7 Cervical Anatomy and Function in Turtles et al 2008...7 Cervical Anatomy and Function in Turtles...
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7 Cervical Anatomy and Function in Turtles Anthony Herrel, Johan Van Damme, and Peter Aerts CONTENTS 7.1 Introduction ......................................................................................................................... 163 7.2 Materials and Methods ....................................................................................................... 165 7.2.1 Anatomical Studies .................................................................................................. 165 7.2.2 Kinematic Analyses ................................................................................................. 165 7.3 Results ................................................................................................................................. 166 7.3.1 Osteology ................................................................................................................. 166 7.3.2 Cervical Joints ......................................................................................................... 167 7.3.3 Musculature ............................................................................................................. 169 7.3.3.1 Chelodina ................................................................................................... 169 7.3.3.2 Apalone ...................................................................................................... 175 7.3.4 Neck Movements...................................................................................................... 179 7.3.4.1 Neck Retraction and Cervical Mobility in Apalone ferox ......................... 179 7.3.4.2 Kinematics of Snorkeling in C. longicollis ................................................ 180 7.4 Discussion ........................................................................................................................... 181 7.4.1 Vertebral Structure .................................................................................................. 181 7.4.2 Cervical Musculature............................................................................................... 181 7.4.3 Movement Patterns .................................................................................................. 183 Acknowledgments .......................................................................................................................... 184 References ...................................................................................................................................... 184 . INTRODUCTION Being mobile is an essential requirement for any animal. Not only do animals need to move about to find food or partners, they also need to be able to escape potential predators (Irschick & Gar- land, 2001). Interestingly, some vertebrate groups appear to have sacrificed part of their mobility in response to predation pressure by the development of a robust armored body (e.g., pangolins, glyptodonts, turtles, and so on). Although body armor can provide an animal with an adequate protection against predators, it also dramatically reduces its locomotor ability and overall agility (Wren et al., 1998; Zani et al., 2005). Thus, many armored vertebrates have specialized on eating non-mobile food items like plants, or clumped food sources such as ants or termites (King, 1996). However, some groups have developed an alternative strategy for capturing elusive prey by devel- oping long, mobile appendages such as projectile tongues (Deban et al, 1997; Herrel et al., 2000) or a long neck (Gans, 1992). For instance, many semi-aquatic and aquatic turtles have developed remarkably long necks that are used to capture elusive prey under water (Pritchard, 1984). Although the turtle carapace provides an excellent defense against predators, it is imperative that the long neck and head can be protected as well. To do so, the head-neck system needs to be withdrawn within the margins of the bony shell. This can be done in one of two ways: in the
Transcript of 7 Cervical Anatomy and Function in Turtles et al 2008...7 Cervical Anatomy and Function in Turtles...
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7 CervicalAnatomyandFunctioninTurtles
Anthony Herrel, Johan Van Damme, and Peter Aerts
Contents
7.1 Introduction......................................................................................................................... 1637.2 MaterialsandMethods....................................................................................................... 165
7.2.1 AnatomicalStudies.................................................................................................. 1657.2.2 KinematicAnalyses................................................................................................. 165
7.3 Results................................................................................................................................. 1667.3.1 Osteology................................................................................................................. 1667.3.2 CervicalJoints......................................................................................................... 1677.3.3 Musculature............................................................................................................. 169
7.3.3.1 Chelodina................................................................................................... 1697.3.3.2 Apalone...................................................................................................... 175
7.3.4 NeckMovements...................................................................................................... 1797.3.4.1 NeckRetractionandCervicalMobilityinApalone ferox......................... 1797.3.4.2 KinematicsofSnorkelinginC. longicollis................................................ 180
7.4 Discussion........................................................................................................................... 1817.4.1 VertebralStructure.................................................................................................. 1817.4.2 CervicalMusculature............................................................................................... 1817.4.3 MovementPatterns.................................................................................................. 183
Acknowledgments.......................................................................................................................... 184References...................................................................................................................................... 184
�.� introduCtion
Beingmobileisanessentialrequirementforanyanimal.Notonlydoanimalsneedtomoveabouttofindfoodorpartners,theyalsoneedtobeabletoescapepotentialpredators(Irschick&Gar-land,2001).Interestingly,somevertebrategroupsappeartohavesacrificedpartoftheirmobilityinresponse topredationpressureby thedevelopmentofarobustarmoredbody(e.g.,pangolins,glyptodonts, turtles, and soon).Althoughbodyarmor canprovideananimalwith anadequateprotectionagainstpredators,italsodramaticallyreducesitslocomotorabilityandoverallagility(Wrenetal.,1998;Zanietal.,2005).Thus,manyarmoredvertebrateshavespecializedoneatingnon-mobilefooditemslikeplants,orclumpedfoodsourcessuchasantsortermites(King,1996).However,somegroupshavedevelopedanalternativestrategyforcapturingelusivepreybydevel-opinglong,mobileappendagessuchasprojectiletongues(Debanetal,1997;Herreletal.,2000)oralongneck(Gans,1992).Forinstance,manysemi-aquaticandaquaticturtleshavedevelopedremarkablylongnecksthatareusedtocaptureelusivepreyunderwater(Pritchard,1984).
Althoughtheturtlecarapaceprovidesanexcellentdefenseagainstpredators,itisimperativethat the longneckandheadcanbeprotectedaswell.Todo so, thehead-neck systemneeds tobewithdrawnwithinthemarginsofthebonyshell.Thiscanbedoneinoneoftwoways:inthe
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mid-sagittalplane(vertically),whichinvolvestheretractionoftheheadandneckwithinthebonyshell,orlaterally(inthehorizontalplane),wheretheneckisfoldedbetweenthedorsalandventralrimofthebonyshell.Inthiscase,theheadandneckdoremainpartiallyexposedintheoutercara-pacialchamberinfrontofthepectoralgirdle(VanDammeetal.,1995).ThisdifferenceinthemodeofneckretractioninturtleshasoftenbeenusedasanimportantcharacterforthesubdivisionoftheclassTestudinesintothesubclassesCryptodiraandPleurodira.Whereascryptodiresretracttheirhead-necksystemintheverticalplane,pleurodiresdosointhehorizontalplane(Figure7.1).
Accuratecontroloftheneckduringrapidmovementsassociatedwithescapeheadretractionandpreycaptureappearscrucialforturtles.However,theturtleneckisahighlycomplexmulti-jointedsystem,consistingofeightcervicalvertebrae,thehead,andthebodyandalargenumberofmusclesthatspananywherefromonetoovereightjoints.Thecontrolofsuchamulti-jointsystemwithalargenumberofdegreesoffreedomappearsinherentlycomplex.Althoughsomewaystofacilitatethecontrolofthesystemhavebeenidentifiedpreviously(Aertsetal.,2001),abetterunderstandingof thedetailedstructureandfunctionof themusculo-skeletalelementsof thecervicalsystemisessentialtogainbetterinsightintothecontrolofthecervicalsystem.Moreover,largedifferencesinvertebralstructure,inthemorphologyofassociatedmusculature,andinthecontrolofthecra-nio-cervicalsystemcanbeexpectedforturtlesthatretracttheirneckspredominantlyineitherthehorizontalorverticalplane.Unfortunately,previousauthorshavedescribeddifferencesinvertebralstructurebetweencryptrodiranandpleurodiranturtlespredominantlyfromataxonomicstandpoint(Vaillant,1881;Williams,1950;butseeWeisgram&Splechtna1990,1992).Thus,itremainspres-entlyunclearwhetherdifferentfunctionalcapacities(i.e.,rangesofmobility)areassociatedwitheithermorphology.Withoutthistypeofinformation,ourunderstandingofthecontrolofthecranio-cervicalsystemincryptodiranandpleurodiranturtlesmust,unfortunately,remainlimited.
Theaimof thepresent chapter is togiveadetailedmorphologicaldescriptionof thecervi-calsysteminpleurodiranandcryptodiranturtles.Indoingso,ouremphasiswillbeonthefunc-tionalconsequencesofdifferencesinmorphologyinthetwogroups.Additionally,somepreviouslyunpublisheddataon theactualkinematicsofneckmovementwillbepresented tohighlight theconsequencesofmorphologicaldifferencesinthetwogroups.Asourtyperepresentativesforcryp-todiranandpleurodiranturtleswehavechosenthegeneraChelodinaandApalone.TheAustralianpleurodiranturtlesofthegenusChelodinaarerenownedfortheirextremeelongatedneck.Becausetheneckislongerthanthecarapace,theseturtlesarealsoknownassnake-neckedturtles.Theseanimalsusetheirelongatedneckbothforquickstrikesatpreyandforsnorkeling,thusaspiratingairfromthesurfacewithoutexposingmorethanthetipofthesnout.Speciesfromthisgenuswillbeusedasatypicalrepresentativeofthepleurodirancondition.TurtlesofthegenusApalone,alsoknownasthesoft-shelledturtles,representthecryptodirancounterpartofChelodina.Theseani-malsarealsocharacterizedbyanextremelyelongatedneck,oftenlongerthanthecarapaceitself(Ernst&Barbour,1989).Soft-shellturtlestypicallyliveinshallowwaterandwillusetheirelon-gatenecktobreatheatthewatersurfacewithminimalmovement.Moreover,justlikeChelodina,
Cryptodira Pleurodira
figure�.� Schematicrepresentationofthetwomajormodesofheadretractioninturtles.Left,lateralviewonthecervicalsysteminacryptodire.Incryptodires,theheadisretractedintheverticalplane.Right,dorsalviewonthecervicalsysteminapleurodire.Heretheheadisretractedinthehorizontalplane.
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membersofthegenusApalonearevoraciouspredatorsthatwillactivelystrikeatelusivepreyunderwater(Dalrymple,1977;Ernst&Barbour,1989).
�.� materialsandmethods
7.2.1 AnAtomIcAlStudIeS
The anatomy of the cervical vertebrae, joint structures, and cervical musculature of Chelodinalongicolliswasstudiedbymeansofdissectionofapreservedspecimen(K.B.I.N.,R.G.nr.4566).Additionally,anadultC. reimani(cadaverobtainedthroughthecommercialpettrade)wasusedtostudythecervicalanatomy.OneindividualofthespeciesApalone feroxandoneA. spiniferusweredissectedtoinvestigatetheanatomyofthecervicalsysteminatypicalcryptodire.Animalswereobtainedthroughthecommercialpettrade,sacrificedbymeansofanoverdoseofNembutalandpreservedina10%aqueousformaldehydesolutionfor24hours.Next,animalswererinsedexten-sivelyandtransferredtoa70%aqueousethanolsolution.
Cervicalmorphologywasstudiedbymeansofdissections.Inthemorphologicaldescriptions,vertebraeareindicatedbycapitalCorD(cervicalanddorsalvertebrae,respectively)followedbytheirserialnumber.C1isclosesttothehead.Jointsarelabeledbythenumberoftheadjacentver-tebrae:C(n)-(n −1),withnthenumberofthemorecaudalvertebraand(n −1)thenumberofthemorecranialoneassuggestedbyHeidweiller(1991).Forexample,thejointbetweenvertebra5and6isdefinedas“jointC6-5.”
7.2.2 kInemAtIcAnAlySeS
Tostudythekinematicsofsnorkeling,twoliveadultspecimensofChelodina longicolliswereusedfortheexperiments(onefemaleof730g,18cmcarapacelengthandonemaleof520g,15cmcara-pacelength).TheanimalswereobtainedwiththehelpoftheAntwerpZooandwerehousedinaglassaqua-terrariumona12-hourlight/darkcycle.OneliveApalone feroxandoneliveA. spiniferus,obtainedthroughthecommercialpettrade,wereusedtostudythemobilityofthecervicalvertebraeintheselong-neckedcryptodires.Thewatertemperaturewaskeptat28°Cforallspecies.Twiceaweek,theturtleswerefedwithmeat,mice,andsmallinvertebrates(crickets,grasshoppers).
Snorkelingmovements(neckmovementsintheverticalplane)ofC. longicolliswererecordedbymeansofcineradiographyinlateralviewusingaPolydoros80SgeneratorequippedwithaSiemensSiregraphD40x-rayflashapparatusat66kV.Thedigitalcineradiographicrecordings(dependingonthesequence4or6framespersecond,FluorospotH)wereprintedonScopixlaserfilm(35×43cm)bymeansofanAgfalaserprinter.Duringtherecordings,theanimalswererestrainedbymeansofabody-shapedcorselet.Thiscorseletwasmountedunderthewatersurfaceonafixedframe.
Thesequenceswereprojectedframebyframeanddigitized.Digitizationofthepositionofthejointsallowedthecalculationofseveralkinematicalparameters(jointangles,elevationofthehead,headposition)inaturtle-boundframe.Thesameterminologyofjointrotationsisusedasdescribedfortheneckmovementsinthehorizontalplane,i.e.,clockwiserotationsaredefinedaspositive.
MobilityofthecervicalvertebraeinA. feroxandA. spiniferuswasstudiedbymeansofCTscanning.TheanimalwasanesthetizedbymeansofintramuscularinjectionofKetamine(150mg/kgbodymass).CTscanswererecordedusingaCT-highlightAdvantagescannerattheUniversityofAntwerpHospital.Of10different staticneckpositions, ranging fromfullyextended to fullyretracted,3-slongrecordingsresultingin1.5mmthickslicesthroughthevertebralcolumnweremadeat140kV,140mA.ScanswereprintedonScopixLT2B-100NIFx-rayfilm.
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�.� results
7.3.1 oSteology
Thecervicalcolumninallrecentturtlesconsistsofeightelongatedvertebrae(C1toC8)andninejoints.Themostimportantelementofthevertebraeisthevertebralcentrum,whichispositionedrightbelow the spinalcord.From thecentrum, theneuralarch risesandcovers the spinalcord(Figure7.2).Theneuralspinesarepositionedmidventrallyontheneuralroofandarereducedinmost turtles (Figure7.2).Thearticulationof thedifferentvertebraeoccursbymeansof thever-tebral centra and the zygapophyses (Figure7.2).Theprezygapophysesof thevertebra articulatewiththepostzygapophysesofthemorecraniallysituatedvertebra.Whereasthearticularfacetsoftheprezygapophysesarepositioneddorsally,thoseofthepostzygapophysesareorientedventrally.Vertebralcentracanbebiconvex(C5andC8inChelodina),biconcaveoramphicoelous(C1inbothspecies;C7 inChelodina), procoelous (C6 inChelodina) or opisthocoelous (C2,C3, andC4 inChelodina;C2toC8inApalone).
Inatransversesection, thevertebralcentrumofChelodina issaddle-shaped(Figure7.3andFigure7.4).Thevertebralcentrumiswelldevelopedonlyattheleveloftheanteriorandposteriorarticulations.Theneuralspineisreducedtoaninconspicuouslongitudinalrim.Theanteriorzyg-apophysesareclearlyseparatedfromeachother(Figure7.3andFigure7.4).Theirarticularfacetsaremainlyorientedinthemedio-dorsaldirection.TheposteriorzygapophysesarefusedtoeachotherexceptthoseofC1(Figure7.3),butthearticularfacetsremainseparatedandfacemainlyven-trallyandslightlylaterally(Figure7.3andFigure7.4).Theelevationoftheposteriorzygapophysisgraduallyincreasesfromdistaltoproximal(Figure7.3andFigure7.4).Thetransverseprocessesarestronglydeveloped,especiallythoseonthemoreproximalvertebrae(Figure7.3andFigure7.4).
Thecervicalvertebrae inApalone are relativelygracileandelongated (Figure7.5andFig-ure7.6).Theybearwell-developedandwell-separatedpre-andpost-zygapophyses(Figure7.5and
A
Posterior zygapophysis
Caudal
Centrum
Ventral
Transverse process
BPosterior zygapophysisArticular facets
posterior zygapophysisAnterior zygapophysis
Neural canal
Transverse process
Posterior articular facetof the centrum
C Posterior zygapophysis
Anterior zygapophysis
Neural canal
Transverse process
Anterior articular facetof the centrum
Cranial
Anterior zygapophysisNeural arch
Dorsal
figure�.� Chelodina longicollis.Terminologyofthemostimportantstructuralelementsofacervicalverte-bra(C7).(A)Lateralview,(B)posteriorview,and(C)anteriorview(terminologyafterRomer&Parsons,1977).
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Figure7.6).Theorientationofthezygapophysesisvariablethroughouttheneck.Becauseoftheabsence of the iliocostalis and logissimus groups (discussed later), the transverse processes areonlypoorlydeveloped(Figure7.5andFigure7.6).Becauseof thestrongdivergenceof thepost-zygapophysesandtheabsenceofawell-developedneuralspine,ahiatusintervertebralis(Bojanus,1821)iscreated.InApalone,thishiatusiscoveredbyathickmembrane(Ogushi,1913).
7.3.2 cervIcAlJoIntS
Joint S(kull)-C1 (occipito-cervical joint). This procoelous ball-and-socket type joint allows theskulltomoveindependentlyfromtheneck.Theoccipitalisspherical.Theridgesofthecongru-entcotyleonC1arewelldeveloped.C1lacksanteriorzygapophyses.Theconnectionbetweenthe
Lateral view
Dorsal view
Frontal view
Caudal view
C1 C2 C3 C4
figure�.� Lateral,dorsal, frontal,andcaudalviewsof thefirst fourcervical (C1-C4)vertebrae inC. longicollis.
Lateral view
Dorsal view
Frontal view
Caudal view
C5 C6 C7 C8
figure�.� Lateral, dorsal, frontal, and caudal views of the last four cervical (C5-C8) vertebrae in C. longicollis.
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neuralarchofC1andthebaseoftheskullisligamentous.ThejointissimilarinbothApaloneandChelodina.
JointsC2-1,C3-2,C4-3,C5-4(anteriorpartoftheneck).Thearticulationfacetsofvertebraecomposing these joints are very similar. The vertebral centra are all opisthocoelous and haveananteriorellipticalcotyle,ofwhich the longaxis isorientedvertically inChelodinaandhori-zontallyinApalone,andaposteriorcondylewithenlargedlateralridges.Thearticularfacetsofthezygapophysesof themostcranial jointof thisgroup(C2-1)are lessstronglydeveloped.TheelongatedneuralspineofC2extendsanteriorlybeyond thearticular facetsof theposteriorzyg-apophysesofC1inbothgroups.TheposteriorzygapophysesofC1areclearlyseparated.In themorecaudaljoints,thezygapophysesareelongatedandslightlyelevated(Figure7.3).Thearticularfacetsoftheanteriorzygapophysesareslightlyconcaveandtheiroutlineiskidney-shaped.Theyareoriented in a dorso-medial direction.Theposterior zygapophyseal facets are ventrolaterallyinclined.LateralmobilityisstronglyreducedinApalonecomparedtoChelodinabecauseofthepairedpost-zygapophyses.
Lateral view
Dorsal view
Frontal view
Caudal view
C5 C6 C7 D1C8
figure�.� Lateral,dorsal,frontal,andcaudalviewsofthelastfourcervical(C5-C8)andthefirstdorsalvertebra(D1)inA.spinifera.
Lateral view
Dorsal view
Frontal view
Caudal view
C1 C1́ C2 C4C3
figure�.� Lateral,dorsal,frontal,andcaudalviewsofthefirstfourcervical(C1-C4)vertebraeinA. spi-nifera.C1′istheintercentrumoftheatlas.
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JointsC6-5andC7-6.ThecentraljointsC6-5andC7-6areprocoelousinChelodinabutopis-thocoelousinApalone.Inposteriorview,theposteriorcondyleofC5inChelodinahastheshapeofaraindrop.Alternatively,inChelodinathecondyleofC6isalmostspherical.ThecongruentcotyleontheanteriorsideofC6andC7haspronouncedlateralandventralridges.Thearticularfacetsoftheposteriorzygapophysisarewelldevelopedandalsohaveakidney-shapedoutline.Thebilateralposteriorzygapophysealfacetscontacteachothermedially,formingasemicircularorhorseshoe-shapedarticularsurface.Thearticularfacetsoftheanteriorzygapophysesaremoreoval(almostcircular)ascomparedtothemoredistaljoints.InApalone,thearticulatoryfacetsofthepost-zyg-apophysesarepositionedhorizontally.Thepost-zygapophysesthemselvesarenearlyinlinewiththelongaxisofthevertebrae(lessthan6°).
JointC8-7.C8-7isopisthocoelousandtheshapeofitscondyleandcotyleresemblepreviouslydescribedophisthocoelousjointsinbothgroups.ThecotylehasenlargedlateralridgesinChelo-dinaandisfullysplitinApalone.TheposteriorzygapophysisofC7iselongated,inclinedindorsaldirectioninbothgroups(Figure7.4).Thearticularfacetsareclearlydistinguishablefromthoseoftheremainderof thezygapophysesandare laterallyorientedinChelodina.TherathershortbutstronglyelevatedanteriorzygapophysesofC8tendtoinclinedorsomediallyinChelodinabutmorelaterallyinApalone.
JointD1-C8(cervico-dorsal joint).D1-C8 isprocoelous inChelodina. InApalone, this jointlacksacentralarticulation.InChelodina,theratherflattenedcondyleontheposteriorpartofC8isalmostcircular.Thearticularfacetfacescaudo-ventrally.ThecircularcongruentcavityontheanteriorpartofD1isshallowerthanthoseonthemoreanteriorjoints.Theelongateposteriorzyg-apophysisinChelodinaismoreelevatedinthedorsaldirectionthanthatofjointC8-7(Figure7.4).Thearticularfacetsofthezygapophysesaremoreinclinedthanthoseinthepreviouslydescribedjoints.OnC8,thearticularfacetsofbothsidesfuseandareclearlydistinguishablefromthepos-teriorzygapophysis.Theirappearanceisthatofaverticallypositionedcylinder(approximatingaverticalhingejoint).TheanteriorzygapophysesonD1arerathershortandpresentanincreaseddor-somedialinclinationofthearticularfacets.InApalone,thepost-zygapophysesofC8areextremelywelldevelopedandwider than thoseof themoreanteriorly situatedvertebrae (Figure7.6).Thearticulatoryfacetsarestronglyconcave.Thepre-zygapophysesofD1havebeenrearrangedtohori-zontallyorientedcylinders.Onlyventroflexionispossibleatthisjoint.
7.3.3 muSculAture
ThefollowingshortdescriptionofthecervicalmusculatureisbasedontheterminologyofShah(1963)forChelodinaandthatofOgushi(1913)forApalone.Othermorphologicalaccountsonthecervicalmusculatureinturtles(Bojanus,1819;George&Shah,1954,1955;Scanlon,1982)wereconsultedtoclarifythepositionofcertainmuscleswhereneeded.
�.�.�.� Chelodina
m.constrictorcolli.Thisisathinsheet-likemusclewhichcoversthefirsttwothirdsoftheneck.Themusclehasadualorigin:somefibersoriginateonthesquamosalandthedorsalconnectivetissueassociatedwiththeoccipitalspineandothersoriginateontheneuralspinesofC2-C6.Thefibersrunventrallyandinsertmidventrallyonacentralconnectivetissuesheet(medianraphe).
m.retrahenscapitisetcollique(Figure7.7).Thismuscleconsistsofanumberofwell-developedandindividualizedbundlesthatconnectthecarapacetotheneckandhead.ThefirstbundleisthelongestandoriginatesatthelateralaspectofD8andtheadjacentpartofthecarapace.Themusclerunscraniallyandinsertsbymeansofalongtendonatthebasioccipital.AnumberoffibersfromthefirstbundleinsertonthelateralaspectofC1-C5.ThesecondbundleoriginatesatthelevelofD5.ThemusclerunscraniallyandinsertstendinouslyatthelateralaspectofC5.Thethirdbundle
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Carapace
Tendon
Bundle 2 Bundle 3
Bundle 1 Tendon
Bundle 4
Bundle 2 *
Bundle 2 *
Bundle 6 Bundle 5
Bundle 7 Bundle 4
m. longissimus cervicis
m. longissimus thoracis
Lateral bundles
Medial bundle
Bundle 3 *
Bundle 3 *
Bundle 1 * Bundle 1 *
Bundle 4 *
Bundle 4 *
Pectoral girdle
*
Skull
m. retrahens capitis collique
figure�.� Schematicrepresentationofthem.retrahenscapitiscollique,them.longissimuscervicis,andthem.longissimusthoracisinC. longicollis.
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m. semispinalis
m. testocapitis
m. spinalis cervico-capitis
Medial bundle
Lateral bundle
figure�.� Schematicrepresentationofthem.semispinalis,them.testocapitis,andthem.spinaliscer-vico-capitisinC.longicollis.
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m. rectus cervicis
m. scalenus complex
m. scalenus I
m. scalenus II
m. scalenus III
m. scalenus IV
Tendon of m. retrahens capitis collique
figure�.� Schematicrepresentationofthem.rectuscervicisandthem.scalenuscomplexinC. longicollis.
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m. constrictor hyoideus
mm. intertransversarii colli
m. longus colli
b8 b6
b7 b5
6
5 4 3 2 1
b3
b4 b2
figure�.�0 Schematicrepresentationofthem.constrictorhyoideus,themm.intertransversariicolli,andthem.longuscolliinC.longicollis.
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originatesatD4and insertsat the lateral aspectofC7.The fourthbundleoriginatesatD3andinsertsatthetransverseprocessofC8.
m.longissimuscervicis(LC,Figure7.7).Thisisasegmentallyarrangedmusclewithamorecomplexarrangement.TheLCofC7originatesonthepre-zygapophysisofC8.Themusclebellyrunsanteriorlyanddividesintoamoremedialandalateralbundle.Thelateralbundleinsertsonthepost-zygapophysisofC6andthemedialonthelateralaspectofC5.TheLC6originatesonthepre-zygapophysisofC7andinsertsonthepost-zygapophysisofC5.TheLC5originatesonthepre-zygapophysisofC6andinsertsonthepost-zygapophysisofC4.TheLC4originatesonthepre-zygapophysisofC5andinsertsmainlyontheneuralarchofC1.Duringthecourseofthemuscle,fibersdivergeandinsertonthepost-zygapophysesofC3andC2aswell.
m.longissimusthoracis(Figure7.7).Thismuscleisresponsibleforlateralflexionoftheposte-riorpartoftheneckandconsistsofonemedialandtwolateralbundles.Allbundlesoriginateattheventralaspectofthecarapace,cranialtotheoriginofthem.testocapitis.ThemedialbundleinsertsatthelateralaspectofC8.ThefirstlateralbundleinsertsbymeansofatendononC6atthelevelofthepost-zygapophysis.ThefibersofthelateralmostbundleruninitiallyventraltothepreviousbundlebutrunmorelaterallyatthelevelofC7.Themusclebundleinsertstendinouslyatthelevelofthepost-zygapophysisofC5.
mm.semispinalis(Figure7.8).Thisisaseriesofshortseriallyarrangedmusclesthatspanadja-centvertebraeandrunfromC2toC8.Themusclesoriginateattheneuralspineofthemoreposte-riorvertebraandrunanterolaterallytoinsertonthepost-zygapophysisoftheanteriorvertebra.
m. testocapitis (Figure7.8). This is a very long muscle that consists of two distinct musclebundlesthatconnectthecarapacetotheheadandneck.Bothbundlesoriginateattheventralaspectofthecarapace,lateraltothescapula.ThefibersofthemedialbundleconvergeontoastrongtendonthatinsertsatthelateralaspectofC5.ThelateralbundleinsertsthroughacomplexarrangementoftendonsintheanteriorpartoftheneckatthelateralaspectofC4-C2.
m.spinaliscervico-capitis(Figure7.8).Thisissuperficialdorsalcervicalmusclebundle.ThemuscleoriginatesattheneuralspinesofC3-C5andrunsobliquelyanteriorly.Themoremediallypositionedfibersinsertonthelateralaspectoftheoccipitalspineandthemorelateralfibersonthedorsalaponeurosiscoveringthem.adductormandibulae.
m.rectuscervicis(Figure7.9).This isaverylongandventrallypositionedmusclethatcon-nectsthepectoralgirdlewiththeventralaspectofthehyobranchium.Themuscleoriginatesatthemid-dorsalaspectofthecoracoid.Thefibersrunventrallyandjointhefibersofthem.constrictorhyoideusofthesameside.Atthelevelofthehyobranchium,thetwomusclesseparateagainandthefibersofthem.rectuscervicisinsertpartiallyonthesecondceratobranchialandpartiallyonthebasibranchium.
m. scalenus complex (Figure7.9).This is a seriesof fourmuscles that connect thepectoralgirdlewiththelateralaspectoftheposteriorneck.Themostsuperficialbundleisverythinandrunsbetweentheacromion,thedorsalaspectoftheplastron,andtheposteriormostcervicalvertebrae(C6-C8).Thesecondandventralmostbundleofthescalenuscomplexoriginatesontheacromionbutdistallytothefirstbundle.ThefibersinsertattheventrolateralaspectofC4andC5.Thethirdbundleoriginatespartlyonthescapulaandpartlyontheacromion.ThefibersconvergeonaflattendonthatinsertsattheventrolateralaspectofC5.Thefourthpartistheshortestandoriginatesacrosstheentirewidthofthescapula.Themuscleinsertsontheproximalaspectofthetendinousinsertionofthesecondbundleofthem.retrahenscapitisetcollique.
m.constrictorhyoideus(Figure7.10).ThismuscleoriginatesatthelateralaspectofC6,runscraniallyandinsertsattheposterioraspectofthefirstceratobranchial.Althoughitsprimaryfunc-tionispresumablyrelatedtotheabductionandretractionoftheceratobranchial,itpresumablyalsoplaysaroleduringlateralbendingoftheneck.
mm. intertransversarii colli (Figure7.10). This is another segmentally arranged muscle thathasadualorigin.Thelateralbundleoriginatesattheventralaspectandthemedialbundleatthe
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CervicalAnatomyandFunctioninTurtles ���
diapophysisofthecervicalvertebra.Bothbundlesjoinandinsertattheposterioraspectofthever-tebralcentrumofthemorecraniallypositionedvertebra.
m.longuscolli(Figure7.10).Thismuscleconsistsofaseriesofsegmentallyarrangedsmallmusclebundlesthatrunincloseassociationtothem.retrahenscapitisetcollique.Thelonguscollibundlesofthefirstfivevertebraeoriginateattheventralaspectoftherespectivevertebrae.Inser-tiontakesplacebymeansofthetendinousinsertionofthesecondbundleofthem.retrahenscapitisetcolliqueonthelateralaspectofC4-C1.Themusclesinthemoreposteriorpartoftheneckaresomewhatmorecomplex.Them.longuscolli8originatesontheventralsideofC8andinsertsonthetendonofthesecondbundleofthem.retrahenscapitisetcollique.Thelonguscolli7originatesattheventralaspectofC7andinsertsbymeansoftheinsertionofthetendonofthesecondbundleofthem.retrahenscapitisetcolliqueatthelateralaspectofC5.Thelonguscolli6originatesattheventralaspectofC6andinsertsatthelateralaspectofC5.
�.�.�.� Apalone
NotableinApaloneisthestrongreductionoftheepaxialmusculature(Hofstetter&Gasc,1969),theabsenceofthelongissimussystem,andtheabsenceoftheiliocostalissystemthatischaracteristicforallturtles.
m. constrictor colli (m. sphincter colli, Ogushi, 1913). This muscle is poorly developed inApaloneandconsistsoftwodiscreteparts.Theanteriorpartcoversthelateralandventralaspectoftheanteriorneckregion.Itoriginatesonthedorsalconnectivetissueassociatedwiththeoccipitalspineandrunsventrallytoinsertonthemedianraphe.Theposteriorpartisoftendifficulttodis-cernandoriginatesmoreposteriorlyintheneckonthenuchalconnectivetissueassociatedwiththeneuralspinesandinsertsventrallyonthemedianraphe.
m.rectuscervicis(m.coraco-hyoideus,Ogushi,1913).Thisistheventral-mostmuscleinthecervicalregion.Themusclehasadualorigin—onepartoriginatesonthedorsalaspectoftheproxi-malpartoftheprocoracoid,andtheotherpartoriginatesatthedorsalaspectoftheepicoracoid.Themusclerunsanteriorlyandinsertsattheposterioraspectofthebasibranchium.
m.carapaco-basioccipitis (Figure7.11).This isavery longmuscle that runs fromthepelvicgirdletothecranium.Threedistinctoriginsonthecristamedianaventralisofthefirst,second,andthirdcaudalvertebraearepresent.Inaddition,threeaccessorysitesoforigincanbediscerned:ontheproximalaspectofthefifthrib,acrosstheentirelengthofthesixthcostalplate,andalongtheentireseventhribandassociatedcostalplate.Thefibersofthislastbundleinitiallyrunatanangleofatmost90°tothelongaxisoftheremainderofthemuscle.
m. carapaco-basioccipitis
Costal plate Rib
figure�.�� Schematicrepresentationofthem.caracapo-basioccipitisinA. spinifera.
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��� BiologyofTurtles
A
m. spinalis cervico-capitis - cauda hyoidea
m. spinalis cervico-capitis - cauda squamosi
m. spinalis cervico-capitis - cauda occipitalis
m. spinalis cervico-capitis - cauda cornu branchiale II
m. spinalis cervico-capitis
m. articulo-transversalis longus
B E
C F
D
figure�.�� Schematicrepresentationofthem.spinaliscervico-capitiscomplex(A–D),them.cervico-spinalis(E),andthem.articulo-transversalislongus(F)inA. spinifera.
A
m. articulo-transversalis brevis
m. articulo-cruralis longus
m. intertransversalis
m. transverso-corporis
m. cervico-spinalis lateralis brevis dorsalis
m. epistropheo-squamosus ventralis
B E
C F
D
figure�.�� Schematicrepresentationofthem.articulo-transversalisbrevis,them.articulo-cruralislon-gus,them.intertransversalis,them.transverso-corporis,them.cervico-spinalislateralisbrevisdorsalis,andthem.epistropheo-squamosusventralisinA. spinifera.
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CervicalAnatomyandFunctioninTurtles ���
A
m. epistropheo-squamosus dorsalis
m. epistropheo-atlantis dorsalis
m. epistropheo-atlantis ventralis
m. atlanto-exoccipitis
m. atlanto-basioccipitis medialis
m. atlanto-opisthoticus
B E
C F
D
figure�.�� Schematicrepresentationofthem.epistropheo-squamosusdorsalis,them.epistropheo-atlan-tisdorsalisandventralis,them.atlanto-exoccipitis,them.atlanto-basioccipitismedialis,andthem.atlanto-opisthoticusinA.spinifera.
A
B m. epistropheo-odontoideus
m. cortico-cervicale I
m. cortico-cervicale II
m. cortico-cervicale III
C
D
figure�.�� Schematic representation of the m. epistropheo-odontoideus and the m. cortico-cervicalegroupinA. spinifera.
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��� BiologyofTurtles
m. spinalis cervico-capitis (cervico-hyo-capitis, Ogushi, 1913; Figure7.12). This is a largemusclethatconsistsoffourdistinctmusclebellies—thecaudahyoidea, thecaudasquamosi, thecaudaoccipitalis,andthecaudacornubranchialeII.Thecaudahyoidea(Figure7.12A)originatesattheneuralroofofC6,runsanteriorlyandmergeswiththefibersofthem.rectuscervicis.Thecaudasquamosi(Figure7.12B)partoriginatesattheneuralroofofC5,runscranially,andinsertsbymeansofabroadaponeurosisattheposterioraspectofthesquamosum.Thecaudaoccipitalis(Figure7.12C)originatesattheneuralroofofC4,runscranially,andinsertsontheexternalfas-ciacoveringtheexternaladductor.ThecaudacornubranchialeII(Figure7.12D)originatesattheneuralroofofC3,runscranially,andinsertsattheconnectivetissueassociatedwiththetipofthesecondceratobranchial.
m.cervico-spinalismedialis(Figure7.12E).Thisisasegmentallyarrangedmuscle.Themus-clesoriginatetendinouslyattheanterioraspectofthecristamedianaventralis,runanteriorly,andinserttendinouslyattheposterioraspectofthecristamedianaventralisofthethirdmorecraniallypositionedvertebra.ThemusclesoriginatingontheC2-C4mergeandinsertjointlyattheventralaspectofthebasioccipitalbymeansofawell-developedtendon.
m.cervico-spinalislateralislongi(Figure7.12&Figure7.13).Thisconsistsofthreelong,super-ficialmusclesthatoriginateatthelateralaspectofthezygapophysesofC5throughC8:
Them.articulo-transversalislongus(Figure7.12F)originatesonthelateralaspectofthepre-zygapophysesofthelastfivecranialvertebrae.Themusclerunscraniallyacrosstheventralaspectofthetwomorecraniallysituatedvertebraeandinsertsonthetransverseprocessofthefollowingvertebra.Them.articulo-transversalisbrevis (Figure7.13A)runsacross threevertebrae. Itorigi-natesatthedorsalaspectofthepre-zygapophysesandinsertsjointlywiththem.articulo-transversalislongus.Them.articulo-cruralislongus(Figure7.13B)originatestendinouslyatthedorsalaspectof thepre-zygapophyses, runscranially, and insertsdirectlyat thedorsal aspectof thepost-zygapophysesofthethirdmorecraniallypositionedvertebra.
mm.cervico-spinalislateralisbrevesventrales(Figure7.13).Thisconsistsoftwodistinctmus-clegroups,themorelaterallypositionedmm.intertransversales(Figure7.13C)andthemoremedi-allypositionedmm.transverso-corporis(Figure7.13D).Theformeroriginatestendinouslyatthetransverseprocess,runscranially,andinsertsdirectlyontheposterolateralaspectofthepre-zyg-apophysisandtheposterioraspectofthetransverseprocessofthemorecraniallysituatedvertebra.Them.transverso-corporisoriginatesontheventralaspectofthetransverseprocessandtheverte-bralbody,runscranially,andinsertsonthecondyleofthemorecraniallysituatedvertebra.
mm.cervico-spinalis lateralisbrevisdorsales(Figure7.13E).This isasegmentallyarrangedmusclerunningfromC7toC3.Eachsegmentconsistsoftwodistinctparts.Themedialpartorigi-natesatthelateralaspectofthecristalateralisofthepost-zygapophysisandinsertsatthedorsalaspectofthebaseofthepost-zygapophysesonthemorecraniallypositionedvertebra.Thelateralpartoriginatestendinouslyontheconnectivetissuesurroundingthezygapophysealarticulationandinsertsatthedorsolateralaspectofthepost-zygapophysisofthemorecraniallysituatedvertebra.
m.epistropheo-squamosusventralis (Figure7.13F).Themuscleoriginatesaponeuroticallyattheposterioraspectofthecristamedianaventralisoftheaxis.Themusclerunsanterodorsallytoinsertattheprocessusmastoideus(Ogushi,1913)ofthesquamosal.
m. epistropheo-squamosus dorsalis (Figure7.14A). This originates fleshy at the neural archandtheposterioraspectoftheneuralroofoftheaxis.Themusclerunsanteriorlyandinsertsattheprocessusmastoideusofthesquamosalandtheposterioredgeoftheopisthoticum.
m.epistropheo-atlantisdorsalis(Figure7.14B).Thisoriginatesattheanterioraspectoftheneu-ralarchoftheaxis.Themusclerunsanteriorlyandinsertstendinouslyattheprocessusarticularistransversalisventralisoftheatlas.
•
•
•
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CervicalAnatomyandFunctioninTurtles ���
m.epistropheo-atlantisventralis(Figure7.14C).Thisliesventraltothepreviousmuscle.Itorig-inatesfleshyatthelateralaspectoftheaxis,bothdorsalandventraltothetransverseprocess,andinsertsbymeansofashortaponeurosisattheprocessusarticularistransversalisoftheatlas.
m.atlanto-exoccipitis(Figure7.14D).Thisoriginatesatthetendinousinsertionofthem.rectuslateralisontheatlasandinsertsfleshyattheexoccipital.
m.atlanto-basioccipitismedialis(Figure7.14E).Thisoriginatesbymeansofashorttendonattheprocessusarticularisventralisoftheatlas.Themusclerunscraniallyanddivergestowarditsoriginonthebasioccipital.
m.atlanto-opisthoticus(Figure7.14F).Thisoriginatesatthedorsolateralaspectoftheatlasandinsertsatthedorsalsurfaceoftheopisthoticum.
m.epistropheo-odontoideus(Figure7.15A).Thisoriginatesatthelateralaspectoftheatlas,justdorsaltothecristamedianaventralis,andinsertsbymeansofanarrowtendonattheprocessusodontoideus.
m.cortico-cervicaleI(Figure7.15B).Thisoriginatesfleshyattheanteromedialaspectofthenuchalplateandinsertsmusculouslyatthelateralaspectofthepost-zygapophysisofC6.
m. cortico-cervicale II (Figure7.15C). This originates at the nuchal plate, just posterior totheoriginof them.cortico-cervicale I.Themuscle insertsfleshyat theneural roofofC6, justposteriortotheinsertionofthecaudahyoideaofthem.cervico-hyo-capitis.
m. cortico-cervicale III (Figure7.15D). This has adualorigin.The lateralpartof themuscleoriginatesatthelateralaspectoftheventralsideofthenuchalplatebymeansofanarrowandlongmuscularhead.Themedialheadoriginatesposteriortotheoriginofthem.cortico-cervicaleII.Bothheadsmergetowardtheoriginontheneural roofofC7, lateral to the insertionof them.cer-vico-spinalislateralisbrevisdorsalis.
m.spinalisdorso-lumbalis.Thissegmentallyarrangedmuscleispositionedinthecanaliscollateralisvertebralis(Vallois,1922).Theoriginispartlyontheinneraspectofthecanalandpartlyonthedorsalaspectofthecapitulumoftherib.Themuscleleavesthecanaliscollateralisver-tebralisrightposteriortotheribassociatedwithD1andinsertsdirectlyatthepost-zygapophysisofC8.
7.3.4 neckmovementS
NeckmovementsinChelodinaaredescribedindetailbyVanDammeetal.(1995,2002),Aertsetal.(2001),Weis-gram et al. (1992), and Van Damme and Aerts (1997).PreviouslyunpublishedinformationonneckmovementsinApaloneandChelodinaarepresentedhere.
�.�.�.� neckretractionandCer�icalmobilityinApalone ferox
Intheextendedconfiguration,jointsC9-8,C8-7,andC7-6showthelargestinitialangles.Themorecraniallyposi-tioned joints are all in the extended configuration. TheretractionoftheneckinApaloneischaracterizedbyrela-tivelysmallangularchangesinthefirstthree(C3-2,C2-1,andS-C1)andthelastcervicaljoint(C9-8).Thelargest
A
B
C
figure�.�� Static cineradiographsrecorded in dorso-ventral view, showingtheconfigurationofthecervicalvertebraein(A)fullyextended,(B)relaxed,and(C)fullyretractedpositionsof theneckinA. spinifera.
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��0 BiologyofTurtles
angularchangesduringretractionoccur in themiddleregionoftheneck.JointsC8-7andC7-6extendduringthecourseoftheretraction.ThesituationforjointsC6-5,C5-4,andC4-3ismorecomplex.C6-5initiallyflexesduringtheretrac-tionbutextendsagaintowardthelatterpartofneckretraction.Thetwomorecraniallysituatedjointsstartwithaninitiallyextendedconfigura-tion.Duringretraction,theangleofthesejointsgraduallyincreases.
The potential range of movement in thedorso-ventraldirectionisrelativelylargeinmostvertebral joints but largest in joints C8-7, C5-4, C4-3, and C3-2. However, joint angles dur-ingasimulatedsnorkelingmovementaremostpronouncedatthemostposteriorcervicaljoints(D1-C8,C8-7,andC7-6).Theanteriorjointsarekept relatively constant throughout the move-ments, as is observed during neck retraction(Figure7.16 and Figure7.17). Lateral mobility
oftheneckinA. spiniferaisalsosurprisinglyhigh,withthemoreproximaljointsbeingtheonesallowingmostmovement in thehorizontalplane. Incon-trast, thelastthreecervicaljointsallowalmostnolateralmovements.
�.�.�.� KinematicsofsnorkelinginC. longicollis
Neck movements during snorkeling in C. longicollis aremuch slower in comparison with those involved duringfeeding behavior (Aerts et al., 2001; Van Damme et al.,2002) and escape retraction (Van Damme et al., 1995).The total duration of a typical ventroflexion followed byadorsiflexionisabout6s.Eachcomponentofthemove-ment takes about 3 s. The representative example of asnorkeling movement in C. longicollis is represented bysuccessivestickdiagramsinFigure7.19.Startingfromanextendedconfigurationinwhichheadandneckareslightlydepressed, the animal initially balances its neck aroundthis configuration.This configuration is characterizedbyverysmall startingangles inall joints (withexceptionofD1-C8). Minor changes in joint angles occur during thefirstphaseofthemovementmainlyintheposteriorpartoftheneck(Figure7.20).Duringthisphase,noconspicuouschangesoftheelevationoftheheadandheadpositionareobserved. After approximately 3 s, a conspicuous, rathersteady increase in the elevation of the head is observed,mainlyasaresultofchangesintheangleofjointsC4-3toC7-6.InpatternsobservedinC8-7andD1-C8inthemostposteriorpartoftheneckandS-C1andC2-1inthemostanteriorpartoftheneck,changesinvertebral jointangle
A
B
figure�.�� (A) Static cineradio-graphs recorded in dorso-ventral viewillustratingthepositionandshapeofthecervical vertebrae inC. longicollis. (B)LateralviewofthecervicalsysteminC. longicollis during snorkeling. Note theradio-opaquemarkers insertedonto thecervicalvertebraetofacilitatetheanaly-sesofvertebralmovements.
A
B
C
figure�.�� CT-scan showing the configurationof the neck and the cervical vertebrae of A. spi-niferainfullyextended,relaxed,andfullyretractedpositions.
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CervicalAnatomyandFunctioninTurtles ���
appear less conspicuously related to the observed movements,showlessoverallchange,anddisplayagenerallymoreirregularmovementpattern.Atveryhighdegreesofelevation—atwhichalso head position is also starting to change—changes in jointanglearemainlyoccurringin jointsC5-4,C6-7,andespeciallyC4-3(morethan30°ofdorsiflexion).ThisisnotthecaseforC6-5.Thisjointreachesupto20°ofdorsiflexionandthenlevelsoff.Figure7.21illustratestheabsoluterangeofmovement(expressedin degrees of flexion) of each joint during the whole sequence.Notice therelativelyminor jointrotations in theanterior(S-C1,C2-1, andC3-2) andposterior parts (C8-7,D1-C8)of theneck.Asmentionedpreviously,themostconspicuouschangesinjointangleareobservedinthemiddlepartoftheneck,especiallyinjointsC4-3,C5-4,andC7-6.
In summary, the range of mobility in the vertical plane ofthecervical joints is limited,especially incomparisonwith thechangesofjointangleinthehorizontalplane.Dorsiflexionofthejoints is more conspicuous than ventroflexion. Ventroflexion inthe joints isnearlynon-existent.Thedominantchanges in jointangleareobservedinthemiddlepartoftheneck.
�.� disCussion
7.4.1 verteBrAlStructure
Thenatureofretractionofthehead-necksysteminturtles(intheverticalplaneasinApaloneorinthehorizontalplanasinChelo-dina)hasprofoundimplicationsonthemorphologyofthecervi-cal system.Although inboth species thecervicalvertebraearemarkedlyelongated,inChelodinathevertebraearerathernarrowand tall. However, in Apalone the situation is reversed and thevertebraearewideandrathershallow.AnothermarkeddifferenceisthepresenceofapronouncedventralvertebralcrestinChelo-dina.InApalone,thesecrestsareonlypresentinthemostanteriorvertebrae.The transverseprocesses that serveas insertion sitesforthemusclesofthelongissimusarewelldevelopedinChelodinaandarepositionedlaterallyattheborderbetweentheneuralroofandthevertebralcentrum.Becausethelongissimussystemisabsent inApalone, the transverseprocessesarepoorlydevelopedandpositionedmorecranially.Also,thestructureoftheposteriorzygapophysesismarkedlydifferentbetweenthetwospecies.WhereasinChelodinathereisonlyasinglebasalelementcarryingthetwohorizontallyorientedarticularfacets,inApalonetwoseparatepost-zygapophysesarepresent.Additionally,thearticularfacetsaremuchmorecurvedinApalonecomparedtothoseinChelodina.However,inbothspeciesthestructureofthezygapophyseslimitsventroflexionconsiderably.
7.4.2 cervIcAlmuSculAture
Thedifferencesinretractionmodeinthetwogroupsarealsoreflectedinthestructureanddifferen-tiationofthecervicalmusculature.Asmentionedpreviously,forexample,thelongissimussystemappearstobecompletelyabsentinApalone.Ashead-neckmovementstypicallyoccurintheverti-calplaneintheseanimals,thisisnotunexpected.Alternatively,inChelodinathelongissimussys-temisstronglydeveloped.Notableinthecryptodiresisthecortico-cervicalmuscularsystemthat
A
B
B ∆T = 0.25 sec.
A
C
Ventroflexion
Horizontal extension
Breathing
Carapace
Dire
ctio
n of
mov
emen
t
figure�.�� (A) Schematicillustration of the neck configu-rationinC. longicollis.(B)Stickdiagram representing an actualsnorkeling movement in C. longicollis.
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��� BiologyofTurtles
50
40
30
Deg
rees
20
10
0S-C1 C2-1 C3-2 C4-3
Joint
Absolute Range of Movement
C5-4 C6-5 C7-6 C8-7 D1-C8
figure�.�� MovementrangeofthecervicaljointsinC. longicollisintheverticalplane.
80 40
0 –40
40 20
0
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–10
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8 Head position
Elevation
S−C1
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t Ang
le (°
)
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figure�.�0 Kinematicplotsillustratingtimeprofilesofjointangle(dashedcurves,rightverticalaxis)andelevationanglewithrespecttothehorizontalofthemoredistalofthesegmentsconstitutingthejoint(solidcurve,leftverticalaxis)duringasnorkelingmovementinC. longicollis.Thefirstpanelrepresentselevationoftheheadsegmentandtherectilineardistance(rightaxisincm)betweenheadandcarapace.
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CervicalAnatomyandFunctioninTurtles ���
presumablyfunctionstoprotractandretracttheneck.PreliminaryelectromyographicdataforthecryptodireT. scripta elegans(VanDamme,unpublished)supportthishypothesis.InpleurodireslikeChelodina,thissystemisabsent.Ratherunexpectedly,them.sphinctercolliispoorlydevelopedinApalone.InChelodinaandmostotherpleurodires,thismuscleappearsmuchbetterdevelopedandmayactuallyplayaroleinaligningthecervicalmusclebundlesalongthecervicalcolumnduringneckmovements.However,thisremainsspeculativeandmustbetestedbyelectromyography.Also,thedominantheadretractormuscle,them.retrahenscapitisetcolliqueinChelodina(Shah,1963)andthem.carapace-basioccipitisinApalone(Ogushi,1913),isnotablydifferentinthetwospecies.InApalone,thismuscleconsistsofapairedmassivemusclebundlerunningfromthefirstcaudalvertebratothebackoftheskull.InChelodina,thismuscleismorecomplexandconsistsofseveraldiscretebundlesthatinsertonspecificsitesalongthecervicalcolumn.
However,astrikingsimilarityamongthetwogroupsistheextremelengthoftheheadretrac-tormuscle.Presumably,elongationoftheretractormuscleallowsformoresarcomerestobeplacedinseries,whichmayconsiderablyincreasethecontractionspeedofthemuscle(Josephson,1975).Moreover, by increasing the number of sarcomeres in series, each individual sarcomere has tocontract less and may thus potentially operate continuously on the plateau of its length-tensionrelationship.However,foranextremelyelongatedmuscletocontractefficiently,allpartsmustcon-tractsimultaneously.Thepolyneural,polysegmentalinnervationofthem.carapaco-basioccipitisin turtles (Guthe,1981)mayallowfor this.Unexpectedly, them.carapace-basioccipitisconsistsnotonlyoffasttwitchfibersbutalsohasaconsiderablepopulationoftonicfibers(Guthe,1981),whichmayhelpcontrolthepositionoftheheadandneckduringslowmovementsornear-stationarybehaviorssuchassnorkeling.
7.4.3 movementpAtternS
Thecranio-cervicalsysteminturtlescanbecharacterizedasanopenkinematicchainofeightver-tebraeandninejoints.Becauseeachjointtheoreticallyhasthreerotationaldegreesoffreedom(andtoalimitedextentalsothreetranslationaldegreesoffreedom),andbecausethepositioningofthevertebraemustbeachievedbythecombinedactionsofroughly50symmetricalmusclebundles,thecontrolofthepositionoftheheadinspaceobviouslypresentsachallengingcontrolproblem(Aertsetal.,2001).However,thecontrolofthesystemislargelysimplifiedbyanumberofmorphologicalconstraintslimitingthemobilityateachjoint.Forexample,inChelodinathehorizontalnatureofthezygapophysealarticularfacetsandtheverticalorientationofthearticularfacetsofthecondyleandthevertebralcentrumwillfacilitatemovementsinthehorizontalplane.Additionalsimplifica-tionofthecontroloftheneckinChelodinaisachievedbythepresenceofdistinctareasofrota-tionalongtheneck(VanDammeetal.,1995).Forinstance,thejointbetweencervicalvertebrae7and8andthejointsbetweencervicalvertebrae6-5and5-4typicallyshowthegreatestrangeofangularchange.Moreover, therestingpositionoftheneckischaracterizedbyadistinctbendattheselocations,facilitatingthecorrectretractionoftheneckusingonlyasimpleactivationofthem.retrahenscapitisetcollique(Aertsetal.,2001).Dorso-ventralmobilityisgreatestatthejointsC3-2throughC6-5.Thejointssurroundingthebi-convexarticularcentrumofC5showthegreatestangularchangeduringdorsiflexion.
ThecervicalsysteminApaloneisnotablydivergentandthekinematicpatternsarealsomark-edlydifferentfromthoseobservedinChelodina.Uponretractionoftheneck,themorecaudallypositionedvertebraearethefirsttostarttheirrotationaroundatransverseaxis.Theangularchangesin all vertebrae arenegativeduring retraction, suggesting that theneck is retractedas a safety-linked bicycle chain. Cervical vertebrae 5, 6, and 7 undergo an angular change of nearly 180°,whichimpliesthatthesevertebraeendupwiththeirventralaspectalongsidetheventralaspectoftheimmobiledorsalvertebrae.Thisismadepossiblebythenearlycompletereductionoftheventralcrestofthesevertebrae.ItisalsostrikingthatC8remainsinanear-verticalpositionatthemomentoffullprotraction.Themoreanteriorvertebrae(C1toC4)donotcontributetoneckretractionat
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all.Thebicycle-chain-likeretractionpatternobservedforApaloneisincontrasttotheretractionpatternssuggestedinothercryptodiressuchasTestudoorTrachemys(Scanlon,1982;Weisgram&Splechtna,1990).Inthelatterspecies,aswellasinChelodina,distinctrotationcentersarepresentwherethemajorityoftheangularrotationtakesplace.Thus,theextremelyelongatedneckandasso-ciatedmorphologyofApalonemaynotberepresentativeforthecryptodiranconditioningeneralbutprovideanexcellentexampleofahighlyspecializedcervicalsystemthatcanbecomparedtotheconditioninChelodina.Clearly,furtherinvestigationintothemorphologyandfunctionofthecervicalsysteminturtlesisneededtoincreaseourunderstandingoftheevolutionofthecervicalsystemanditscontrolinturtles.Especiallyinsightfulwouldbestudiesexploringcervicalstructureandfunctioninabroadersampleofturtlesincludingshort-neckedrepresentativesofbothcrypto-diresandpleurodires.Functionalapproachesincludingelectromyographyofthecervicalmuscles,albeitchallenging,areessentialtofurtherourunderstandingoftheevolutionofthecervicalsysteminturtles.
aCKnoWledgments
WethankA.DeSchepper(UniversityHospitalAntwerp)forallowingustousethecineradiographymachineandCTscanner;theAntwerpZooforprovidinguswiththespecimensofChelodina lon-gicollis;G.A.Wood(Wood,1982)forprovidinguswithasoftwarepackagefordatasmoothinganddifferentiation;andA.CuylitsformakingthedrawingsofthecervicalvertebraeinC. longicollis.ThisstudywassupportedbyIWONL-grant910091(JV)andFKFO-grant2.9005.90(FDV).AHisapostdoctoralfellowofthefundforscientificresearch,Flanders,Belgium(FWO-Vl).
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Aerts,P.,VanDamme,J.,andHerrel,A.,Intrinsicmechanicsandcontroloffastcraniocervicalmovementsinaquaticfeedingturtles,Am. Zool.,41(6),129–1310.2001.
Bojanus,L.H.,Anatome Testudinis Europaeae, Vol. 1.,Vilnae,Luthuania, republished in1970,FacsimilereprintsinHerpetology,no.26,SocietyfortheStudyofAmphibiansandReptiles,Ohio,1819.
Bojanus,L.H.,Anatome Testudinis Europaeae, Vol. 2.,Vilnae,Luthuania, republished in1970,FacsimilereprintsinHerpetology,no.26,SocietyfortheStudyofAmphibiansandReptiles,Ohio,1821.
Dalrymple,G.H.,IntraspecificvariationinthecranialfeedingmechanismofturtlesofthegenusTrionyx,J. Herpetol.,11,255–285,1977.
Deban,S.M.,Wake,D.B.,andRoth,G.,Salamanderwithaballistictongue,Nature,389,27–28.1997.Ernst,C.H.,andBarbour,R.W.,Turtles of the World,Washington,DC:SmithsonianInstitutionPress,1989.Gans,C.,Whydevelopaneck?,inThe Head-Neck Sensory Motor System,A.Berthoz,P.Vidal,andW.Graf
(eds.),NewYork:OxfordUniversityPress,1992,17–21.George,J.C.,andShah,R.V.,ThemyologyoftheheadandneckofthecommonIndianpondturtle,Lissemys
punctatagranosaSchoepff,J. Anim. Morph.,1,1–12,1954.George,J.C.,andShah,R.V.,ThemyologyoftheheadandneckoftheIndiantortoise,Testudo elegans,J.
Anim. Morph.Physiol.,2,1–13,1955.Guthe,K.F.,Reptilianmuscle:Finestructureandphysiologicalparameters,inBiology of the Reptilia, Vol 1,
C.GansandT.Parsons(eds.),NewYork:AcademicPress,1981,265–354.Heidweiller,J.,VanDerLeeuw,A.H.J.,andZweers,G.A.,Cervicalkinematicsduringdrinkingindeveloping
chickens,J.Exp. Zool.,262,135–153,1991.Herrel,A.,Meyers,J.J.,Nishikawa,K.C.,andAerts,P.,Themechanicsofpreyprehensioninchameleons,J.
Exp. Biol.,203,3255–3263,2000.Hofstetter,R.,andGasc,J.P.,Vertebraeandribsofmodernreptiles,inBiology of Reptilia, Vol. 1,C.Gansand
T.Parsons(ed.),NewYork:AcademicPress,1969,201–231.Irschick,D.J.,andGarland,T.Jr.,Integratingfunctionandecologyinstudiesofadaptation:Investigationsof
locomotorcapacityasamodelsystem,Ann. Rev. Ecol. System.,32,367–396,2001.Josephson,R.K.,Extensive and intensive factors determining theperformanceof striatedmuscle, J. Exp.
Biol.,194,135–154,1975.King,G.,Reptiles and Herbivory,London:Chapman&Hall,1996,160.
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Ogushi,K.,AnatomischeStudienander japanischendreikralligenLippenschildkröte (Trionyx japonicus):Muskelundperipheresnervensystem,Morph. Jb.,46,299–562,1913.
Pritchard,P.C.H.,Piscivoryinturtles,andevolutionofthelongneckedChelidae,Symp. Zool. Soc. Lond.,52,87–110,1984.
Romer,A.S.,andParsons,T.S.,The Vertebrate Body,Philadelphia:W.B.Saunders,1977,161–167.Scanlon,T.C.,AnatomyoftheneckoftheWesternPaintedturtle(Chrysemys picta belliGray;Reptilia,Tes-
tudinata),unpublisheddiss.,UniversityofMichigan,UniversityMicrofilmsInternational,1982.Shah,R.V.,TheneckmusculatureofaCryptodire(Deirochelys)andaPleurodire(Chelodina)compared,Bull.
Mus. Comp. Zool.,129,343–368,1963.Vaillant,M.L.,Mémoiresurladispositiondesvertebrescervicaleschezleschéloniens,Ann. Sci. Nat. Zool.
Paleont.,Ser.6,10,1–106,1881.Vallois,H.V.,Lestransformationsdelamusculaturedel’épisomechezlesvertébrés,Arch. Morph. Gen. Exp.,
13,180–217,1922.VanDamme,J.,andAerts,P.,KinematicsandfunctionalmorphologyinaquaticfeedinginAustraliansnake-
neckedturtles(Pleurodira;Chelodina),J. Morph.,233,113–125,1997.VanDamme,J.,Aerts,P.,andDeVree,F.,Kinematicsoftheescapeheadretractioninthecommonsnake-necked
turtle,Chelodina longicollis(Testudines:Pleurodira:Chelidae),Belg. J. Zool.,125,215–235,1995.VanDamme,J.,andAerts,P.,CervicalmovementsduringpreycaptureinAustraliansnakeneckedturtles,
genusChelodina(Pleurodira,Chelidae),inTopics in Functional and Ecological Vertebrate Morphol-ogy, A Tribute to Frits De Vree,P.Aerts,K.D’Août,A.Herrel,andR.VanDamme(eds.),ShakerPub-lishingBV,2002,77–94.
Weisgram,J.,andSplechtna,H.,Intervertebralmobilityintheneckoftwoturtlespecies(Testudo hermanni hermanni,Pelomedusa subrufa),Zool. Jb. Anat.,120,425–431,1990.
Weisgram,J.,andSplechtna,H.,CervicalmovementsduringfeedinginChelodina novaeguinaeae(Chelonia,Pleurodira).Zool. Jb. Anat.,122,331–337,1992.
Williams,E.E.,Variationandselectioninthecervicalcentrearticulationsoflivingturtles,Bull. Amer. Mus. Nat. Hist.,94(9),505–562,1950.
Wood,G.A.,Datasmoothinganddifferentiationproceduresinbiomechanics,inExercise and Sports Sciences Reviews,10,308–362,1982.
Wren,K.,Claussen,D.L.,andKurz,M.,Theeffectsofbodysizeandextrinsicmassonthelocomotionoftheornateboxturtle,Terrapene ornata,J. Herpetol.,32,144–150,1998.
Zani,P.A.,Gottschall,J.S.,andKram,R.,Gianttortoiseswalkwithoutinvertedpendulummechanical-energyexchange,J.Exp. Biol.,208,1489–1494,2005.
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���
8 FunctionalEvolutionofFeedingBehaviorinTurtles
Vincent Bels, Sabine Baussart, John Davenport, Marc Shorten, Ruth M. O’Riordan, Sabine Renous, and Julia L. Davenport
Contents
8.1 Introduction......................................................................................................................... 1878.2 Objective............................................................................................................................. 1888.3 FeedingStructures.............................................................................................................. 1898.4 OverviewofFeedingandDrinkingBehaviors................................................................... 1898.5 Kinematics.......................................................................................................................... 192
8.5.1 TerrestrialFeeding................................................................................................... 1928.5.1.1 Ingestion..................................................................................................... 1928.5.1.2 Intra-oralTransportCycle.......................................................................... 1958.5.1.3 Swallowing................................................................................................. 197
8.5.2 AquaticFeeding....................................................................................................... 1988.5.2.1 IngestionCycle........................................................................................... 1988.5.2.2 ManipulationandTransportCycle.............................................................204
8.5.3 FeedinginDermochelys coriacea:ATypicalExampleofaMarineTurtlewithaHighlySpecializedDiet........................................................................................2048.5.3.1 MaterialsandMethods...............................................................................2048.5.3.2 Results........................................................................................................204
8.6 EvolutionofFeedingBehaviorinTurtles...........................................................................2088.6.1 Ingestion...................................................................................................................2088.6.2 Transport(andOtherFeedingPhases).....................................................................208
Acknowledgments.......................................................................................................................... 210References...................................................................................................................................... 210
�.� introduCtion
Turtleshaveoneofthemostunusualbodyplansamongtheamniotes,withacarapacethatconstrainstheirbehavioralactivitiesdifferentlyfromallothertetrapods(Gaffney,1979;Reisz&Laurin,1991;Laurin&Reisz,1995;Lee,1997;Schafferetal.,1997;Poughetal.,2001;Cebras-Thomas,2005;Kear&Lee,2006;Shedlocketal.,2007).Althoughtheoriginandevolutionofthiscladeofverte-bratesisstilluncleardespitethoroughdiscussion(Joyce&Gauthier,2004;Hill,2005;Nagashimaetal.,2005),suchabodyplanappearstobeconservative.However,reductionoftheshellhasbeenreportedinrelationtochelonianlifestrategies,especiallyinaquaticturtles(Pritchard,1979).Evo-lutionarytransformationsofthelocomotorsysteminaquaticturtlesenablethemtodisplayhighlyadaptedmobilityandmaneuvering,presumablyforoptimizingsearchingforfood,sexualpartners,andareasforegglaying(Davenport&Clough,1986;Renous&Bels,1989;Wyneken,1997;Chap-ter5).Althoughsomeseaturtlepopulationsnestandfeedinthesamegeneralareas,others(speciesorpopulationswithinaspecies)canmigrateovergreatdistances.Leatherbackshaveprobablythe
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longestmigrationofallseaturtlesbecausetheycanbefoundmorethan7000kmfromtheirnestingbeaches(Hughesetal.,1998).
Despitetheir“armoredtank”shape,turtleshaveadoptedspecializedforagingandfeedingstrat-egiesderivedfromthoseofthestemreptilesthathaveprovidedenduringadvantageswhilesimulta-neouslyimposingbasicrestrictions.Thelivingspeciesofturtles,distributedamong99generaand14families(Ernst&Barbour,1989),inhabitalargenumberofvariousecologicalnichesinmarine,freshwater,andterrestrialhabitatsfromtemperateandtropicalregionsofallcontinentsexceptAnt-arctica,andinalloceans.Itiswellknownthatturtlesareeitherspecializedorgeneralizedintheirdiet,withpossibleontogenicdietaryshiftsbeingcommon(Pritchard,1979).Foragingandfeedingbehaviorshavebeengenerallydescribedforalmostallfamiliesofturtles(Pritchard,1979).Dietarypreferencesandontogenicchangesduringthelifecyclesofturtleshavebeenreportedinnumer-ousspecies,particularlyinmarineturtles.Mostcheloniansshowdietaryfluctuationsduringtheirlivesandcanshiftfromcarnivoroustoomnivorousandherbivorousdietsastheyage(Harless&Morloch,1979;McCauley&Bjorndal,1999;Bouchard&Bjorndal,2006).Briefly,trueterrestrialturtles(Testudinidae)aretheonlyspeciesabletoingestandswallowfoodonland,soaresubjecttothesameconstraintsasallothertrulyterrestrialvertebrates.Apartfromtheseturtles,alargenum-berofspeciesmakeforaysintoterrestrialhabitatsforfeedinganddrinking(e.g.,Emydidae).Someotherspeciesarewhollywater-feedersandchasetheirfoodbyusingvariousstrategiesfromactiveforagingtosit-and-waitpredatorbehavior(e.g.,softshells,Tryonichidae).Somespeciescancapturelivefoodonlandbutswallowitinwater.Severalherbivorousspecies(e.g.,Bataguridae)canfeedonplantmaterialatthesurfaceofthewaterorcandragterrestrialvegetationintothewater(Davenportetal.,1992).Somespeciescanfeedonlandorinwater,completingtheprocessfromfoodcapturetoswallowingineithermedium(e.g.,Terrapene carolina,Emydidae).Althoughbaskingonlandhasbeenreportedinafewcases,marineturtlesaregenerallyfoundonlandonlyintwosituations:whenadultfemalesreturntothelandforegglayingandwhenhatchlingsmusttravelfromthenestdownthebeachtothesea.Marineturtlesalwaysforageandfeedinthewater.
Aseriesofphylogeneticstudieshavedemonstratedsignificantrelationshipsbetweenvariouscharacteristicsofthetrophicsystemandcorrespondingecologicalspecializationsinsomegroupsof turtles (Gaffney, 1975, 1979; Claude et al., 2004). From these data, there have been severalhypothesesgenerated todemonstrate a relationshipbetween feedingperformancesand thephy-logenetichypotheses.Forexample,themorphologicalvariationofthesuperfamilyTestudinoidearelatestobothdietandhabitat(Claudeetal.,2004).Theseauthorssuggestthataspectsofthefeed-ingmode(e.g.,diet)canbeakeyfactorindeterminingmorphologicalevolutionanddiversificationofturtleskulls.Phylogenyappearstoconstrainonlylocalizedfeaturesoftheskullandremainsofminorinfluence.
�.� oBJeCtive
Therearesubstantialproblemsinprovidingacompleteoverviewofthefeedingbehaviorofturtlesusingaquaticandterrestrialhabitatsbasedonlyonpreviouslypublisheddata:kinematicandfunc-tionalanalysesofcompletefeedingmechanismsarerelativelyrare,andfeedingbehaviorhasbeenstudiedusingnon-standardizedmethodsandtechniques.Inhiscomprehensivevolumeofevolutionoffeedingbehaviorintetrapods,Schwenk(2000)providesanexhaustivelistofliteraturedescrib-ingfeedingbehaviorandmechanismsinturtles.Thepresentchapterprovidesthefirstcomparativeanalysisoffeedingbehaviorinturtles.Thoughaquaticfeedinghasbeenstudiedinseveralverydif-ferentrepresentativespeciesdrawnfromfreshwaterfamilies,fewdataareavailableconcerningthefeedingbehaviorofmarineturtlesorofterrestrialturtles.Consequently,thischapterwillnotonlyprovideinformationfromtheliteraturebutwillalsopresentdatacollectedbythechapter’sauthors,togetherwiththeiranalysesoffeedingbehaviorinterrestrialandaquaticspecies.Allofthesedataareconsideredfromacomparativeviewpoint.Whennecessary,arapidsurveyofthemethodsused
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forcollectingdataisprovidedforeachofthefeedingmodes,terrestrialandaquatic.Themecha-nismofneckmovementsthatplayakeyroleinfeedinginturtlesisdiscussedinChapter7.
�.� feedingstruCtures
Detailedanalyseshavebeenmadeoftheskull,hyobranchium,andtongueinturtles(Lindeman,2000;Schwenk,2000;Claudeetal.,2004).Whenneeded,weprovidemorphologicaldatathatarenecessary to explain the functional andbiomechanical aspectsof feedingbehavior.Some func-tionalanalysesdemonstratehowstructuresareusedinvariousphasesoffeedinginaquaticturtles(Schwenk,2000;Lemelletal.,2002).
�.� overvieWoffeedinganddrinKingBehaviors
Arapidsurveyoftheevolutionofturtlesandtheirdietshowthatturtlesusetwomainfeedingstrate-giestogainwater,energy,andnutrients:feeding/drinkingonlandandfeedinginwater.Drinkingwaterisaparticularproblemforterrestrialturtlesandforsometurtleslivinginsaline/marinehabi-tats.Alloftheseturtlesneedtodrinkwater(whenavailable)tomaintainthehydricbalancethatisessentialtowelfareandsurvival.Waterintakeratesandfrequenciesarehighlyvariableamongturtles.Forexample,somedesertturtlesareabletoconsumealargeamountofwaterinoneintake,therebyincreasingbodymassbyupto40%.Drinkinginaquaticturtleshasbeenrarelydescribed.Arecentstudydemonstratedthathatchlingseaturtlescanosmoregulateeffectivelyandgainmassbydrinkingseawater(Reinaetal.,2002).Althoughwellreportedintheliterature,drinkingbehav-iorhasbeenquantifiedonlyinMalaclemys terrapin(Davenport&Macedo,1990;Belsetal.,1995).Thisspeciesisabletomodulateitsdrinkingpostureinrelationtothewatersource;itcandrinkfromverythinfilmsoffreshwatereitherontheseasurfaceoronthesurfaceofintertidalmud,andcanevendrinkdirectlyfromfallingrainorfromwaterdropletsonvegetation(Davenport&Macedo,1990).Malaclemyscanalsoforciblyexpelwateroutofthebucco-pharyngealcavitywhendisturbedduringthedrinkingsequence,orwhenthevolumeofwaterwithinthiscavityistoogreat.Malaclemyscanexpelwaterveryquickly(lessthan1s)byasuddengapeincreaseaccompaniedbythroatelevationandneckretraction(Belsetal.,1995).
Asrecognizedforallvertebrates,feedingbehaviorinturtlesisamodal-action-pattern(MAD),involvingmovementsofthetrophicelementsintegratedwithneckdisplacements,sometimesasso-ciatedwithcomplexlimbmovements,sometimesnot.Allofthesecoordinatedsensori-motormove-mentsdefinethefeedingstrategyofturtles.Anyfooditemconsumedbyturtles(fromplantmaterialtofast-movingmobileprey)mustbelocatedandingestedbyarhythmicseriesofhead,jaw,andhyo-lingualmovements.Therearethreemajorsuccessivephasesinterrestrialturtles(Schwenk,2000):ingestion(capture),transportandintrabuccalmanipulation,andswallowing.Afourthphasecalledpharyngealpackingoccursattheendofseveralfeedingsequencesbutdoesnotinvolveanyjawopening-closingcyclicmovement(Figure8.1).Sincetheearliestfunctionalstudiesofvertebrates,acleardifferencehasbeendemonstratedbetweenfeedingstrategiesinwaterandonland(Liem,1990).Incompressiblewatercanbeusedtodriveamobilefooditem(livingprey)intothebuccalcavitybyproducingnegativepressureinsidethatcavity.Whenfoodiscaught,itmustbetransportedandswallowed.
Allfeedingphasesarebasedonrhythmiccoordinatedseriesofmovementsofthetrophicele-ments (e.g., jaws, tongue, hybranchium) associated with neck movements producing whole dis-placement of the head (Figure8.1). These movements are probably the result of rhythmic jawmovementsgeneratedbyacentralneuronalpopulationcalledthecentralpattern(orrhythm)gener-ator(CPG)(Schwenk,2000).Allrhythmicjawopening-closingactivitiesaremodulatedbysensoryfeedbackgeneratedbyvariousstructureswithin thebuccalcavity.Forexample, tastebudshavebeendescribedin thebuccalandtongueepitheliumofseveralspeciesof turtles(Iwasaki,1992,2002;Iwasakietal.,1996a,1996b,1996c,1996d;Beisseretal.,2001).Althoughalargenumberof
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studiesprovideinformationontheforagingbehaviorofturtles,noquantitativeanalysishasactu-allydemonstratedtheeffectoffoodproperties(i.e.,texture,volume,size)onthemodulationofthemovementsofthetrophicsystem(e.g.,jaws,tongue,andhyobranchium).Inthemajorityofstudies,turtleshavebeenfedinthelaboratoryonstandardizedpreyitems(e.g.,livefishaselusiveprey)orplantmaterial(e.g.,fruitsandlettuceitemsforterrestrialspecies,availableplantsforaquaticspe-cies)forherbivorousspecies.
Foraquaticturtlesmainlylivingonthesubstratum,huntingstrategiesusuallyinvolveimmobil-itywhileawaitingpreyproximitybeforestriking,ormovingslowlytowardtheprey.Forexample,averyslow(0.4cms-1)stalkingmotionisreportedinthehighlycamouflagedpleurodiranChelus fimbriatusthatmovestowarditspreyuntilthetipofthesnoutisclosetothepreyitself(Lemellet al., 2002).Lemell andWeisgram (1997)described the feeding sequence in the aquaticPelu-sios castaneuswhilecatchingpreyonthesubstratumbyassociatingmovementsoftheturtleandthe use of the trophic system. Lauder and Prendergast (1992) described a preparatory phase in
figure�.� SeriesofframesdepictingthesuccessiveeventsofatypicalfeedingsequenceinGeochelone radiataeatingapieceofgrape.(A)Ingestioncycle,(B)transportcycle,(C)swallowingorpharyngealpack-ing,and(D)pharyngealcompression.Foodingestionalwaysinvolvescontactbythetonguepriortosurround-ingbythejawsforgrasping.Foodingestionandtransportinvolverhythmiccyclicjawandtonguemovements.Intransport,theforwardmovementofthetongueismodulatedbythepositionofthefoodinthebuccalcavity.Inswallowing,themouthisopenedandthefoodmovedtowardthepharynx.Inpharyngealcompression,thejawsalwaysremainclosed.Thetimingofeachframeisprovidedinms(lastthreenumbersrecordedontheframes).
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FunctionalEvolutionofFeedingBehaviorinTurtles ���
Chelydra serpentinafeedingonvariouspreytypesthatconsistsofaslow,voluntarystalkingmove-mentwithlittlehorizontalbodyandneckmovementbeforeafastopeningofthemouthassociatedwithasuddenneckextension(seeChapter7).SlowstalkingmovementpriortomouthopeningwasalsoreportedinM. terrapineatingfoodonthesubstratum(Belsetal.,1998).
Fromafunctionalpointofview,itisratherdifficulttodeterminetheintegrationbetweenloco-motorandtrophicsystemsfortheseturtlesbecauseinthelaboratory,foodisoftenpresentedattooshortadistancefromtheheadtomeasurethekinematicandhydrodynamiccharacteristicsofthefeedingbehavior.However,itisclearthattheneuromotorintegrationbetweenbothsystemsplaysaparticularlykeyrolewhenturtlesarehuntinginthewatercolumn,orwhenthepreyitemsshowspecializedbehaviororphysical texture (e.g., shells inmollusksandcrustaceans).Manyaquaticturtlesmustassociatecomplexlimbmovementswithneckmovementsandrhythmicmovementsofthetrophicsystemtosupportthecomplexmaneuveringabilitythatimprovesfoodcapturesuc-cess(Figure8.2).DavenportandClough(1985)reportanapparentlyuniquefeedingbehaviorthatinvolvedtheuseoftheforeflipperstogainfoodinthemarineturtleCaretta caretta.Theseauthorsobservedtheroleof“pseudoclaws”(sharp-pointedscales)ontheproximalportionsoftheforelimbsofyoungspecimenstoallowthecombineduseofforeflippersandbeaktotearfooditemsthatareotherwisetoolargetobeswallowedwholeorreadilybittenintochunks(thusmimickingthefeedingbehavioroffreshwaterturtlessuchasemydidsthatusetrueclawsandthebeaktoachieveasimilargoal)andallowingfoodmorselsadheringtothepseudoclawstobeingestedbytheturtle.
Feedingbehaviorinthebrackish-wateremydidM. terrapinisthebestexamplecurrentlyavail-able in the literature todemonstrateplasticity inneuromotor integrationof limb,neck,and tro-phicsystemsduringpreycapture(Belsetal.,1998).Capturingimmobileprey(e.g.,mussels)on
figure�.� (continued)
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��� BiologyofTurtles
thesubstratumismainlyachievedbycoordinatedneckextensionandjawopeningwithrelativelysmallinertialsuction(VanDamme&Aerts,1997;seefollowingfordiscussion).Capturingmobileandaggressivelydefensiveprey in thewatercolumn(e.g., livingcrabs) requirescoordinationofneckextensionandjawopeningwiththelimbcyclesusedforswimming.Inallcases,theneckisextendedtoplacetheopeningjawsclosetothepreyduringlimbretraction,toincreasethethrustoftheturtletowardtheprey(Figure8.2).Anothersortofcoordinationoflimb,neck,andjawshasalsobeendescribed.BelsandRenous(1992)andBelsetal.(1998)demonstratedthatfeedingonsoft,slowlyswimmingprey(jellyfish)byyoungleatherbackturtlesalwaysinvolvesplacementofthelongforeflippersalongsidethebodyduringthecatchingcycles.Theysuggestthatthisstrategystronglydecreasesthepossibilityoflimbmovementsdisplacingjellyfishawayfromthebuccalcav-ity.Interrestrialhabitats,turtlesoftenapproachfoodslowlyandstopallmovementsbeforecaptur-ingthepreyorbitingtheplantmaterial.
Theuseofthelimbsinallotherfeedingphasesremainsrelativelypoorlyunderstood.Forturtlesfeedinginthewatercolumn(e.g.,Emydidae),thelimbsplayamajorruleinoptimizingfoodtrans-port(Belsetal.,1998);typically,theforelimbclawsareusedtotearlargefooditemsintosmallerpieces.However,forturtlesthatfeedinterrestrialhabitats,thelimbsonlyplayanoccasionalrolebystabilizingthepositionofafooditemonthesubstratumoraidingtheseizureof“difficult”hardfooditemsbetweenthejaws(e.g.,Testudinidaeeatinglivingpreysuchassnails).Alloftheseexamplesshowthatfunctionalstudiesmustbeecologicallyrelevant toyieldafullunderstandingof turtlefeedingstrategiesandtheirplasticitythatplaysakeyroleintheoverallfitnessoftheorganism.
�.� KinematiCs
8.5.1 terreStrIAlfeedIng
�.�.�.� ingestion
Twomodesof foodprehensionhavebeenreportedfor terrestrial turtles: lingualprehensionandjawprehension(Figure8.1&Figure8.3).AcleardifferenceiningestioncycleshasbeenreportedforTerrapenesp.feedingoninsectsandGeochelonesp.feedingonplantmaterial.T. carolinaandT. ornataneveruselingualprehensionbutonlyjawprehensionwhencatchinginsects(e.g.,Belsetal.,1997).Geochelonesp.andTestudosp.alwaysuselingualprehensionforfeedingonplantmaterial.Formobileprey (mealworms, asused inTerrapene studies),Kinixys alsouses lingualprehension.However,noquantitativecomparativeanalysesofthemodulatoryeffectsoffooditems
figure�.� TwotypicalfeedingsequencesofMalaclemysattackingadefendingcrab.Thesesequencesshowthecomplexinteractionbetweentheturtleandthelivingprey.However,imagesshowthestereotypedpatternofneckextension,gapecycle,andthroatdepressionforbothattemptstoingestpartsofthecrab.Thearrowshowsthejumpingbehaviorofthecrabattackingtheturtlethatdefendsbybiting(correspondingtoingestioncycle).
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FunctionalEvolutionofFeedingBehaviorinTurtles ���
onkinematicandmotorvariableshaveyetbeenreportedintheserepresentativetortoisesofTes-tudinidae.Incasesoflivingprey(e.g.,insects),onlyoneingestioncycleisusedtocatchthefoodanddrivethefooditemintothefrontofthebuccalcavity.InTerrapenesp.studiedwiththisfooditem,thejawmovesquicklyaroundthepreyandthetongueisneverusedforprehensionofinsects(Belsetal.,1997).Forplantmaterial,theingestion(capture)cycleismorecomplexanddependsonthesizeofthefooditembecausethefeedingboutisacontinuousprocessthatdoesnotterminateatoneparticularphase.Twoexamplesdemonstratethiscomplexity.Forrelativelylargefooditemssuchasgrapes,G. radiatacontactsthefoodwiththetongueandretractsthefooditemwithinthebuccalcavitywhilethejawsaremovingaroundthefood.Theturtleusuallyusesonetothreeinges-tioncyclestobringthefoodmaterialsuccessfullyintoitsbuccalcavity.SimilarbehaviorhasbeenreportedfortheherbivorouslizardUromastixfedonendive(Herreletal.,2002).TheG. radiatahead is thenplaced in an approximatelyhorizontal positionduring the immediately subsequentcycles,allowingtransportandintrabuccalmanipulation;for“long”fooditemssuchaslettuceleavesthataredrawnintothemouthbyrhythmicjawcycles,thefooditemsarecaughtbythetongueandthejawsmovethepieceoffoodaroundseveraltimesbeforethefoodpartlyorcompletelyentersthebuccalcavity.Itisratherdifficulttoseparatefoodingestionandtransportbecauseateachtonguecycle(Figure8.1andFigure8.3),thefoodwithinthebuccalcavityismovedbythemidandposte-riorportionsofthetonguewhiletheforetonguemovestoadheretothepartsofthefooditemthatarestilloutsideofthebuccalcavity.Whenapieceoffoodiscutoff,theturtlecanstoptoingesttherestofthefooditem,whichcontinuestobeactedupononlybytransportcycles.Suchacontinuous
figure�.� SeriesofframesdepictingthesuccessiveeventsofatypicalfeedingsequenceinKinixys bel-lianaeatingapieceoflettuce:(A)ingestioncycleand(B)transportcycle.Foodprehensiondoesnotinvolvecontactbythetongueoutsidethebuccalcavity.Foodtransportinvolvesrhythmiccyclicjawandtonguemove-ment.Contactbetweentongueandfoodoccurswithinthebuccalcavity.Intransport,theforwardmovementofthetonguethatplaysthekeyroleismodulatedbythepositionofthefoodinthebuccalcavity.Thetimingofeachframeisprovidedinms(lastthreenumbersrecordedontheframes).
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��� BiologyofTurtles
processofingestion-transportisstronglyinfluencedbythesizeofthefoodmaterial.Whenashortpieceoflettuceisprovidedtoturtles,onlyoneortwoingestioncyclesareusedtodealwiththefood.Theeffectofthesizeofthefooditemonthecontinuousprocessinvolvingtheforetonguetocatchthefooditemandthemid-andhindtongueportionsfortransportingthefoodhasbeenclearlydem-onstratedinallherbivorousmammalsfeedingonlongpiecesofhay(Bels,2006),sothisprocessisnotunusualinvertebrates.AssoonasthefoodiswithinthebuccalcavityofG. radiata,aseriesofintegratedhead(neck),jaw,andhyolingualcyclestermedtransport-intrabuccalmanipulationmovethefoodposteriorlytowardthepharynx.Attheendofacompletesequence,cyclesdeterminingtheswallowingphasetypicallyshowadifferentgapeprofileashasbeennotedinherbivorouslizards(Herrel&DeVree,1999).
Inbothmodesoffoodprehension,turtlesalwaysusecombinedmovementofthejaws,thehead,andtheneckthatmayormaynotbeassociatedwithdisplacementsofthehyolingualapparatus.Allingestioncyclesinallterrestrialturtlesareaccompaniedbyneckextension,movingtheopeningjawstowardthefooditem(Figure8.4).Duringthenextextension,theheadispositionedrelativetothefooditemdependingonthepropertiesofthefoodanditsproximalcues(i.e.,size,volume,texture,mobility),showingacomplexsensory-motormechanismcontrollingtheinitiationofthisfeedingphase.Ateachingestioncycle,theturtlerotatestheheadinvariouspositionstobeabletotakeholdoftheplantmaterial.Thesensory-motormechanismsunderlyingsuchfunctionalplastic-ityduringingestionremainunderstudied.Interrestrialturtles,thequestionofpositioningtheheadtogetherwithaneckextensionremainsanopenquestion.Probablydifferencesinthespeedofheadmovementstowardthefoodarekeyparametersthatpermitthesereptilestomodulateheadrotationduringfoodingestion.Thisdifferencecanbeseenasafunctionalconsequenceofdietselectioninterrestrialturtles.
Twomaintypesofingestioncycleshavebeenreported:jawprehensionandlingualprehension.Inbothmodesoffoodprehension,turtlesalwaysusecombinedmovementsofthejaws,thehead,andtheneck,associatedornotwithdisplacementsofthehyolingualapparatus.Inallprehension,themouthisopenedinslow(SO)andfast(FO)stages(Figure8.4).However,thedurationofSOstageisvariable.InT. carolinaandT. ornata,acleardistinctionbetweenSOandFOstagewasnotalwayseasytodeterminebecausethegapeincreasesratherregularly,andoftenthemeandurationofFOstageislongerthanthatofthefastclosing(FC)stage.ThetonguealwaysmovesforwardwithinthebuccalcavityduringgapeincreasesandretractsduringthebeginningoftheFOstage.Uponprotrusion,thetonguebulgesandthetonguetipcurvesventrally,sothattheforetonguemakescontactwiththefooditem.DuringtheSOphase,thetongueisprotrudedfromthemouthandcon-tactsthefood.Next,thetonguecontinuestobeextendedandpushedagainstthefooditem.Thefoodisthenmaintainedincontactwiththetonguebecauseofstrongmucousadhesionbetweenthetonguesurfaceandthefood.Oncethetonguehasbeenretractedwithinthejawmargins,thejawsareclosedquickly,andtheslowclosing/powerstrokephasestarted.ThemeandurationoftheFOstageislongerthanthatoftheFCstage.Duringthedecreaseingapesize,thelowerjawarrivesunderthebeakformedbytheupperjawsasintransportcycles.Thetonguemovesforwardwhilethegapeincreasesandcontactsthefoodbeforemaximalgapeisachieved.RetractionofthetongueoccursduringthebeginningoftheFOstage.Afterclosingthejawsontheprey,theheadretractsand rotates in reverse.TimingofkinematiceventsofG. elephantopus (lingualprehension)andT. carolina(jawprehension)issimilarinthesedifferentspecies(Figure8.4).Forexample,peakhyoidretractionoccurs justafterpeakgapeangleandmaximumthroatdepressionoccurs30 to100msaftermaximumgapeangle.Thesuccessivesixeventsinbothturtlescanbesummarizedasfollows:
NeckextensiontodrivetheheadtowardthefoodOpeningofthemouth(SOandFOstages)RetractionofthetongueduringthebeginningoftheFOstageDepressionofthethroatimmediatelyfollowingthetongueretraction
••••
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FunctionalEvolutionofFeedingBehaviorinTurtles ���
ClosingofthemouthonthefoodRetractionoftheheadtowardthecarapace.
�.�.�.� intra-oraltransportCycle
Assoonasthefood(e.g.,livingprey,plantmaterial)entersthebuccalcavity,transportofthefoodtowardthepharynxbegins.Forexample,afteringestionofamealworm,thepreyisnotcompletelyheldwithin thebuccalcavityand is reduced(i.e.,partiallycrushed)by the jawmarginsateachtransportcycle(Figure8.3andFigure8.5).Becausethemealwormentersthebuccalcavitypro-gressively,successiveportionsofthemealwormarereducedattheclosingstageofeachtransportcycle.
TheslowopeningofthemouthduringtransportiscomposedoftheSOI(opening)andoftenSOII(stationarystage)stages.TheFOstagecorrespondstoarapidincreaseintheverticaldisplace-mentofthejaws(Figure8.5).TheFOstagebeginsafteraslightdecreaseingapeangleattheend
••
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figure�.� (A)Meangapeprofile (±standarddeviation) from10 lateral ingestioncycles inonespeci-menofGeocheloneelephantopus.Thearrowindicatesthemeantimeoftongueretraction.(B)ComparisonbetweentimingeventsinG.elephantopusandT. carolina(datafromBelsetal.,1997).Timingswerecalcu-latedfromthetimetopeakgapeangle(time0).Gapeisdividedintoslowopening(SO),fastopening(FO),fastclosing(FC),andslowclosing(SC).TBNE:timetobeginningoftheneckextension,TMNE:timetomaximalneckextensionduringingestioncycle,TTOR:timetotongueretraction,TBTD:timetobeginningofthroatdepression,TMTD:timetomaximumthroatdepression.
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��� BiologyofTurtles
ofSOstage.Theclosureofthemouthisdividedintofastclosing(FC)andslowclosing(SC)stages.TheFCstagecorrespondstoarapiddecreaseintheverticaldisplacementofthejaws.TheSCstagecorrespondstotheelevationofthelowerjawunderthebeakoftheupperjaw.Thehorizontaldis-tancebetweenthetipoftheupperjawandlowerjawdecreasesduringtheFCstagebecauseverticaldisplacementofthelowerjawproducesanarc,andtheupperjawmoveslittle.TheSCstageisnotreflectedinrecordablegapeangleandgapeverticaldistancechangesbecausethelowerjawmovesundertheedgesoftheupperjaw.However,duringthisstagethehorizontaldistancebetweenthetipoftheupperjawandthemostanteriorpointofthelowerjawincreasesjustafterFCstageinthegapecycle,indicatingthatthelowerjawcontinuestocloseagainsttheupperjaw.WhengapeincreasesduringtheSOstageofthenextcycle,thishorizontaldistancedecreasesagain.
Inthetransportcycle,duringtheSOstagethetongueisprotractedasillustratedbyadecreaseofthehorizontaldistancebetweenthetipsofthetongueandthelowerjaw(Figure8.3BandFig-ure8.5).Atthesametime,thetongueisslightlyelevated.Inthetransportcycle,theforwarddis-placementofthetongueintothebuccalcavityisstronglycorrelatedwiththeverticaldisplacementofthelowerjawduringtheSOstage.Whenthetonguemovesforward, thelowerjawdepresses
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figure�.� KinematicprofilesoftwosuccessiveintraoralfoodtransportcyclesinG. elephantopus.Throatverticalmovement(TH)associatedwithtongueretractionshowsthecyclicdepressionandelevationofthethroat.Headmovementtowardthefoodwasmeasuredbythehorizontaldisplacementoftheeye(EY).Thismovementshowsthecyclicdisplacementofthejawstowardthefoodassociatedwithgapeangle(GA)pro-ducedbycombinationofverticalmovementoftheupper(UJ)andlower(LJ)jaws.Thearrowsindicatethefirstframeoftongueretractionwiththefoodadheringtothetonguesurfaceandthelineindicatespeakgapeangleforeachofthegapecycles.
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FunctionalEvolutionofFeedingBehaviorinTurtles ���
(SOI),andwhenthetongueisstationarypriortomovingbackwardduringtheFOstage,thelowerjawdoesnotmoveandthegapeangleremainsstationary(SOII).TheheadextendsduringtheFOstageandthebeginningoftheFCstage,anddepressesduringtheSO,FO,andthebeginningofFCstages.DuringhalfofthedurationoftheSOstage,theheadrotatesdownwardasshowedbytheverticaldisplacementofthehead.Preliminaryanalysisoffoodtransportbyusingx-rayvideo(250Hz)inatypicalplantfeedingturtle,K. belliana,showsthatthefoodisaccumulatedwithinthepharynxandtherearpartof thebuccalcavity(Figure8.6).Subsequently,swallowingofthealimentarybolusbegins.
�.�.�.� swallowing
AccordingtoSchwenk(2000),wecandivideswallowinginterrestrialturtlesintopharyngealpack-ing(openingofmouth)andpharyngealcompression(nogapecycle).Figure8.3andFigure8.6showtypicalswallowingcycle in twoT. carolina (Figure8.3)andK. belliana (Figure8.6)feedingondifferentfooditems(mealwormsinT. carolinaandlettuceleavesinK. belliana).Probablybasedonthesensory-motorfeedbacksfrompropertiesofthealimentarybolus(i.e.,volume,size,tough-ness),theturtleeitherentersintoanewfeedingsequencethatdrivesmorefoodintothepharynx,
figure�.� (A)TypicalingestioncycleofapieceoflettuceinK. bellianafilmedbyx-rayvideofluoroscopy(100Hz),showingthetonguecontactingthefoodwhereasthejawsmovedtosurroundthefoodmaterial(leafoflettuce).Thecontactbetweenthetongueandthefoodoccurswithinthebuccalcavityattime0.(B)Typicalswallowingcyclefilmedbyx-rayfluoroscopy(200Hz)involvingmouthopeningtoshowthecombinedmove-mentofthefoodassociatedwiththeswallowingcycle,demonstratingthekeyroleofthetongueandthroatintheposteriordisplacementofthefoodtowardtheesophagus.Peristalticactivityoftheesophagushelpingmovementofthefoodwithintheesophagusisalsoshown.Thedisplacementofthefoodalongpharyngealpackingisshownbythearrowoneachframe.Time0correspondsforthiscycletothefirstframeofmouthopening.f:markers(thelettucewascoveredwithathinfilmofwaterchargedwithbariumpowder).
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��� BiologyofTurtles
ormovesthebolusintotheesophagus,whichstructuredrivesthebolusdirectlytothestomachbyperistalticmovement.Foremptyingthepharynx,theturtlesproduceeitherjawcyclesorpharyngealcompression(Figure8.6).
8.5.2 AquAtIcfeedIng
Feeding in aquatic turtles has received more attention than that of terrestrial turtles, althoughrelativelyfewspecieshavebeenstudied.However,robustexperimentalconditionswithmore-or-lesssimilarenvironmentalconstraintshavebeenemployed.SincethefirstquantitativeanalysisoffeedingmechanisminChelydra(Lauder&Prendergast,1992),turtleshavebeenusedfortestinghypothesesandgeneralizationsregardingmorphologicalandfunctionalpatternsassociatedwithaquaticfeedinginlowervertebrates.
Thelargenumberofspeciesandforagingstrategiesinaquatic-feedingturtlesprobablyreflectsaratheruniquegroupofvertebratesthathasevolvedaquaticfeedingconvergentlywithanamniotefeedingsystemsandwithamniotesthathavereturnedsecondarilytoaquaticenvironmentsuchasseveralmammals.Manyfoodresourcescanbeexploitedinaquatichabitats.Plantmaterialconsti-tutesafirstsourceoffood.Thismaterialcanbefirmlyattachedtothesubstrateandmustbebittenandextractedorpulledoutbeforebeingtransportedandswallowed.Otherplantmaterialcanbefloatingandmustbebittenandcaughtfrombeneath(Davenportetal.,1992).Livingpreycanbeexploitedbyrapidstrikesiftheyhaveelusiveabilities(e.g.,fishes)ormustbeapproachedslowlytoavoidtheirmovementawayofthebuccalcavity(e.g.,jellyfish).Sincetheearliestanalysesoffeed-ingmechanismsinwater,thequestionofimportanceofsuctionhasremainedparamount(Aertsetal.,2001;Figure8.7).
�.�.�.� ingestionCycle
Aquaticturtlesallshowmuchthesamepatternofhead,jaws,andhyobranchiummovements.Toourknowledge,thetongueisnotusedforcapturingaquaticprey.Typicalcapturecyclesforsomeaquaticturtles(C. longicollis,C. fimbriatus,C. serpentina)involveasuddenforwardthrustoftheheadbyneckextension(seeChapter7).Incontrast,otherspeciesstrikelessrapidly(meandurationbetween250and300msinM. terrapin,Belsetal.,1998;400msinT. carolina,Summersetal.,1998;andupto800msinD. coriacea,thischapter),openingthemoutheitherbyusingSOandFOstagesorregularlywithouttheSOstage.Allkinematicprofilesavailableintheliteratureprovideclassicalexamplesofneckextensionproducingasuddenthrustoftheopeningmouthassociatedwithlargedepressionofthehyobranchium.Depressionofthehyobranchiumoccurs30to50msaftermaximumgape(Lauder&Prendergast,1992;Bels&Renous,1992;VanDamme&Aerts,1997;Belsetal.,1998;Summersetal.,1998;Lemelletal.,2002).
Theproblemofapproaching the food inaquaticenvironmentalwaysremains thesame:anyflow of water produced by the turtle must be compensated for in efficient capture. Lauder andPrendergast (1992)werethefirst tostress thehydrodynamicconstraintsonaquaticpreycaptureresultinginkinematicsimilaritiesamongpredatorssuchasfish,amphibians,andturtles.Theirfind-ingsweresupportedbyotheranalysesofingestioninturtlesfromfreshwaterandmarinehabitats.Alloftheaquaticturtlescangenerateabackwardwaterflowrelativetothebuccalcavity(calledsuction)toacquirethefood(VanDamme&Aerts,1997).VanDammeandAerts(1997)discussedindepththequestionofcompensatoryandinertialsuctioninpreycapturebyaquaticturtles.Theterm“compensatorysuction”indicatessuctionusedtomaintainfoodimmobileduringthestrike,andpermitsengulfingofthefoodasthejawapparatussurroundsit.Theterm“inertialsuction”isusedtodescribesuctioninwhichfoodandwatermovetowardthebuccalcavitywhereastheheadofthepredatorremainsessentiallyimmobile(VanDamme&Aerts,1997;Aertsetal.,2001).Aertsetal.(2001)statethatprobablyfoodcaptureinvariousaquaticturtlesisrelatedtoacombinationof both modes of suction, as demonstrated by displacements of various food items recorded indifferentaquaticturtles.Forexample,inertialsuctionplaysamajorroleinChelodina longicollis
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FunctionalEvolutionofFeedingBehaviorinTurtles ���
butcompensatorysuctionisdominantinC. serpentina(VanDamme&Aerts,1997).VanDammeandAerts(1997)andSummersetal.(1998)donotagreewiththeuseoftheram/suctionindex(RSI)proposedbyNortonandBrainerd (1993) todescribe the feedingmechanismsoffishes. In theirrecentstudy,Lemelletal.(2002)appliedthisindextocaptureofbyC. fimbriatus.TheequationforRSIis
CBI
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figure�.� (A) Drawings of lateral and ventral views of the strike used for illustrating the kinematicprofiles.(B–D)KinematicprofilesofonerepresentativestrikeinChelodina longicollistoshow(B)themodi-ficationofareasofcrosssectionsthroughthreesuccessivelevelsontheheadoftheturtle(VanDamme&Aerts,1997):themouth(gape)andatthelevelofceratobranchialI(CBI)andII(CBII),thedisplacement,oftheprey,thehead,andthecarapaceoftheturtleintheearthboundframeofreference(ebfr=fixedframeofreference).Timescaleisgiveninmsandnumbersoftheuppertimescalecorrespondtothenumberofthesequencespresentedattheleftofthefigure.(ModifiedfromVanDamme&Aerts,1997.)
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�00 BiologyofTurtles
RS I =
D - D
D + Dpredator prey
predator prey
where Dpredator and Dprey are the net distances moved by the predator and the prey between themomentthemouthfirstbeginstoopenandthemomentthepreydisappearsorisseizedbythejaws).RSIrangesfrom+1,indicatingapureramstrikeinwhichonlythepredatormoves,to−1,indicatingapuresuctionstrikeinwhichonlythepreymoves.ThecalculatedRSIduringprey(fish)captureinP. castaneusvariesbetween0.36and0.55,andinC. fimbriatuswasalwayspositive(mean=0.36±0.23,range=0.071to0.664;prey=fish;N=20).However,theseauthorsthinkthattheequationusedforRSItendstooverestimatetheramcomponent.
Whatever the terms used for describing food capture (e.g., suction, RSI), and whatever thehydrodynamic calculationsor other considerations involved, all aquatic turtlesmust expand theoropharyngealcavityforsuccessfulfoodcapture.Summersetal.(1998)demonstrateclearlythatpreycaptureinwaterinvolvesgreaterhyoiddepressioninT. carolinafeedinginwatercomparedwithfeedingonland.TheseauthorsandBelsetal.(1998)showthathyoiddepressionismodulatednotonlyfromlandtowaterbutalsoinwaterfeedinginrelationtofoodtypeandbehavior(e.g.,crabscapableofdefensivebehavior).Itisevidentthatthisexpansionplaysakeyroleinthesuc-cessfulcaptureofelusivepreybyanymodeofpreydisplacementtowardthebuccalcavity(inertialsuction)orofmaintainingthepreyimmobileinthewatercolumn(compensatorysuction).Aertsetal.(2001)suggestthatfunctionaldemandsrelatedtofeedinginwateralwaysrelatetoexpansionoftheareaposteriortothejawapparatusthatopenstoallowpreyandwatertoenterpartlyorcom-pletelyintotheoropharyngealcavity.However,theroleofthisexpansionbecomeslessimportantinturtlesfeedinguponplantmaterialfloatingatthesurface,pullingmaterialoutofthesubstratum,orattackingavigorouslydefendingprey.Inthelattercase,bitingperformancebythejawsprobablyplaysthekeyrolebecauseitallowstheturtletoobtainfoodandalsodefendagainsttheattackoftheself-protectingpotentialprey(Herreletal.,2002).Despitelargestructuralvariations,theexpansionoftheoropharyngealcavityismainlyproducedbymovementofthehyobranchiumasnicelydem-onstratedbyx-rayfilms(Aertsetal.,2001;Lemelletal.,2002).ForillustratingthemotorcontrolofthroatexpansioninChelonida,fewdataareavailable.Aertsetal.(2001)providedthefirstdescrip-tionofmotorsequencesthatshowdepressionandretractionofthehyoidbody(Figure8.8).Lemelletal.(2002)reportthattheesophagusisfilledwiththelargeamountofwatersuckedinduringthegapecycleuntilthemouthisclosed.Theseauthorsprovideacompletex-rayanalysisofpreymove-mentwithinthebucco-pharyngealcavity(Figure8.9).Inallturtles,thepreyiseithersuckedinward(inertialsuction)orbittenbyclosingjaws(compensatorysuction).Inthemeantime,thethroatislaterallyexpandedbyrotationof lateralelements (ceratobranchials I)of thehyobranchium.Thedisplacementof theelementsof thehyoidapparatushasalwaysbeenassumedtoproducethroatexpansioninallstudiedaquaticturtles(Lemell&Weisgram,1997;VanDamme&Aerts,1997;Lemelletal.,2002),andnowthereisclearconfirmatoryevidence.Theposteriorpartofthethroatisexpandedbyrotationoftheposteriorlateralelementsofthehyobranchium(cetarobranchialsII;VanDamme&Aerts,1997;Lemelletal.,2002).Themouthisthenagainopenedslightlytoexpeltheexcesswaterbyreturningthehyoidapparatustoitsstartingposition,andthepreyisretainedonthefloorofthebuccalcavity.
Allmajordataonfoodingestioninaquaticturtleshavebeencollectedinenvironmentalcondi-tions(e.g.,temperature,salinity)closetotheclassicalrelevantecologicalconditionsdeterminedforthestudiedspecies.Forexample,Belsetal.(1998)recordedfeedingbehaviorinM. terrapinat25°Cinwaterwithsalinityof33psu.Leatherbackturtleswerefilmedat26°Cinclassicalartificialsea-water(Bels&Renous,1992).However,performancesinturtles(asinallreptiles)canbemodulatedinrelationshiptotemperature.Itwouldbeexpectedinectothermicturtlesthatspeedsofjawactionwouldincreasewithhighertemperatureswithinthephysiologicalrangeofaspecies,andviceversa.
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FunctionalEvolutionofFeedingBehaviorinTurtles �0�
Giventhedifferentthermalconditionsoftheirnaturalranges,wecomparedgapeperformancesofthreeaquaticspecies(Figure8.10).Inthisstudy,itwasnecessarytostudyjawactionatarangeofrealistic temperatures foreachspecies.Datawereobtained forTrachemys (Emydidae)at18,24and30°C.Cuora(Emydidae)andSiebenrockiella(Bataguridae)wouldnotfeedat18°C;theywerefilmedat24,28,and30°C(threespecimensofeachspecieswereheldovernightformorethan14hoursateachstudytemperaturebeforebeingfilmed).Figure8.3andFigure8.4respectivelyshowtheeffectsoftemperatureonbitetime(i.e.,timetocontactfood)andjawopeningtime(i.e.,timetomaximumgape)foradultsofallthreespecies.ItisevidentthatthetwoemydidspecieswerebothlessaffectedbytemperaturechangesthanSiebenrockiella,whichshowedasteepdeclineinbitetimeandjawopeningtimebetween24and30°C(at24and30°C,one-wayANOVAcomparisonsamongthethreespeciesrevealedhighlysignificantdifferences,p<0.005).Trachemysshowednochangeinbitetimeandjawopeningbetween24and30°C;evenat18°Ctherewasrelativelylittleslowingofjawactionincomparisonwith30°C(bitetimeby24%,jawopeningtimeby55%).TukeyposthoctestsshowedthatTrachemyswassignificantlyfaster(shorterbite/jawopeningtimes)thanCuoraatcommontemperatures(24and30°C;p<0.05inallcases)andalsosignificantlyfaster(p<0.05)thanSiebenrockiellaat24butnotat30°C.Dataforbitetimeweremorevariablethanforjawopeningtime;thispossiblyreflectsvariationinfoodmorselsizeandthepositioningofthejawsrelativetofoodduringjawclosure.Jawopeningtimeappearstobemoreusefulforcomparisonsandissolelypresentedfortherestoftheresults.Differencesbetweenthetwoemydidspecieswereparticularlymarked,withjawopeningtimebeing227%longerinCuorathaninTrachemysat24°C,and200%longerat30°C;clearly,TrachemysbitesfarfasterthanitsAsianrelative.
These resultsprovide thefirst relevant functionaldata toexplain the roleof feedingperfor-mancesinthesuccessofinvasionofTrachymysturtlesthroughouttheaquatichabitatsoftheworld.
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figure�.� (A) Schematic representation of the head skeleton of C. longicollis in the adducted andexpandedconfigurations.(B)ResultsofelectromyographicalanalysisduringexpansionofthehyobranchiuminC. longicollis(fromAertsetal.,2001).ThegraphrepresentsthechangeofthecrosssectionalsurfaceoftheoropharyngealcavityatthelevelofthegapeandthroughthethroatatthelevelofceratobranchialsIandII.Arrowsindicatepositionandorientationof themajorexpansionmuscles.CB1:ceratobranchialI;CB2:ceratobranchialII;mBH:m.branchiohyoideus;mBM:m.branchiomandibularis;mCH:m.coracohyoideus;mDM:m.depressormandibulae;mIC:m.intercornuatus.,exp.:throatexpansion(Aertsetal.,2001).
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�0� BiologyofTurtles
Wedemonstrate too that the invasiveTrachemys bites faster over awide rangeof temperaturesrelativetothetwoAsianspecies(Cuora,Siebenrockiella)whosehabitatitnowshares.Thissug-geststhatitcandealmoreeffectivelywithelusiveordangerouspreyaswellasfeedingoncarrionorvegetationmorequickly.ThethermaldataalsoindicatethatTrachemysiscapableofeffectivefeedingoverawidertemperaturerangethanthetwonativespecies,allowingittocontinuefeed-ingundercoolerconditions.Theintroductionofanomnivorous,highlyeffectivecompetitortoanecosystemisclearlyundesirable,butthesituationismadeworsebytheunusualcharacteristicsof
figure�.� Successiveframesofahigh-speedx-rayfilmsequence(150frames/s)showingalateralviewofC. fimbriatusduringfoodcapture.Thetime(s:ms)isprovidedforeachframe.Thepreyitemappearsdarkbecauseofthex-raycontrastmedium.Leadmarkerswerealsopositionedontheskulloftheturtle.(FromLemelletal.,2002.)
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FunctionalEvolutionofFeedingBehaviorinTurtles �0�
Trachemysintroductions.Mostinvasivespeciesdonotbecomeestablishedinnewhabitatsbecausetheyfailtoreproduce,ordonothaveimmunitytopathogenspresentintheirnewhabitat.WhereasferalTrachemyshavebeenshowntobreedinJapan,Israel,Germany,andFrance(Ernstetal.,1994;Cadietal.,2004),thegreatbulkoftheirnumbersinAsia(aselsewhere)stemfromrepeatedandcontinuinglarge-scaleintroductions.Tosomeextent,theirabilitytobreed/notbreedisirrelevant,particularlyas theyareverylonglived,oftensurviving30+years inthewild(Kuhrt&Dewey,2002).AccordingtotheTurtleConservationFund(2002),Asiais“thegeographicregionthatwar-rantsthehighestpriorityifwearetoavoidlosing[chelonian]speciesinthenearfuture.”Theresultsofourcomparativebiomechanicalstudyprovidefurtherindicationofthenecessityfortrappingandremovingthishighlycompetitiveintroducedturtlefromnon-nativeecosystems.
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figure�.�0 (A)Examplesofgapeanglesequencesinthethreestudyspeciesat30°C.Thebodymassesofthethreespecimensfilmedwereasfollows:Trachemys(492g),Siebenrockiella(701g),andCuora(1041g).(B)Effectoftemperatureonbitetimes(timetocontactwithfood)inadultTrachemys,Cuora,andSieberocki-ella.Symbolsrepresentmeanvalues(n=3)andstandarddeviations.(C)Effectoftemperatureonjawopen-ingtimes(timetomaximumgape)inadultTrachemys,Cuora,andSieberockiella.Symbolsrepresentmeanvalues(n=3)andstandarddeviations.
3339.indb 203 11/26/07 12:09:36 PM
�0� BiologyofTurtles
�.�.�.� manipulationandtransportCycle
Although poorly analyzed, transport of thefood is more complex because it involves twomaintypesofuseofbothelementsofthehyo-branchium: the tongue and the hyoid appara-tus.InM. terrapin,thetongueplaysakeyrolein manipulating food in association with thedepression of the hyobranchium (Figure8.11).For transporting the food, the tongue is alsoclearly associated with classical depression ofthe hyobranchium in helping backward dis-placementofthefoodwithintheoropharyngealcavity.Inotherspecies,thefoodcanbesuckedinwithout any actionof the tongue.Basedondifferences in movement of the hyobranchiuminC. fimbriatus,Lemelletal.(2002)describedtwo modes of transport cycles involving slowsuction effects on the prey within the buccalcavity(Figure8.12).Inthefirstmode,thehyoidis depressed slightly and the mouth is openenoughtofacilitatethereleaseofthepreyfromthejaws,withthefishbeingheldattheendoftheceratobranchials.Inthesecondmode,hyoiddepressionisofthesameextentasduringpreycapture.Thevolumeoftheanteriorpartoftheesophagusincreasesslowlyandthepreyisheldbetweentheceratobranchials.Theturtleexpelsthewater very slowly and theprey remains attheendofthehyoidapparatus.
8.5.3 feedIngInDermochelys coriacea:AtypIcAlexAmpleofAmArIneturtlewIthAhIghlySpecIAlIzeddIet
�.�.�.� materialsandmethods
Fouryoungleatherbackturtles(80to500g)havebeenfilmedat200to300Hzusing16mmfilms.TheturtlesfromFrenchGuianawereincubatedat30.5°Candkeptinanaquariumof2.3to5.0m3at25°Cinseawater(pH=8.0to8.1;salinity=32g/l).Theanimalswerefilmedunder500Wwhenfedwithcrudemussels(Belsetal.,1988).Thefoodwaspresentedgentlyinfrontoftheturtles.Onlytruelateralsequenceswerekeptfortheanalysisusingthetypicalmethoddetailedpreviously(Belsetal.,1998)andpointsweredigitizedtocomparemovementsofthejaws,thehyobranchium,andthelimbsduringthesuccessivephasesofthefeedingbehavior(Figure8.12andFigure8.13).
8.5.3.2reSultS
FeedingboutsinD. coriaceaconsistofsuccessivejawandhyolingualcyclesfrompreycapturetoitstransportintotheesophagus.Duringthefeedingbouts,theturtlesstabilizethebodybyslowdisplacementsoftheforelimbsthatarenotrelatedtothesuccessivegapeopenings.Twotypesofjawcycleswereobserved: ingestion (includingbitingof the smoothmaterial that is cut at eachcycle)andtransportcycles.Wedidnotrecordanyspecificswallowingcycleswiththetypeofsoft
figure�.�� Typical stages of food (entire mus-sel)manipulationinM. terrapin.Thetongueplaysamajorroleinmovingfoodfromonesideofthejawsto the other. The food is partially crushed at eachclosingofthejaws.Timebetweenframes:0.08s.
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FunctionalEvolutionofFeedingBehaviorinTurtles �0�
foodusedinthisstudy(piecesofmusselflesh).Insuccessiveingestioncycles,thefoodentersthe
buccalcavityandisreducedbetweentheclosingjaws.However,insomeoftheseingestioncycles,
transportalsooccurswhenthefoodismaintainedinfrontoftheturtles.Intruetransportcycles
(Schwenk,2000),thefoodistakencompletelyintothebuccalcavityandthenmovesposteriorlyto
theesophaguswithoutanyreductionbetweenthejaws.However,thefoodmaybereducedbetween
thehardpalateand the tongue.Suchreductionandbitingcyclesproducesmallparticulatemat-
terthatisejectedfromthemouthduringtheslowopeningofthenextjawcycle.Throatelevation
duringthetimebetweenthetwoFOstagesofsuccessivecyclesproducedmovementofwater(and
particulatematter)outofthebuccalcavity(Figure8.13).
figure�.�� Successiveframesofahigh-speedx-rayfilmsequence(150frames/s)showingalateralviewofC. fimbriatusduringfoodtransport.Thetime(s:ms)isprovidedforeachframe.Thepreyitemappearsdarkbecauseofthex-raycontrastmedium.Leadmarkerswerealsopositionedontheskulloftheturtle(figurefromLemelletal.,2002).
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�0� BiologyofTurtles
Kinematically,eachgapecycleofthebitingandtransportphasesinvolvesaslowopening(SO),fastopening(FO),andclosingstage(C).TheSOstageofbothcycle types ishighlyvariable indurationandamplitude.Insomecycles,itinvolvesa“stationarystage”(SOII)priortothesuddenincreaseoftheFOstage;inothers,itdoesnot.TheSOstagemaybealsocompletelyabsentinsomecycles.Fromhigh-speedcinematographicfilms, itwasnotpossible to recordclear relationshipsbetween thepresenceanddurationof thisSOstage,with thecycle functionor the tongue-foodposition.ThemeandurationofSOstageinbitingcyclewassignificantlylongerthanofSOstageinthetransportcycle(Kruskall-WallisANOVA,T=4.7;df=18;P<0.05),whereasFOandCstageswerenotsignificantlydifferent.
Themouthisopenedbyacombinationofventraldepressionofthelowerjawanddorsaleleva-tionoftheupperjaw.Typically,thehyoid-tonguedisplacementsarenotdifferentiningestionandtransportcycles.DuringtheSOstageandthefirsthalfoftheFOstage,thehyoid-tonguecomplex
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figure�.�� Successiveframesshowing(A)ingestionand(B)transportcyclesinD. coriacea(high-speed16-mmfilmsat100Hz).Thegapeisdividedinslowopening(SO),fastopening(FO),andclosing(C)stages—thedivisioninfastclosing(FC)andslowclosing(SC)stageswasnotalwaysclearduringtheingestioncycle.Inertialsuctionplaysakeyroleinbothfeedingphases.Thedurationoftheingestioncycleis0.22s(22frames)andthedurationofthetransportcycleis0.16s(16frames).Thenumbersindicatedateachdrawingcorrespondtothenumberofframesrelativetothetotalnumberofthecycle.TimetopeakgapeisindicatedbyGA.Con-tactbetweenthefoodandthetonguewasalwaysobservedandtongueretractswiththefoodasthethroatisdepressed.TO:tongue.
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FunctionalEvolutionofFeedingBehaviorinTurtles �0�
iselevatedandprotractedasillustratedbydecreasingofthethroatangle.ThedistancebetweenthemandibleandthehyoidbodyvisiblethroughthethroatskindecreasesstronglyduringSOstageandis0.07±0.01spriortomaximalgapeamplitude(endofFOstage).Thethroatexpansionthenoccursduring0.14±0.05sattheendofFOandFCstages.IncasesofastationarystagepriortoaSOstageorveryslowopeningstage, thehyoid-tonguedistancedoesnotchangegreatlypriordecreasing.Therewasnosignificantdifferencebetweendisplacementsofthehyoidpointonthethroatduringbitingandtransportcycles(Figure8.14).
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figure�.�� KinematicprofilesofingestionandtransportcyclesinD. coriaceafeedingonsoftmaterial(piecesofmussels)withpropertiesclose to thematerialcaught in thenaturalenvironment (jellyfish).Wecategorizeingestioncyclesasallcyclesusedformovingfoodintothebuccalcavity,andtransportcyclesasallcyclesthattakeplacewithfoodinsidethebuccalcavity.Gapecyclesinbothphasesaredividedintoslowopening(SO),fastopening(FO),andfastclosing(FC).Divisionbetweenclosinginfastclosing(FC)andslowclosing(SC)isnotyetclear.However,attheendoftheclosingstagetheangularaccelerationofthegapeangledecreasesslightly.Thekinematicprofilesillustratingthethroatdisplacementfollowasimilarpatternduringbitingandtransportcycles.ThethroatdistancesIandIIwerecalculatedasthedistancecorrespondingtothelinetracedfromonepointonthethroattothehorizontallinepassingthroughtheedgeofthemandibleateachframeatanangleof90°.ThethroatdistanceIcorrespondstothehyoidbodyandthethroatdistanceIItotheregionoftheceratobranchialsI.DuringtheSOandfirsthalfoftheFOstagesofeachcycle,thethroatdis-tanceIiselevated0.01sbeforethethroatdistanceII(posterior).Retractionofthehyoid-tonguesystembeginsduringtheFOstageandoccursduringtheclosingstage.Peakhyoidretractionbeginswithorjustbefore(0.01s)fastclosing.Thehyoidapparatusismaximallyretracteduntilthefastclosing(FC)isachieved.TheneckdistancewascalculatedasthedistancebetweenpointNE(endoftheskull)andCA(carapace).
3339.indb 207 11/26/07 12:09:44 PM
�0� BiologyofTurtles
DuringSOandFOstages,watermovesintothebuccalcavitysimultaneouslyasthepreythatmoveseithertothebuccalcavity(biting)orposteriorlyintothebuccalcavity(transport).Anaddi-tionalinertialsuctionmechanismhelpsdisplacepreytowardthepharyngealcavity;thisismainlyproducedbytongueretractioninbitingandtransportcycles.Strongcontactsbetweenpreysurfaceandtonguedorsalsurfacewereobservedinbothcycles.
�.� evolutionoffeedingBehaviorinturtles
Discussionofevolutionoffeedingbehaviorinturtlesremainscontroversial.BasedontheirstudyofpreycaptureinT. carolina,Summersetal.(1998)statethat“thecurrentlyacceptedhypothesisisthattheancestortorecentturtleswasterrestrial(Gaffneyetal.,1987),butthatanaquaticlifestyleevolvedearlyinthehistoryofthecladeandisprobablyprimitiveforallextantturtles(Gaffneyetal.,1987,1991;Carroll,1988).”Theseauthorsconcludedthatterrestrialfeedinginturtlesisaderivedbehavior(Belsetal.,1997;Summersetal.,1998).Hereweprovidesomediscussionthathighlightstheneedforfuturequantitativekinematicandmotoranalysesinterrestrialandaquaticturtles.
8.6.1 IngeStIon
Terrestrialfeedingmodesincludelingualandjawprehension.Bothmodesareusedforvariousfooditems.ExceptinTerrapene(Belsetal.,1997;Summersetal.,1998;Bels,2003),lingualprehensionisthemainmodeforallstudiedturtlesoftheTestudinidae.Thefoodadherestothetongueeitherin(e.g.,Kinixys)orout(e.g.,Geochelone)ofthebuccalcavity.Summersetal.(1998)suggestthatT. carolinausesaterrestrialfeedingmodeinwaterbecausethevelocitiesofallskullelementsduringfoodcapturebygeneralistsareslowerthanthoseofspecialists.Fromavailabledata,threehypoth-esescanbesuggested.First,theingestioncyclehasbeenderivedinthe“true”terrestrialcheloni-ans(i.e.,Testudinidae)showingatongue-basedintraoralfeedingbehaviorfromfoodtransportandreductiontoswallowing.Ingestioncanbeviewedasanevolutionarytransformationofatongue-basedfeedingmechanismforefficientprocurementoffood.Thecoordinationofthetonguemove-menthasnotchangedgreatly,withthetonguemovingslightlytowardthefoodduringjawopeningandretractingthefoodaftercontact;alternatively,thejawapparatuscansimplysurroundthefooditemandthetonguemakescontactwiththefoodwithinthebuccalcavitypriortobeingretracted.Second,bothmodesofprehension(lingualandjawprehensions)werepresentinancestorsofturtlesandcanbeusedinvariouswaysdeterminedbythepropertiesofthefood.Suchmodulationinfoodprehensionhasbeenreportedforsquamates(Schwenk,2000).Third,terrestrialturtlesderivedfromaquaticancestorshave“reinvented”thekeyroleofthetongueforimprovingefficiencyoffoodpro-curementtogetherwiththeirconquestofterrestrialhabitats.Inthiscase,wemustadmitthatlingualprehensionisaderivedpatternconstrainedbythepropertiesofthefoodresourcesbecomingavail-ableduringtheevolutionofterrestrialturtles.InTerrapene,whichbelongstoaprimitivelyaquaticclade,terrestrialfeedingisasecondarilyderivedmodeinwhichthejawprehensionthatplaysakeyroleinaquaticfeedinghasbeenconserved.Summersetal.(1998)suggestthatT. carolinawouldusetongueprehensiononpreythatislargerthanmealworms.WehavenotyetconfirmedthissuggestionbyexaminingprehensionofvarioustypesoffoodinTerrapene(Bels,personalobservation).
8.6.2 trAnSport(AndotherfeedIngphASeS)
Theevolutionoffeedingbehaviorandmotorcontrolofturtlesstillremainsdifficulttofullyunder-stand.First,theoriginofturtlescontinuestobelargelyproblematic.Second,onlyafewspecieshavebeenextensivelystudied,mainlyintermsoffeedingmechanismsandnotfromanevolution-aryperspective.However,availabledatacanprovidesomeinsight,particularlywithrespecttothelikelihoodofsomepossiblehypothesesconcerningtheevolutionoffeedingbehaviorinchelonians.
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FunctionalEvolutionofFeedingBehaviorinTurtles �0�
Acomparativeanalysisofallfeedingphases—exceptfoodcapture—appearsinteresting.LauderandGillis(1997)comparedtransportkinematicsandmechanismsoftrulyaquaticvertebrates(e.g.,fishesandamphibians),firstwiththoseofamphibiansthatfeedinbothterrestrialandaquatichabi-tats,andsecondwiththoseoftrulyterrestrialAmniota(e.g.,squamates).Theysuggestthatseveraltraitsrecordedforsquamatesarenovelfeaturesofthefeedingmechanismthatappearedwiththeconquest of terrestrial habitats and can therefore be considered as plesiomorphic for tetrapods.Thesetraits includediversityofintraoralprocessing,thepresenceofaSOstagepriortosuddengapeincrease(FOstage),andhyoidandtongueprotractionduringSOproducedbyauniquepatternofhyoidmusclecontraction(Lauder&Gillis,1997).Thesesuggestionsagreewiththeevolution-aryapproach to feedingbehaviorproposedbyReillyandLauder (1990),whoadvocatea singlegeneralizedmodeloffoodtransportintetrapods.Morerecently,McBrayerandReilly(2002)donotsupportallthefeaturesofBrambleandWake’s(1985)generalmodel(i.e.,presenceofSOIandSOIIinslowopening).Thesetwomodelshavebeenproposedtodescribethegeneralizedgapepatternandtonguemovementduringfoodtransportinterrestrialvertebrates.Basedonavailabledatain1985,BrambleandWake(1985)presentedahypotheticalgeneralizedmodelforancestraltetrapodswithgapebeingdividedintoslowopening(SO),fastopening(FO),fastclosing(FC),andslowclos-ing(SC-PS)stages.BeforeFO,thegapeincreaseisdividedintoslowopeningI(SOI)involving“acomparativelylowgapeangle”(Bramble&Wake,1985)whilethetongueslidesbeneaththefoodandaslowopeningII(SOII),that“isrecognizedbyadistinctdeclineintherateofchangeofgape”(Bramble&Wake,1985).Thislatterstageisrepresentedinthemodelbyaplateauinthegapecycle.ThenduringFO,thefoodismovedposteriorlybyactionofthetongue.AfterFO,themouthclosesrapidly(FC)andthenmoreslowlyasthejawscontactthepreyduringSC-PSstages.
Reilly and Lauder (1990) proposed another generalized model for amniotes. These authorsdividetheincreasingstageofthegapecycle(openingofthemouth)onlyintoslowopening(SO)andfastopening(FO),withnoSOIIstage.Thisdifferenceingapeincreaseishighlysignificantbecauseitemphasizesadifferenceintonguemovementduringtransportingofthefood—seeMcBrayer&Reilly(2002)foradiscussionbasedonquantitativedatainalargesetofsquamates.AccordingtoLee(1997),thedevelopmentoftheshellandratherflattenedbodyofturtlescouldbelinkedtoanancestralherbivorousdiet.Itmaybeassumedthatancestralformswereterrestrialandfedonplantmaterial(andperhapssmall,slowlymovingpreyorcarrion),asisthecaseforalargenumberofextantspeciesstudiedtodate(e.g.,Geochelonesp.,Kinixyssp.).Basedonthishypothesis,wemayconcludethatavailabledatasupporttheconclusionthatthecharacteristicsoftransportcyclesareplesiomorphicforterrestrialfeedinginturtles,althoughthereisalargevarietyindietandspecial-izationofthehyobranchium,yieldingthepresenceofaSOstagebeforeFOofthemouth,amove-mentofthetongueunderthefoodduringtheSO,andretractionofthefoodbythetongueatSO-FOtransitionoratthebeginningofSOstage.
Intheirquantitativeanalysis,Belsetal.(1997)comparedtheirdatainterrestrialfeedingbyT.carolinawiththetwopreviouslydescribedgeneralizedmodelsfortetrapods.Availabledatadonotpermitcategoricalconclusions.However,arapidsurveyofkinematicsfacilitatesthecomparisonofaquaticandterrestrialtransportphases.Inallturtles,withalltypesoffood,thejawcycleisoftendividedintoSO,FO,andclosingstages.TheSOstageisalwayspresentinallterrestrialturtles.Thisstagehasalsobeenreportedinalargenumberofaquaticturtles(P.castaneus,Lemell&Weisgram,1997;T. carolina,Belsetal.,1997;Summersetal.,1998;M.terrapin,Belsetal.,1998;D. coria-cea,Belsetal.,1998;C. frimbriatus,Lemelletal.,2002).Wesuggestthatthereisanintra-oraltransportcyclethatissimilarforallterrestrialturtles.Itisalsoevidentthatthetongueisusedinalargenumberofaquaticturtlestotransportfooditems,justasinterrestrialturtles.ItsprotractionoccursduringtheSOstageanditretractswiththefoodattheboundarybetweenSOandFOstagesorearlyduringFOstage.Wemaycallthismechanismintra-oral aquatic lingual transport.Incon-trast,suctionplaysthedominantrolefortransportingfoodinsomespeciessuchasC. fimbriatus(Lemelletal.,2002).Wemaycallthismechanismintra-oral aquatic hyoid transport.Probably,therelativesizeofthetongueisthelimitingmorphologicalfactorindetermininguseoftongue-based
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��0 BiologyofTurtles
intra-oraltransportorhyoid-basedintra-oraltransport.Theslowlyopeningmouthcangeneratelowpressurewithinthemouthcavitybecauseofprotractionofthehyoidduringthisstageinbothcases.However,thisisrapidlycompensatedforbysuctionthatoccursduringthroatexpansionaftermaxi-mumgape.DuringtheFOstages,rapidmouthopeningisimmediatelyfollowedbyaposteroventralmovementofthehyoidapparatus;highnegativepressureoccurswithintheoropharyngealcavity,whichisproducedbypeakhyoiddepressionfollowingpeakgapeinallstudiedturtles.DuringtheFCphase,thehyoidapparatusremainsdepresseduntilthemouthisclosed.
aCKnoWledgments
Theauthorsthankallthosewhohelpedtogatherthedatausedinthispaper.TheyareverygratefultoS.Attereforherhelpinwritingthispaper,andtopersonsfordiscussionandhelpinvariouspartsofthiswork(G.Daghfous,S.Montuelle).Wethanktwoanonymousreviewersfortheirhelpfulcomments.
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