexample,withextremesseeninlargerflightlesstaxa,suchas
SW,mid-shaftwidth;TL,totallength. thelargeflightlessHawaiianmoa-nalos[4].Moreover,reductioninpectoralgirdlecomplexity
associatedwithflightlessnessoveralongtimecouldeasilyhaveledtothelossoffeatures.One
suchfeaturelikelytobesoimpactedisthecup-likecotylascapularisobservedinstemgalli-
forms[17]butabsentinthecrowngroup:itslossinS.neocaledoniaemaynotnecessarily
reflectthederivedgalliformstate,contraMourer-ChauviréandBalouet[16].Alsothepost-cra-
nialskeletonremainsincompletelydescribed,asPoplinandMourer-Chauviré[12]mainlyhad
fragmentarymaterialavailable,sopresacralvertebraeotherthantheatlas,axisandnotarium,
arevirtuallyunknown,thehumeruswaspoorlydescribed,andmajorfeaturesofthelegbones
includingtheiractualsizeandproportionswereunknown.Theseobservationswereaug-
mentedbyBalouetwithasimpleskeletalreconstructionandsomesketchydetails,including
thatthepelvishadequallydevelopedtransverseprocessesandalargeilioischiadicforamen,the
ribslackeduncinateprocesses,theclavicleswereunfusedsotherewasnofurcula,althoughthe
clavicleandcoracoidwerefused,andthattherewerealargenumberofsynsacralandcaudal
vertebrae[14].
Knowledgeofthebiologyofthisbirdalsoremainsverylimited.Mourer-Chauviréand
Balouet[16]comparedtheskullofS.neocaledoniaetothegiantgastornithidsanddromor-
nithids,thedodoandsolitairepigeonsoftheMascarenes,andthemoa-nalosofHawaii,finding
significantdifferencesbetweenitandtheselargeherbivores.Whilenotingthepossibilitythatit
fedoninvertebratestheyleftopenthequestionoftheprecisedietofS.neocaledoniae,other
thanthatitwasveryspecialised.Similarly,nothingisknownaboutitsbreedingbiology.Buton
thebasisofthecontemporaryunderstandingthatS.neocaledoniaewasamegapode[11–13],
severalauthorsassumedittobeamoundbuilderandthuspotentiallyresponsibleforcon-
structingtheenigmaticlargemoundsortumulionLaGrandeTerreandIledesPins(e.g.,
[18–20]).Megapodesaretheonlybirdsknowntoemployectothermicincubation,thatisdo
notbroodtheireggsandrelyonenvironmentalheattoincubatetheireggs[21].Whilst
PLOSONE|DOI:10.1371/journal.pone.0150871 March30,2016 2/62
OsteologyandRelationshipsofSylviornis(Aves:Sylviornithidae)
S.neocaledoniaewasconsideredtobeamegapodethisideahadmerit.IfSylviornisisnolonger
consideredacrownoratleaststemmegapode,thenmoundbuildingforeggincubationwould
beunlikely.
AsecondgiantflightlessgalliformisknownfromFiji.MegavitiornisaltirostrisWorthy,
2000fromVitilevuinFiji,isslightlysmallerthanS.neocaledoniaeandwasdescribedasmega-
pode[15].Mourer-ChauviréandBalouet[16]consideredthesimilaritiesbetweenthesetwo
species,whichincludearemarkablysimilarcraniofacialhingeandatall,narrowrostrum,tobe
convergence.However,thesemorphologicalfeaturesarerareandapparentlyonlydistributed
amonggalloanseres,beingelsewhereonlyknowninDromornithidaeandGastornithidae[22–
24],soanyreappraisalofS.neocaledoniaethushastoalsoassessthisaberrantFijiangalliform.
Inthiscontribution,wethereforeseektoaddresssomeoftheseknowledgegapsbydescrib-
ingthepost-cranialskeletonindetail.Wehaveacollectionof600bonesofS.neocaledoniae
representingallskeletalelementsmadebysomeofus(THW,CS,AA)incavesonPindaiPen-
insula,NewCaledonia,inJuly2003[25].Detailsofthesitesandchronologyofthedepositsare
inAndersonetal.[25].Thematerialreportedpreviously[13,14,16]alsoderivesfromcaves
onPindaiPeninsula,butintheabsenceofanysitedescriptionsbyBalouetetal.,itisnot
knownwhetheritderivedfromoneofthesixcavessurveyedbyAndersonetal.[25],or
another.ThematerialdescribedhereallderivesfromseparatesitesinCaveB[25].Weuse
thesespecimenstointerpretthemorphologyofS.neocaledoniaeinacomprehensivephyloge-
neticanalysisofbothcranialandpostcranialcharacterstoestablishtherelationshipsofthis
strangebird,andtherebytestthehypothesesthatthisspeciesis(1)agalliformand(2)warrants
itsownfamilyseparatefrommegapodes.Indoingso,suchaphylogeneticanalysiswillshed
lightonwhetherS.neocaledoniaebuiltmoundsorusedectothermicincubation.Wewillfur-
thertestthispossibilitywithinthecontextoftheskeletaldescriptionbyexaminingthefunc-
tionalcapacityofS.neocaledoniaetoactuallyundertakeextensivediggingasdomegapodes.A
cursoryexaminationofsomefeatures,suchastheunguals,showsthattheydiffergreatlyfrom
thoseofmegapodesthatconstructlargemounds,e.g.Megapodiusspp.Thusinthecontextof
theskeletaldescription,wehavepaidparticularattentiontofeaturesthatmayimpacton,or
constrain,itsdiggingability,andcompareittomound—andnonmound—buildingmega-
podesandchickensGallusgallus.
MaterialsandMethods
Nomenclature
WefollowthenomenclatureandtaxonomicorderinDickinsonandRemsen[26].Namesfor
specificbonelandmarksfollowBaumelandWitmer[27]unlessotherwiseindicated.Anatomi-
callandmarksareabbreviatedinfigurecaptions.Somecommonanatomicaltermsareabbrevi-
atedasfollows:artic.(articularis);cond.(condylus);lig.(ligamentum);m.(musculus);proc.
(processus).
FossilMaterial
ThefossilsofS.neocaledoniaereportedherewascollectedbysomeofus(THW,CS,AA)in
cavesonPindaiPeninsula,NewCaledonia,inJuly2003[25].Detailsofthesites,theirloca-
tions,excavationstherein,andchronologyofthedepositsaregiveninAndersonetal.[25].
ThematerialdescribedhereallderivesfromseparatesitesinCaveBat21°21'005"S,164°57'
50.5"E[25].TheexcavationswereconductedwiththeauthorisationoftheNorthernprovince
PresidentPaulNéaoutyineandtheculturalauthoritiesandtheagreementofthecustomary
authoritiesofthetribesofthePoyaandPouemboutregion.AlltheSylviornisneocaledoniae
materialdescribedbelowispartofthecollectionsofInstitutd'ArchéologiedelaNouvelle-
PLOSONE|DOI:10.1371/journal.pone.0150871 March30,2016 3/62
OsteologyandRelationshipsofSylviornis(Aves:Sylviornithidae)
CalédonieetduPacifique,Nouméa,NewCaledonia.AllIANCPcataloguenumberscitedin
thispaperhavetheprefix‘IANCP.PN/WNP011.PA/1.2003/’,whichisabbreviatedto‘IANCP’
herein.TheSylviornismaterialiscataloguedintherange526–1088asdetailedinthedescrip-
tivesection.
ComparativeMaterial
Palaeognathae:Fossiltaxa.LithornispromiscuusHoude,1988[28]–USNM391983,336535,
424072;LithornisplebiusHoude,1988[28]–USNM336534–holotypeskeleton;Paracathartes
howardaeHarrison,1979[29]–USNMspecimens:cranium–361415;premaxilla–404758;
mandible–361437–9,404806;quadrate–424067;palatine/pterygoid–391984;vertebrae,C2–
404756,C3–361428–9;404747–8,404906;2Lcoracoids–361416–417;LRscapula–361418–9;
2Rhumerus–361420,361421;radius—L361424,proximalparts–361422–3,361441;ulnae—R
361425,L361426,R361427;LRcarpometacarpus–361445–6;Rfemur–361412;tibiotarsi—L
361407,R361408,d+pL361409,distal361410,pR361411,R404749,dL361409;5fibula–
361413–4,361442,361444,404750;tarsometatarsus—R361402,L361403,L361404,R
361405,L361406,L404747,L404748,361407,ungualphalanges–404069,404789,404797;
DinornisrobustusOwen,1846[30]–NMNZS.163,23342,23654,28225,32667.Extanttaxa:
Tinamusmajor(=robustus)–SAMB.31339,USNM347794,621694;Struthiocamelus–SAM
B.10941,11411,31336;LACM99638;Dromaiusnovaehollandiae–SAMB.6863,6898,7068,
31580,31581.
FossilGalliformes:MwalauwalterliniiWorthyetal.,2015[31]–seespecimenslistedin
Worthyetal.[31];MegavitiornisaltirostrisWorthy,2000–seeNMNZspecimenslistedin
Worthy[15];ProguranaracoortensisvanTets,1974–SAMP16700,17152–17154,17856–
17857,17876–17879,18181–18187,36710–36716,52473–52502;ProguragallinaceaDeVis,
1888–QMF1132,1134,1139,1143,5553,5556–5558,7005,7033.
ExtantGalliformes(alphabetical):Acrylliumvulturinum–LACM88965F,90645M,SAM
B23933;Aepypodiusarfakianus–ANWCO26042;Aepypodiusbruijnii–USNM146767;Alectura
lathami–SAMB46568,NMVB2209,B4288,B11471,B19290,B23648,B23649,B23650,QM
O27218,QMO27843,QMO27844,QMO27852;Coturnixpectoralis–SAMB49460;Crax
rubra–LACM113548,101626;USNM288713,19918;Eulipoawallacei–USNM558275;Gallus
gallus–SAMB11484,B46451,NMVB6363,B12748,B25087,QMO29536;Leipoaocellata–
SAMB414,B1094,B5039,B11480,B11481,B11482,B47825,B48526,B48765,B49461,
B51215,B55458,B55528,B58520,B58560;Macrocephalonmaleo–AMNH12013(byphotos
taken2000byJ.Palmer),NHMUK1891.7.20.97,1871.7.21.1;USNM225130;Megapodiusere-
mita–NMVB20648,(andB20641,B20642,B20647,B24000,B24947,B24948,B24949,B24950,
B24951,B24952,B25389);Megapodiusreinwardt–ANWCO22869;Ortalisvetula–KU13342,
USNM19632,288721,288722;Talegallafuscirostris–KU97007,ANWCO3669;Talegalla
jobiensis–USNM146744,ANWCO7567.
FossilAnseriformes:PresbyornispervetusWetmore,1926[32].Skull:USNM299846,
618166,618202.Premaxilla:USNM510082,299845(6noseslab).Mandible:USNM299847,
618169,618215.Quadrate:USNM498770.Thoracicvertebrae:USNM616555(specimenon
smallslab),618205,618207.Sternum:USNM618212,618214.Scapula:USNM616557–
616560–4specimens,618223—1L.Coracoid:USNM618183–left,616561–616564–4sternal
parts,616565–616567–3omalparts.Humerus—USNM483163castL,USNM616568–ptR
hum,618204–completeLonslab,618180–dL.Ulna—USNM616569–616571—3pL,616572
—1pR,616573&616574—2dR.Carpometacarpus—USNM616168–leftonslab,618226—
1pL,618227—1pR.Femur:USNM618228–completeR,618229—1dL,618230–618232—3dR,
618233–4—2pL,618235—1pR.Tibiotarsus:USNM483165–castR,618192–618196—5dL,
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OsteologyandRelationshipsofSylviornis(Aves:Sylviornithidae)
618236—1dR.Tarsometatarsus:USNM483166cast,USNM618175–dR,618176–dR,618177
–R,618178–pR(4parts),618213–R;618237–proximal.Pelvis:USNM618167–Rilioischial
complexexternalviewonslab,618172–Lilioischialcomplexinternalviewonslab,618198–
synsacrum.AnatalavisoxfordiOlson,1999–seeOlson[33];DromornisplaneiRich,1979[34]–
seeMurrayandMegirian[23]andMurrayandVickers-Rich[24].
ExtantAnseriformes:Chaunatorquata–USNM631124,614549,428074;Anhimacornuta–
MVB.12574;Anseranassemipalmata–SAMB36790,B48035;Dendrocygnaeytoni–SAM
B45769;Cereopsisnovaehollandiae–SAMB39638,49165;Ansercaerulescens–SAMB36868;
Malacorhynchusmembranaceus–SAMB39384,B39385,B39639;Tadornatadornoides–SAM
B.39583,39872.
Neoaves:Burhinusgrallarius–SAMB.49554,B.48793;Porphyriomelanotus–SAMB.49644;
Grusrubicunda–SAMB.49462.
Measurements
Allmeasurementsaremadewithdialcallipers(TESA)androundedtonearest0.1mm.Mea-
surementsareeitherasdescribedinthetextor,forthe56variablesusedinaPCA,areasgiven
inS1File.
Statisticalanalyses
SummarystatisticsformeasurementsweregeneratedinMicrosoftExcel.PrincipalComponent
Analyses(PCA)wereconductedinPASTv3.08[35]toinvestigatehowtheshapeofthetarso-
metatarsusandphalangesvariedamongthecomparedspeciestofacilitateapredictionofthe
diggingcapabilityofSylviornisneocaledoniae.Weassumethatdiggingcapabilityisaproxyfor
thepotentialtobuildmounds.Wethereforeassembledmeasurementsfrommultipleindividu-
alsofarangeofmegapodeswithvaryingmound-buildingability,fromthosenotknownto
buildmound(e.g.Macrocephalonmaleo)tothosethatbuildlargemounds(e.g.Megapodius
sp.)andcomparedthesetodataforS.neocaledoniaeandGallusgallus(S1File).Becausethere
isnoindividualofSylviornisneocaledoniaetocomparetotheseindividuals,weconstructedan
averageS.neocaledoniae‘individual’usingmeandataforallthevariablesfromTables1–21.
Thetaxavariedgreatlyinsize,withS.neocaledoniaebeingmanytimeslargerthanallofthe
extantmegapodes,thereforeinitialPCAplotsofuntransformeddatashowedS.neocaledoniae
widelyseparatedonPC1fromallothertaxa,whichweretightlygrouped.Astheaimofthe
analysiswastoassesshowshapevariedamongthesetaxaregardlessofsize,westandardized
thedatatosizeofthebirdbydividingallvaluesbyfemurlength.Femurlengthistightlycorre-
latedwithmass(e.g.,[36,37]),thereforethistransformationwillreducethemeasurementstoa
functionofbirdsize,whilepreservingdifferencesinshapeorrelativeproportionsofthedistal
leg.Missingdatawasanissue,especiallywhererarespecieswererepresentedby1to3speci-
mense.g.,Eulipoawallacei,M.maleoandMegapodiusreinwardt,andmanyspecimenstended
tohavethehornycoverstillontheunguals.Wethereforerestrictedmeasurementstothose
mostoftenavailableandonlymeasuredtheproximalphalangesandungualsI.2andIII.4.
Wheremissingdatawereunavoidable,weutilisedtheiterativeimputationmethodinPAST
v3.08wheremissingvaluesareatfirstreplacedbytheircolumnaverage,thenaninitialPCA
runisusedtocomputeregressionvaluesforthemissingdata.Thisprocedureisiterateduntil
convergence,seeIlinandRaiko[38].Weaddedtothesize-transformeddataaseriesofratios
designedtocapturetherelativelengthsofphalangesasaproportionofthetarsometatarsus
andalsoaratioofwidthanddepthoftheungualsatmidlengthtocapturethevaryingdegree
ofdorsoventralflatteningevidentintaxa.SeeS1Fileforanalysisdetails.
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OsteologyandRelationshipsofSylviornis(Aves:Sylviornithidae)
Massestimatesweremadeusingfemoralmid-shaftcircumference,whichforS.neocaledo-
niaeistheleast-shaftshaftcircumference,andthealgorithmsproposedbybothCampbelland
Marcus[36]andFieldetal.[37].
Phylogeneticanalyses
Theprimarypurposeofthephylogeneticanalysisemployedherewastoexaminetherelation-
shipsofSylviornisneocaledoniae.Thisspecieswasoriginallydescribedasaratite[10],but
affinitieswithmegapodeswerequicklyestablishedandwidelyaccepted[11–16]untilMourer-
ChauviréandBalouet[16]establishedamonotypicSylviornithidaeforit.Datamatriceshave
beencompiledtoexaminethephylogeneticrelationshipsofpalaeognaths[39–40],anatids
[41],galliforms[42–44],butnoneontheirownaresuitabletoassessthoseofapotentially
basalgalloanserinetaxon.
Wedevelopedasetof285characters(S2File)derivedfromdirectcomparisonofspecimens,
andfromtheliterature[mainlyfrom39,41,42,44–54].AsperWorthyandScofield[39],we
followedtwoguidingprinciplesthat:(1)thecharactersmustasfaraspossiblerelatetoasingle
morphologicalfeatureorcomplexthatisputativelyhomologousacrossallingroupandout-
grouptaxa;and(2)characterstatedefinitionshouldcapturethefullrangeofvariationacross
thetaxaanalysed.Followingtheseprinciplesandbecauseourtaxonsampledifferedfromany
previouslyused,werevisedallcharacters,sometimessubstantiallyfromthoseofpreviousdefi-
nitions.Thecharactersusedwerethoseidentifiedaspotentiallyrelevanttorelationshipswithin
Galloanseres.Therefore,charactersfrom,forexample,Ericson[48]andMayrandClarke[49],
withstatesthatwereconstantforcrownandstemgalloansereswerenotused.ThatGalloan-
seresisthesistergrouptoNeoavesiswellestablishedusingbothmorphological[48,49,55]
andmoleculardata(e.g.,[56–58])andsoexaminingthatrelationshipwasnottheaimofthe
presentwork.
WeassembledataxonsetthatsampledpalaeognathsandNeoavesastwosuccessivelycloser
outgrouptaxa,andaningroupencompassingarangeofanseriformandgalliformtaxa(gal-
loanseres)withafocusonmorebasaltaxa,andincludingkeyfossils.Becauseofpervasive
problemsofhomoplasyamongratitepalaeognathsrelatedtolossormarkedreductionof
wingsandlargesizeoflegbones,weincludedthreespeciesoflithornithids,whicharevolant
Eocenepalaeognaths.Theirage(55–48Maold:[28])meanstheyareseparatedfromthecom-
monancestorofcrowngalloanserinesbylessbranchlength(andthus,potentiallylessmorpho-
logicalevolution)thanareanyextantpalaeognathsorNeoaves.Inthephylogeneticallyfurthest
(palaeognath)outgroup,wealsoincludedatinamou,andthreeratites(Struthiocamelus,Dro-
maiusnovaehollandiaeandDinornisrobustus).
Thephylogeneticallyclosestoutgroup,andimmediatesistergrouptogalloanseres,included
threeNeoaves(Burhinusgrallarius(Charadriiformes),andPorphyriomelanotusandGrusrubi-
cunda(Gruiformes)),chosenfortheirsemi-terrestrialhabitstominimisemorphologicaldis-
paritywiththegalloanseres.
WithinGalloanseres,wesampled27extantandfossiltaxa.Thefollowingextanttaxawere
included:sevenspeciesinsixgeneraofMegapodiidae,sixothergalliformsrepresentingNumi-
didae,Cracidae,andPhasianidae,AnseranassemipalmataforAnseranatidae,Chaunatorquata
andAnhimacornutaforAnhimidae,andCereopsisnovaehollandiae,Ansercaerulescens,Den-
drocygnaeytoni,Malacorhynchusmembranaceus,andTadornatadornoidesinAnatidae.To
theseweaddedthefollowingfossiltaxa:Sylviornisneocaledoniae,thegiantFijianMegavitiornis
altirostris,describedbyWorthy[15]asamegapode,anextinctmegapodefromVanuatu
(Mwalauwalterlinii;[31]),theEoceneanseriformPresbyornispervetus(see[48,59]),thelate
CretaceousVegavisiaai(see[60]),andtheAustraliandromornithidDromornisplanei,which
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OsteologyandRelationshipsofSylviornis(Aves:Sylviornithidae)
iscurrentlyconsideredananseriform(see[23,24]).Allcharacterscoringwasbydirectexami-
nationofspecimenslistedinComparativeMaterial,exceptforV.iaai,whichwasscoredfrom
publisheddescriptions[60,61].Anatalavisoxfordiwasinitiallyalsoincluded,scoredfrom
Olson[33]andphotographsprovidedbyGarethDyke,butthistaxonactedasawildcard
greatlyreducingtreeresolutionandsupport,andwasthereforeexcluded.
(cid:1)
Thetaxon-charactermatrixwasanalysedwithparsimonyusingPAUP 4.0b10[62]and
BayesianinferenceusingMrBayes3.2.5[63].TheexecutabledatamatrixwithPAUPand
MrBayescommandsisappendedasS3File.Treeswererootedbetweenpalaeognathsandall
othersampledtaxa.BothparsimonyandBayesiananalyseswereperformed(1)withmultistate
charactersorderediftheyformedmorphoclines(seeS2File),or(2)allunordered.Thestates
for60charactersmarkedwithanasteriskinS2Filewereidentifiedasformingmorphoclines
andsoweretreatedasorderedinsomeanalyses.
Withthefulltaxonsetof27ingroupand10outgrouptaxa,theNeoavestaxaandthelithor-
nithidsandtinamouwereattractedtothestemoftheanseriformlineage,inconsistentwiththe
well-supportedmonophylyofpalaeognaths,andtheknownsistergrouprelationshipof
Neoaveswithgalloanseres(e.g.,[56–58]).Thiswasnotunexpectedbecauseoftworeasons:1,
theknownproblemswithhomoplasywithinlargeflightlessratites[39–40]thatwasexacer-
batedbymuchmissingdata(e.g.pectoralgirdleelementsnotscorableformanycharacters);
and2,thatthedatasetwasmainlyconstructedtodifferentiategalloanseres,with(asnoted
above)exclusionofcharactersinvariantamonggalloanseres,whichwouldpotentiallyhelp
resolveingroup-outgrouprelationships.Weconsiderthataseparatecharacterssetisrequired
toteaseouthigherrelationshipsofbirdsfromthosedesignedtoaddressthoseofspecific
groups,asexemplifiedbyEricson[48]andClarkeetal.[60].Ratherthanconstructanentirely
newanalysisanddatasetaimedatresolvingingroup-outgrouprelationships,weperformedthe
analyseswith(1)amolecularbackboneenforcingrelationshipsbetweenextanttaxasupported
bygeneticstudiesand(2)constraintsenforcingthewell-corroboratedingroupandoutgroup
relationshipsdiscussedabove,e.g.,(palaeognaths((Neoaves)(galloanseres)).
Themolecularbackboneemployedbelowconstrainstaxawithmoleculardata(allliving
taxaplusmoaDinornis)torelationshipssupportedbythisgeneticdata,withfossils(Mwalau
walterlinii,Dromornisplanei,Sylviornisneocaledoniae,Vegavisiaai,Presbyornispervetus,and
thethreelithornithidspecies)freetomovewithinthisbackbonetotheiroptimalpositions
basedonmorphologicaldata.Thisapproachensuresfossiltaxaareplacedwithinaphyloge-
neticframeworkoflivingtaxawhichisrobustlysupportedby(oftenlarge)amountsofavail-
ablemolecularevidence.Thefollowingstudieswereusedtoconstructthemolecularbackbone:
AvesandNeoaves[55–58],Palaeognathae[40–64],Galliformes[65],andAnseriformes
[66–68].
Parsimonyanalysestreatedallchangesasequal("unweighted")andusedheuristicsearches
withtree-bisection-reconnection(TBR)branchswappingandotherdefaultsettings,and1000
randomadditionreplicatespersearch.Whencalculatingtreelengths,multistatetaxawere
treatedaspolymorphismsratherthanambiguity.Gapsweretreatedasmissingdata.Strictcon-
sensustreeswerecomputedfromthesetofmostparsimonioustrees,andcladesupportwas
assessedbybootstrapping[69]usingthesamesettingsand1000replicates.Topreventthe
bootstrapanalysesfromgettingstuckonreplicateswithhugenumbersofequally-parsimoni-
oustrees,nchuckwassetto2000.
BayesiananalysesusedtheMarkovmodelofmorphologicalevolution[70]asimplemented
inMrBayes[62].BayesFactors(twicedifferenceinmarginallog likelihoods)ascalculated
n
usingstepping-stoneanalyses,stronglyfavouredincludingthegammaparameterforaccom-
modatingratevariationacrosscharacters(BF=65.48fortheanalyseswithorderedcharacters
andmolecularbackbone).The‘coding=inf’commandwasusedtocorrectforunder-sampling
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OsteologyandRelationshipsofSylviornis(Aves:Sylviornithidae)
ofinvariantandautapomorphiccharacters.Strengthofsupportwasassessedusingposterior
probability.
Results
Descriptionofthepost-cranialskeletonofSylviornisneocaledoniae
Vertebrae. Atlas,(Fig1A,1F,1K,1P,1a,1f,1kand1p):
Material:IANCP617,complete;IANCP618(Fig1),complete;IANCP619,nearcomplete,
missingtherightprocessusartic.caudalis.
Measurements(mm)inorderofspecimenslisted,withadashforunmeasurable:length
midlineofcentrum,7.0,6.8,10.9;widthacrosszygapophysiscaudalis,24.8,25.7,-;maximum
widthfossacondyloidea,13.0,12.7,12.0;maximumwidthfaciesartic.axialis,17.3,16.7,16.2;
heightatmid-widthfaciesartic.axialis,10.6,10.6,12.3;widthforamenvertebrale,12.0,10.9,
12.7;maximumheight,25.2,28.3,29.6.
TheatlaswasbrieflydescribedbyPoplinandMourer-Chauviré[12].Itisrelativelyshort,
beingaboutthreetimestallerthanitiscraniocaudallylong,althoughthearcusatlantisisonly
littleexpandeddorsallyoverthewidthofthecorpusatlantis(Fig1aand1k).Thecorpusatlan-
tishassubparallelsidesinitscaudalsectionthatframethenear-circularfossacondyloideain
cranialaspect(Fig1k).Theincisurafossaeisbroad,buttheforamenvertebraleisrelativelynar-
row,beingonlyslightlybroaderthanthefossacondyloidea.Theatlaslacksforaminatransver-
saria.Theprocessusartic.caudalesarerobust,lateromediallythickerthantheyarecaudally
projecting,andareroundedcaudallyinlateralview(Fig1fand1p).Thefaciesartic.zygapoph-
ysescaudalesaredistinct,yetsmallat5mmlongby4mmwide(Fig1k).Theincisura
arcuscaudalisisshallow(Fig1p).Thereisnodistinctprocessusventralismedially,butin
IANCP618,thereisasmallmedianpointcaudallyandinIANCP619theprocessusventrolater-
alesareconnectedmediallycreatingaslightventralprojection.Thereisapairofprocessusven-
trolateralesthatarecaudoventrallydirectedandprojectlesscaudallythantheyarewide;they
areusuallyseparatedbyashallownotchmedially(Fig1kand1p).
Axis,(Fig1B,1G,1L,1Q,1b,1g,1land1q):Material:IANCP620,complete;IANCP623
(Fig1),complete;IANCP624,nearcomplete,worncranially.Ofthese,IANCP620isofappro-
priatesizeandsimilarpreservationtoINACP619(atlas)andthefollowingcervicals,3
(IANCP621),4(IANCP622),and5(IANCP631),arelikelytobefromoneindividual.
Measurements(mm)inorderofspecimenslisted:Lengthmidlineofcentrumexcluding
dens,28.3,25.6,-;widthacrosszygapophysiscaudalis,47.5,44.8,42.0;maximumwidthfacies
artic.atlantica,estimatedat16.0,17.0,-;maximumwidthfaciesartic.caudalis(atdorsalside),
11.4,8.7,10.1;heightfaciesartic.caudalisincludingprocessusventralis,19.8,16.2,15.3;total
maximumheight,49.8,46.0,45.4.
TheaxiswasbrieflydescribedandfiguredbyPoplinandMourer-Chauviré[12].Itisdorso-
ventrallydeeperthanitiswideandischaracterisedbyamassivedorsoventrallythickened
arcusaxialisconnectingtheprocessusartic.caudalis(Fig1band1l).Thecorpusvertebrais
caudallynarrowerthanitisdeep,lacksbothafoveacranioventralisandafoveacaudoventralis,
andlaterallyhasaroundedprominenceatmid-depthjustcaudaltothecranialmargin(Fig1l).
Thefaciesarticularisatlanticaisbroaderthandeep,andshallowlyconcave(Fig1b).Thedens
isbroaderthandeepandnarrowscranially(Fig1g).Thefaciesarticulariscaudalisisheterocoe-
lusanddeeperthanwide,butisdirecteddorsally(Fig1land1q).Theprocessusspinosusis
low,formingarobustcrestcranially,butmergescaudallywithagreatlythickenedcaudalside
tothearcusaxialis,suchthatincaudalviewthearcusaxialisandprocessusartic.caudalisform
anevencurve(Fig1gand1q).Therearenoforaminatransversariaandprocessuscostalesare
absent.Theforamenvertebraleislaterallycompressedcranially,butcircularincaudalview.
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OsteologyandRelationshipsofSylviornis(Aves:Sylviornithidae)
Fig1.Vertebrae1–5ofSylviornisneocaledoniae.(A-E,a-e)anterior,(F-J,f-j)dorsal,(K-O,k-o)posterior,and(P-T,p-t)leftlateralviews.Photographs
(A-T)andinterpretivedrawings(a-t):Vertebra1,atlas,IANCP618(A,F,K,P);vertebra2,atlas,IANCP623(B,G,L,Q);vertebra3,IANCP621(C,H,M,R);
vertebra4,IANCP622(D,I,N,S);vertebra5,IANCP631(E,J,O,T).Abbreviations:aat,arcusatlantis;aax,arcusaxialis;ac,ansacostotransversaria;ale,
arealig.elastici;ave,arcusvertebrae;ca,corpusatlantis;faa,faciesarticularisatlantica;fac,faciesartic.caudalis;facr,faciesartic.cranialis;fazc,facies
artic.zygapophysiscaudalis;fazcr,faciesartic.zygapophysiscranialis;fc,fossacondyloidea;fcr,foveacranioventralis;forac,foramenarcocostalis
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OsteologyandRelationshipsofSylviornis(Aves:Sylviornithidae)
cranialis;fort,foramentransversarium;fv,foramenvertebrale;iac,incisuraarcuscaudalis;pac,proc.artic.caudalis;pc,proc.costales;ps,proc.spinosus;
pv,proc.ventralis;pvl,proc.ventrolaterale;tub,tuberosity.Cross-hatchingismissingbone.
doi:10.1371/journal.pone.0150871.g001
Thefaciesartic.zygapophysescranialesaregracileprojectionsonthearcusvertebraeatmid-
depthoftheforamenvertebraleandareabout5mmlongby4mmhighinIANCP623(Fig1b
and1q).Thefaciesartic.zygapophysescaudalesarenearcircularfacetsabout10mminwidth
thataredirectedventrallyfromtherobustprocessusartic.caudalis(Fig1land1q).Theproces-
susartic.caudalishaveadistinctgroovealignedcraniocaudallyontheircaudalmargin(Fig1b
and1l).Thecaudalfaciesofthearcusaxialisdorsaltothefaciesarticulariszygapophysescau-
dalesisnearplanarandatrightanglestotheventralsideofthecorpus(Fig1land1q).The
arcusaxialisisnarrowwhereitjoinsthecorpusvertebrae,butwidensmarkedlydorsally.There
isadeepincisuraarcuscaudalisbutnoincisuraarcuscranialisbelowthezygapophysescrania-
lis(Fig1q).Theprocessusventralisisbroadandrobust,withgreatestprojectionatthecaudal
endofthecorpus,butitisofvariabledepthinthethreespecimens(Fig1q).Thearcusaxialis
haspneumaticforaminapenetratingitcraniallyatthejunctionwiththecorpusasnotedby
wasbrieflydescribedbyPoplinandMourer-Chauviré[12],butthesearevariablypresenteven
oneachsideofanindividual,e.g.IANCP623hasalargeforamenontherightsidebutnoneon
theleft(Fig1q).
Anteriorcervicals,vertebra#3,(Fig1C,1H,1M,1R,1c,1h,1mand1r):Material:IANCP621
(Fig1),complete;IANCP625,incomplete,missingpartoftheleftside.
Measurements(mm)inorderofspecimenslisted:Lengthcentrumfromcranial-mostpoint
totheventralsideoffaciesartic.caudalis,31.7,31.0;widthacrosszygapophysiscranialis,-,
38.5;widthacrosszygapophysiscaudalis,52.1,46.1;maximumwidthfaciesartic.cranialis,
13.7,12.0;maximumwidthfaciesartic.caudalis,12.7,-;heightfaciesartic.caudalistoventral
sideprocessusventralis,15.9,-;maximumheighttakenparalleltoforamenvertebrale,46.0,-.
Vertebrathree,asbestexemplifiedbyIANCP621,iswiderthanhigh,andindorsalview
widenscaudally.Thecorpusvertebrahasamarkedfoveacranioventralisforreceptionofthe
upturnedfaciesartic.caudalisoftheaxisvertebra(Fig1c).Itislateromediallycompressed.The
faciesarticulariscranialisismuchbroaderthandeepanddirectedcranioventrally(Fig1c).The
faciesartic.caudalisisheterocoelousanddirectedslightlydorsallyfromtheplaneofthefora-
menvertebrale.Theprocessusspinosusisindistinctand,asfortheaxis,thearcusvertebraeis
veryrobustandarchesbetweentheprocessusartic.zygapophysescaudalesformingabroad
anddeepnearplanarcaudalfaciesabovethem(Fig1mand1r).Inthecentreofthisplanarcau-
dalfaciesisasmall(9mmhigh,7mmwide)arealigamentielasticifortheinsertionofliga-
mentslinkingtovertebrae4(Fig1m).Therearestronglyenclosedforaminatransversaria
about10mminlength(Fig1m).Theansacostotransversariabearsashortventralprocessus
butlacksaprocessuscostalis,soisroundedcaudallyinlateralview(Fig1r).Dorsallyatmid-
lengththereisasmallcircularforamenarcocostaliscranialis,whichpassesthroughtothecau-
dalsideofthefaciesarticulariscranialis(Fig1h).Theforamenvertebraleisslightlylaterome-
diallycompressedincranialviewbutcircularincaudalview.Thefaciesartic.zygapophyses
cranialesareslightlylonger(11–12mm)thanwide(8–10.5mm),andpointedmediocranially,
althoughtheirmarginsarenearcircularelsewhere(Fig1c).Thefaciesartic.zygapophysescau-
dalesarenearcircularandwiderthanlong(Fig1m).Thearcusvertebra,likefortheaxis,isnar-
rowatthejunctionwiththecorpusandbroadensdorsally.Theincisuraarcuscaudalisis
shallowerthanintheaxis(Fig1r).Theprocessusventralisisbroadandrobust,largestcaudally,
andextendsventrallyadistanceequivalenttoathirdofthedepthofthefaciesartic.caudalis
(Fig1mand1r).Therearesmallpneumaticforaminapenetratingthearcusvertebraewithin
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