Evidence for Endothermic Ancestors of Crocodiles at the Stem of Archosaur Evolution
linger S. Seyniblir1 ln(roduc; Far- ARSTRAU ■. i ■ i ; ; . . ijc i N ,s lj i, Physiolrtpi-i:aI, atffttiwniilal, .nui deirloprtjcntiil fcaturifi uT lhe Om- line nil evidence concerns ihe relationship behveen cn- eriichiJEifitt heart Support the paleontological evid en t- lhai lhe dorheritiy, nier.bliihli^- riHe, and a lour-chambered he-art. I.oris aUceattt'r* o f living oraicodilians Wr're attivr and iridbther'ciic, S. Russell (WftSi.i and pussibly olliL'i:. be (ti re him, recogjiis^il hin il v i U’dgi inverted I ■ i ■.■■' rv when t IttViadsd lhe rIi.tI the four chambered bcarl of archosaurs |>iTl’eclly separates aquatic, ambush pr^tJjiKjr niche. lij endoiherms, I here is j func oxygenated and dcoxypeiiidcd bloods, which should optimj.SL tional nexus between high metabolic rates, high Wiftttd flow gas tir:insport by sending only dvnvygenated blood to lhe lunLj fatcj* and complete ‘Uipafatlttfl o f high sysienik bl.Oiid pressure and OKyycrn.ilcd blood to ibr bckJy. VVchb (1979) dre^' from low pulmonary blood pressure in .l four-chambered heart, attention lo lhe significance nf ilk’ I'our-chiimliered heart and KcfOltwrris generally U d .ill o| ihtse diaracifristiis, bill ctDt- elevated aclivUv in the ancestors !ifhiri.ls ,ind crocodiles. The iidilians main a tb ur-chambered heart However, crocodilian* inicreucf il I hnl lii^liei mi'taboliL rj^es of eudm herins would have a neurally prmtrtjiJLcd, pulmonary bypass shunt that is1 selecl for 11 if perfect separalum of blooi.^. This aiy.umenl was funetjonal in diving. Shunting occurs outside of the head ajid used in io tn t^tn jn with the discovery til the dispmed fij)si) involve1) the left aortic arch rhiil originates froifi tbo right ven fi^ur chambeieil Iumti in an ornirhin. bian ('.inos'aiu' [Hslicr el tricle. lhe foramen of Paniz/a between the lift and right aortic iii. 2WU,. Flowevci, despite an anatomic id l.y incomplete sepa ration n I the chaml^ers of noncrocodiliau re|p|ili,m hearts, vnnc arches, and lhe <.og-Louth valve .it the base or the pulmoii.uy snakes and lizards are able to reduce ntfjmig to almost zero artery. Pevelopmejital siudies. show that all of these oniquely (Jiitlts iy^&). This, shou-s that a lour chambertd lie.irt is nipt crocodilian tea In res are secondarily derived, indicating a shift tiu. - -a y m e!. lu s ,-a ■ onds. from 1)kl complete separation o f blood ftniv of endotherms to We believe thai the prfntHry mloof the four-tltambercd heart Lhe controlled shom ing of cctijtherms. We present other evi- is ht separate systemic and pulmonary blood pressures, rather ■j:ii ■ :’uren ithtr;in; m .■ ■ ;■ ar Unuii rsatiflti.igpL-.Trl . .m- i ban itisl blood osygenalion stales, lo achieve liigh metabolic dinosaur:, inay brtve inherited the trj.il. ralc,s. endotherm.s fi'iiorre a greater CLH'diovasi'oia: ittid b|.tyl(>di ZJinihi, Heart mass j vet aye', ahiut tL4%-(f,7% of bo.dy mtiss in rnanimals .uid 1.2% in biftK iPnupa an cl -fn i.Jstadal l^fiL'; Uisliop tV?7; Seymour and Blttyloek ^itOCIj, bui *—+ ■ WjrTTTTU*£ __ | “ ii is ojily [).Iyl>ij—0.32'N/ in nujfil repuies (Pttupa and I mdstrom 19k3; Seymi^ur 1%’7; Farrell et al. lWfi]. In alligators, heart ma-A titvieases from 11.2 :!% at I body mass to U. 13% at 70 ] 1 . ul tj 1 r ; : ,l i H ■ i ■ ■ . :'t :d. I:v^ The level of syt.lemic arterial bleiod prt'ssnri' is iciated imt HuifriTnnry only to metabolic r,itr and heart si?.e but also Io the of the animal, Nlore specifically, iiiiliongh all ot the heart’s energy is ' ■ ■ .1 4 uliiinaiely lost to frictional rcsisiante ii' the circulation, one Ij, !■ ■■■! ■■ ‘i • i .. Ri ii 111 I i ’ , innni'diale reL|uirement ot central Hyyi-irrUc arterial blood pres sure Is to mjiport the vertical blood toltmin abr>ve the heart Figure 1. SvsKlnii' ^rtf.rini him id pmnjri.‘s ill ftl.ltlfifl In m^v-tfK{rpiif. Urnl suruidrj liieMlhilk rate among vcrleiirak' Quill's i^:, are (Seymour el jl, 1993). Tlllvrflgujjifrif'Trt cxpisifii why the giraffe mptfwatul 95% Loiifidence intervals. Ln fiik amrpWhliilii, repnles, Ifii-iis, has an arterial blood pressure jbnui twice the m;nitmali.in norm and m.irtinub, lj|txnJ pressure it based nn 2.1, t>, 15, l~, .lnd species. lHarwns 1VS7) and why ai ferial blood pressure increases sig retpiwtlviHy; metailwlic rale is hnsi'ii on K. H>. fiV, 1^8, nlid M'J spotlrX, nificant I v in larger mammals (Sfymour and Rlavlock ’ (1001 find 1 espetI nv!y, than tile literature. (Tie ringe nl ItuJmfo)^rv .irterdl bliasif lunger lerfestrial snakes (Se'ynlonr I9K71. Thus, tt is possible prijnna ls|"ak-^iieflthuift wtttMriicii> shtiwii Hit &etfriraii-<.in [fnhanstrn 1 ^ 7 HTtte Lo tiilunlate the m inim um arterial blond pressure of an animal from a skeletal nxunstruciion, a.sMtming that the heari wab in the sternal riri'a ami ibe blnod column was the vertical distance peripheral resistance i,s not d pressures lit be- jxvusihle I unciiunal roles twJmv: At this paint, bowe-ter, uV neeii uvcen 10 ,md 25 tP a in some ornithopr.id and theiopod di- I mly fo tibiit.’TV'i: the ^1 rung correlation. Pulmoi ur y arterial blood jiosaurs (Seynn.mr I 'ind possibly higher in sornesaurnpods pressures. oil tile ill her hand, remain kiw in both eclolherms tSeyn’mur anil LtlWbltC 2llfH)|r These measurements show that and ctldothmtlt ! Fjg, J 1 In these uises, h U yenerally accepted tbe hearts of dinos and inhibit :ei|lih'l'i! the lunctkmal se|:ar.ilion of systemic and pulmonary ga> exchange i.Wrtrig tt al. I yyH>. Although fbdliian reptlfo rely on miwituUi i b.nnbered hearts that 'vere rap tlll*’. in'ucJiemting high svslcnot force Hi keep opposing walls and ridges preyed to o th e r ti) bliKtd pressures consonant ^'ith eni.Utlhetmy I Seymour 2un! Fr), jchicve separation during svst include 3.^ kl'j Ifjflntiifwbl and origins in basal archosaurs. O ur stndv foither supports the Mmri>w ISiM i, n.3 kP^i (Vvhite ]y701, and 5.2 kPa ((ones and po^iibilUy at endothermy in dino*1turs thtfit evi^lved from this Shelton l‘W !; tliose for (TfticodyiUf ['i>ro>u> inctudf 7.1 fcPa group. The ovjdcnce }ve present is jt hr>t ptiltufilOlMjgifid. to ! Altimir.is rt .iL 199ft!, 7.9 kP;i and liih.inien l'W7l,;iMd show huiv itif ijwiwitj'ot crocodiiians changes! Inrun krreslriq] 11. : I I i Asels^nn cl I. . V97i. to aquatic Ijlestv’les, T'hen we discus-, ihe cardlovascuiar phys T'ljtre are also consiJerable differences tn rffuHve (leat i si/e iology jss^ciak'd with aquatie brhavioi in reptiles. This k-mk between t'ndotherms an1'jS-j fi.. S. Seymour, C. L. UeitneK Srampcr. S. D. Johnston 1). R. f-arritr, and C. C. Crigg
While the^e Jri? iml Onrisidurcd th r pcogistiitprs of oroaidiles, Webb ,md Carl CJans ( I9S2) speculated Ihsti liotmdin^ hehavior they a it from iluj TrUssic and dyse id [lit .s;;!i( defining the miiihi be ancient. However, we kaiotv tlur houndinp behavior crown-tlade A.rthtwiunSa [Sirt'ty,' 11>1-*I; brnchu The r.T3tntk>! be tfllerated tor long periods In livinf; cn>codiiians, be- ornithosuehids (e.^,, and art an t.msv sirenuous activity is iupporled anaerobicaily (Seymotit other group flf.tiasst arthosaurs lhat appear tn ile dose to el al. KaJdwin et at. Crocodifes now use bounding th<.' IfiVisintl between crumtar'iaiis afl(J mnithodirans. n111y tor shcirr dashes lo water, loday, hounding anceiiry may Tin; Cfcici'kiylj tbTrrt lineage of kmrutarsans appeared hi thtf jjIs^i be relleeted in embryonic or)uvenik iorm.s. The himllitltbs li.;jrlv )uras's jc, exemplified by wl/jijs i~ l mS and tin h ti develop more quickly than the forelimbs in enKodilcSt bipeda] *;t, 11.- ;n , nJ it imdi'i ev.i: inns... . rad . iimi ll i ■ i il'.Ii- birds, anti jumping amirans. while tlie torelimbs develop hrst i>ui the Juravsk jcld O'etSMOLK Thin lin^Myc: i-; traditionally in other qu-'di njirdal vertebrates (l.fodsyti i97S; M. Richard i lassiried into su ited ive ^roirsychmni, mt'snsiiihirtns, and fi son, personal conimunication). The jumping, insectivorous' nally eusuc hu m , hui niily Rustic hi a is not pBTapitylftic I Brochu babih tif juvenile cnKodilians give wajr to slt-and-wait habits 2Uf)J). Some ii! these jurassic en>codylifVirin> were highly of the adults (L. Gam, perstmal eonmumlcationj. These geneiic shifts in [drm and tn-'luvior niirmr the phylogenetii.; wholly tWresfftsl, The eusuehian!. aj>j>eaied in [he Cretaceous, shift from terrestrial to a. The skeletal tea condudftl I Iwt I he hasni archo.satirs were endotherms, based ttires nf Hnftti/iHrriiii F.rpeioslunhus, lhe sj>lniiio;,uchians, iheor- on nevoral iines tit palcontologital e^,idence1 including upright tilth rwnchld;*, and the early oniltli'.Hllj'ans are suggestive of eur- slauce, low predator-pn'y ralins, bone histology,- ant! the ap SLiiiality: hip and shoulder jmuls capable-nl p«hiri0Wi|fth£-l(jjps parent compctilHT dojtiination by thearchosaurs yver prchum- iit parasogiioil plftnts, delicate and wirtw)fim*i* lonjj htnb bone*;, nbly eiLiliidiLi mic piJitontammals (lli(.iapsids:. It has turned and ihspioportinnate lore- .nul liiitdlinb lengths iIilll inditdle imt that nunc of these lines o f e\ridence in ii^elf h.is prm-ided .it least Me ultativc biped.-ilbm. This description lils I hi.- ha.wl a con du sivt- case foe I'odiithermy in basal -nvlHwanrjr iBennett crocodyloinuipbs hnr not the advanced ones. The fossil evi and Kohen tVftfi'J. On the uthet hund, neither has the eaye fnr dence sh\Wi that locomoLion sin fil'd from running to swim i . tothennv oeeti prnv n. ming i Parrish IV^?;. rtrrRing the ciocodyiiieirms, there- wav a nend toward fcduttk+lt in fhe dermal armour and development Physiulo^) of .\qimtic Reptiles til pn.noi'lous vertebrae, btitti aiissclatcd with a loss of the lat erally .'.iiJTened trunk talubblu tbi ctiisorjal iespccijJJy bijujdj)) Living cn.ieoi bUans deiitonsliflte a suite of physiological teal ures liKiimntion and I hi- dcvdLipinent ol'inereawd luk'ral movement ih at serve dieir hehavior of sit-.md-w.bit pnidatitijj in water til ,m.i! iwHnnitlfig (Sjli'sbury and Srey 2CX>IJ iMesoiuehi^oK Seymour I 2 1. Whellier they eal fish nr lerri^iriitl animals, aiul eusuehiiins developed ^.econdarv palales that allow crocrHlili;in'i l>enefit from long brejlh-hold di\'es, because they hreathinji wlicn lhe mouth is open underwater (Iordansky ( an remain cryptic before ihey eapiure prey and stay submerged iy7.l |. Thus, the tossiU irrtpl^ a shin fmm ciir^ori.d pwdali^n while they *ulujue it. Obviously, an aquiilii. prtdaun- that on l.md in lhe Trinssit to a primarily arju.ilie nitjie ofam hush port innate that scmvt juthois sujs^ested [hui they bounded time by reducing oxygen consumj'l iori and increasinp tolerance about tho landscape (Walker 1970; Mt'nmn l^yjj. Today, to .I..:..■. ■[->x metabolistii, bounding liiconuition, often talk'd gflEkfptrjg; i>ceasionally t>c- inr-^ in adult Cw-D(fvfws ((ifmitHUij1 (Webb and Clans 19flJi, iu- j", i 'i y veniJe Crdctfdykfi riJeltfiii (C.iitt and Cmoclyhii pinouts ;Ztig ll)74;. Tin.1 sagittjil tle>in^ of iht spine-and limbs has been iUislnig rates o f oxygen consumptitin are fi-MJ times lower in de.snihed as similar fn itljt a Llieerah al lull.spet’tl. tJraii.ntu; reptile,; than in mammals ur bnd^i at ci>mpatrable body size ami iMiitotiitrmic Archosaurs |(l55
lem ptrjuire fRennett and Hawuon I 97m; I yK31 In water, ui turlles ssphvxiated frtr .i day or mon: (L'ltsch and lackson moreover, body lertipeiailjrert ul' reptiles are frondJtrjbly lower jyK2). CwfViiyitts' poroms can survive bknid pH droppmt; tn lhan :hose of most endothemis, li it I her reducing melabolic in contrast to most reptiles, whii.li ;ire latigued oi dead rate by a Factor uf perhaps tWy, M.fiitat body temperatuies of when pH drops much below 7.0 (Seymour ti ,tl. 1^ 3 ), Mulscle Crucoiiytiis p o w i if range between about 27cC and J IJC in w ir pH can drop below h.tl in Irirge C. p a tiim i possible netting the ier snd summer, nesp’ecii vfiy, under tie id conditions when the limii on anaerobic capacity (hulilwin et al. IW 5). animals arc engaged in basking during rtie day (Crigg cl al. I*H$.; Seebachcr et al. LW9>, IxLolhermy is therefore an im- it ..■■ tlfSCiJl':,; i portanl lea Lure ol’ divirg that lengthens dlvea, and ;i should be of selective; advaniage m aquatic predators. keio- The incompletely divided hearts o f noucroeodilian reptiles po therrny is also an energetically advantageous strategy for an tentially permit mixing of oxygen a ted bloi.nl from the lung with ambush or sleuth predator, because there is rm requirement ileoxygenated blond from lhe body. W hen mixing occurs, the fur lhe sfflv 01 motionless animal to ria.imdin a high body flow of blood from fine side to the other is called a '‘shunt.’1 lemperfture against the high ihcrmal conductivity and heat It is possible to observe deovygcjialed blood returning from capacity 9 rWatej. There are no Jiving endotherms thar teed like the body in sysivmit veins being shunted out to the body a^ain in the systtntk arteries a so-c.ilk'd pulmonary bypass shunt, or right to kl'l shurii, because tbtr shunted blot>d moir'es from the righl to the left side of lhe heart. Left-lu-ri^ht ^h^^H^ can tintiy Hize also oci-irr w'hen Mime of the osygenateid hi odd frutii ihe lung Bccause uS^tot stores ir the blood, lung and musck volume ii recirculated lo it Csiisfit controls, and >,h.i[ relations of shunt are nearly proporiion.il la bddjf Site, bul rtieiftbwlk rale scales ing have been mk-ii'oVfly simlied in iepli!es. p.irlicularly in allometrkaily with ar eipcnrtii of about (1.7 (Piffles 198.1 >, conneclion to diving or hreaihing paiietns (see renews by Sey diving lime should he pinpoi'llunal m body m,,-.:- r>4.ibvtl to m our iyS2 |, Burggien i ]y.S51. and Hicks | l LJVtiJl. It can lie roughly the |sower of 0.3. This jricartf that for every nrdei uf concluded that tliert.1 is a v,idi.' va rial ion in p^i terns of shun ting magnitude body mass increases, aerobic dive tirtic i> ipprttiti between species and physiolo^ieiil stfltcs. In general, hitwewr, In a (fly double^!. Larger predaiors arc not only able in itm ain there is goinl evidence that link si urn Ling occurs in repiiks under the water longer, they are also stronger a rd better able breathing noi maily in a ir but pulmonai y bypass) shunts can to ■. >d ic targei piey. develop during voluntary diving and especially durinj; enforced dives undet hhorjlorv conditions. Despite their completely divided, font-ch a inhered hearts, H:.J' Aaaerohit 1 'iiprtLdC,' i_rO[.oilili-im can develop pulmonary lupass shunis. bu! unlike t-Ctiithftttnk reptiles rely tnore highly on anaerobic riietfttwlisni noncrocodiliHii n'piiles that shun I willnn ihe vein ricks, crou- than any oilier animal group iHemiell and jSawsor 1976!. mlilinns shunt through .i unique arrangeitu nl of the outflow While the aerobk pal h way is able to snpprnl rr-lalively sluggish vessels nf the heart iWebh 147^; f'arrell et al. ly9K). Hot It righl MCti^iLy. anaerobic metabolism fslies over during intense adiv- and left aoitic an, lies iirv prescTtf, as in urhianten of Pan- u bios is leads to accumulation uf lactic a a d and add-base dis i 7.7Jt cim net Is the right and left ai'^kes above then1 bicuspid imb.ir!L.T. To avoid incapacitation by fatigue, selection has fa valves. The pulmonary artery also comic-cis to lhe right ven- vored a high tolcrancc to the prodncls of anaerobic metabolism Iricle, but uniquely in Cffli i.nlilians, the pulmonary bJiJthd passes ir reptiles. Diving wouid be expected to pro mole further re ilirnugh iwth viilves, first a (Wft-ttnith valve tl’.at can rr-sh ii,l How1 liar ce o r ar aerobk pathways and tolerance to acid metabolites. ju d then a leal vjjyc that pievetiis reverse llow. pinalb, ilnj An atpmliu sit-arid:wisii predator might fljlyoi) aernbiosis while right and left arches join by an anastomosing vessel posterior slalkirg and an.itrobiosis while fighting underwater. lo it ,i i. Crocodilians In puilicular show ar exceptionally Jijjjh reli The patkm ^jlblooi.1 How duiin^ mimbniilrngand shunting ance f>u anacrobic nirt'abnliMN. Auaerubk capacity increasi.s in in ^TfK'odiles has been titr locus of many studies llur reviews larger pi'iiyHif- yriimals about I kg fatigue in about 3 min see While 147(1, Grigg l^ny, Avelsson and Franklin 1^7, and of strunuous exercise, but lliosr above 100 kg can Iasi an hour Axcbsi:r 2 0 0 " i, L'nder rionshunting conditions, (Tow Irom rtie or su (Uennett el aL Bltiod lattale levels rise lo 20 mmol riglil venlriclc goes only inlo rhe pulmonary artery; lhe valve I.' in ,4/fijj[JJ[)r miftittippittffh Rkiulson and Hernandez 197^1 to the left arih remains closed, hecausi: ilse pressure in the k n and above 50 mmol I/ 1 in C. porcsus (Bennett et il- )9f^), I tie anch is always greater (liar thai ir Hie right venrricle. Ulood latter possibly being the highest concentration ever recorded ftoiti the left venuick flows iniu the right arch, and somf ol in a verltbrale as a result of activity, [.at I ale rises higher tmly this can pass through the furann:ij ul P.liljyjn into the leit arch, [056 R, S. Seymour, C. L Ik'nnujtl-St.jm pcr, S. D. Johnston, I). R. C arrier, and G. C. C»ri££
Dorsal View ■V 'ill f V'r,.,./
Figuir J. t..lumlvi't ilrild uiiTlinw vtcs&ti uf ;Ue c MJCiftlitiiM hcan {Grij*g ]S*K4r. ,rV„ m'V, J-£m = left n*Vi'i iliIIv during diatftjk* Blood can afcu pa.'* fctwetn arirfe ctjffiitt]lion),]w liji_reasing righi wcfilrluilsi pressure and opening at mss I hi1 jn^siomo'ds- behind the htstrl. Reg-atdlesi, at varia the '.'ak'f tit the lei I arch. [I if cogtin u h valve (ty ijjlts as a bility in ihcdivision and tim ingnf J tow events, there is cornplcU' vitfiabU nrjiituT1 imtlty' rtirvrtui cuntrol. Ath-errttifj^LL siimulation sepaiLiUnn ot oxygenated arid dfpsrv'gettakd blijctdf when rhe ix-liAfti |hf valve, probably keeping it ciptn Jnriu^ valve to the left arch remain:; clos^-tl. Under th urning condi tfiudilifiiu. o f itrrsii or t'm'rviyt; ll’fanklin ami AftvlfAr.in iHfHJU tions, hn’ivcvei-, contraction o f flic ^’rtg-rooth valve VJUiei pner,- Shums dt’veldjiin^ liiinnj^ tilvjfjg hradyc^rdia sii.iy involve cho- nuf^ in rhe right ventricle 10 exceed that ir die left arch, and lirergiL' L'lie-.is. mi ihe valve (W hite I97ni Axelvwin i.-t .1! iT^ bicuspid waive opens.. Blood ejected intd the left arch gvil h tjllint; niainlv to dir jilt, but there in rv'ntrtics that an apfireciitbit r^ystc-nnic biixjtl pressure Shelton and Jnncs 1‘Wl). The sizeol amount can go in the reverse direction ihrs I hrt.niyii I ht? foramen though tihtilinfcrgk effects hjvc not been lested fin the loramen : ILi|i ' nf Viiiii//.i, if ucetykhnlim' ;k^ like Vlf' then one wonttl Imvl: Shunting tsi certainly controlled in trvjcodLlians. Il ii initialed the sitaaiiiin in whuli diviiift hraiiJ^tirdia ii nswuJatcd with by ton! met ion of the co^-tooih valve at the base of die pul- contraction of iIk coj>-tooth vjjve ,iml teI^xjIIiiH a t the fora m o 11 a rv conns, Tb is 1 nt rta ses- 1 he resist a nee of I h*.1 o u t fl l i w i ract, men of Paui/7,1, both promoting ,i [luhno^aiy bypas% shunt. L.ntloihtrmic /Vrijhosaiiti JIJ57
Shunting tlas been suggested as bein^ involved \\rLth sevet.il bryos do not show aihill phy logenetic rliar;i;.ieNHtics, and chere re.-piilLi.in characteristics, including behavioral Lhi_TnjinteguJati Red nut ion in aerobic me tabu hi rate helow normal a n cm riser ve he adaptations by the embryo m ils tin: uni stances, these oxygen during a dive. Studies of aquatic lurfles have shown changes can have origins early in develoi'irmn hut are not that diving is associated with increased pulmonary bypass suhiecl tw selixfion unlil fater lRithards:)n 1949!-. \Ve Ily-pptVi shunting leading to a decrease in arlerial Plj, fBurggren and tsise, Theiefnrtjhal late develop mem ol'rhe i^iramen nt Pan i r.j* ihelton iy79; White et ai. I9N9I. Ejqftysure W hypoxic pas aiul cog-looth ealve in cftx;ot|iliiift emhryos ^voidil he i'.sLimpies (Hicks and VVang 1999) or vagal stimulation (Halzack and of ^Licrtoyenesis associated yftlii tlie seciindary evoiurion t>f Hicks 2W>1) also results in low arterial Pu;, decreased systemic '1111 ltinj ca ■.111ir11;. mcroen transport, and a iedu^ii«n in metabolic iaic (VI .maes.- JIil' emhryolngy of verTebrale heart.s Is well known, including thetisad 'Ihhht'inys sirripui. This hypumetabolic state is consid specific studies of cnicodiiians hy O eil i 1903>, Hoehstetter ered to be an active downregulation rather than a simple failure (|9tl6j, Reese iiy in j, Wellslein (IM ^J. Goi'Hdrich I I L>5M), tiha ofo\ygen delivery tn mitochondria. Hypomerahnlism, whether ner ( |9ft2), ;uid Ferguson (19^.^;. The nuUttitntMJs Hiiil tin- derived frorn shunting or general hypoxia, is clearly adv.mlrf- early and inrtnnediate dcvelupmeiual siag<^ arc the same m gootis f(jt exlemhug dives. But shuntiitg itiay be a more effective crocodilians and other vertebra Lev The hearr Ivgins as a single mechanism, becfluic it c.m induce hypomeiatmlism earlier in I ul>e thai bends on itsell, liinttina si tinus \'eiinsiis, atrfum, a dive, when considerable oxygen stores remain in lhe lungs. ventiicle, bnlhus, and ventral aorla- The ventral aoeta in turn Without the shunt, hypometahnlism could only he initiated branches Into several at>rlic archcs. Two -.I’pia 'hni grow toward late in the dive, when most oxygen reserves have been ex the heart from the basts of specific arches pfngrnlively divide h.iussed. Unfortunately, liiert- are no data on the rfitaiioflsfiip the aorla and luilhus i Pig. 4j. The pnInm-aortic septum grail- between shinning and metabolic rates lor crtscodibans. ually separates the pulmonary artery froin ibu Iefl arch, and th(‘ lriteraortic sepium separairn lefl and right arches. Mean while, a m uses liar interventricular seplmn grows toward the CroLOtlilf I k'jrl Development bulbus and begins tn separate lhe Tight and [efl ventricles. The The controi of shunting in crocodiles is dependent on four intermediate result is a Ihrce-eh.tmlH'red ventricle with three anatomical feal tires thai are unique among rep riles: ( I > com- L>utflow vessels, each wilii vahes ,ok1 ,tll connecting tn diliaii i'he inlet- righl ventricle, (3j a cog-toorh valve at lhe origin of lhe pul aortic sepium mav remain perforated in itnmiucodilian rep- monary artery, and (4) a foramen o f Paniszii. insight into the nlrs— is-hethr.r above the aorlie wilves I Yonng el al. 1493) or evolution nfihesc features may he gained from a sludv isl heart below iliem fVVehh !*+7u) j^, jj^j ^eriain— bit; these perforalions cltvejopjtteut The argument we apply here is thai ile novo ire not homologous l<> lhe foramen nf Pan i if fa of crocodilians developments ol a nglu venu'iadur origin of lhe left ?ftrlic (Wehb l^79i. I’Ctufi (lbs pmnL, the irrocoviih:in Uf.iri unique arch, .the fnr.imen or Paniria, and the tog-voorh vnlve in em among reptiles, bee a use ir proceeds in form a inembrauoos bryonic crocivilians Tt:present secondariJy evolved features septum that prows trom I be muscufat ventricular Septum, (apomorphies). This hypothesis should nol he rejected hy as an'ross lhe com m on chamber, and into the wall beiWrtiTi lhe sociation with Haeckel's Jliogenetic L.aw, which propused that right and lell arches, thus compSerely separating lhe left, and tht adult stages o f phyiogenel it history are present in the em ■igii! vcStffiekfcs ig. : j. bryo (ontogeny recapitulates phytogeny). In faet. vertebrate em kernarkahlv, details ot the jppe h jil i' til lhe lonnnen nf I Or>H R. S. Seymour, L. I., Ken net [-St a riper, S. D. Johnston. R. K. {'Jarrier, and Cx. C. Grigj;
PA LA oR A o
septum
^------Bitlbus
O Interventricularc j c i ) sepfurtt
Hyure -i. iiL.hi.Jii.itiL- >il L-incifiiL dtt*lupHllftH in repsllftr, ihntyit^ tlie litngfe^iivf nui, I.-..I Judujimcn! ol llrf.j'iilnii' iwrti< -iitl! rnisHiirlil1 -jrpi;i jiiJ the *.T-iffll4t| tltfl'flfiptlieflT "p":ir.il nf imncroLLijLtuii] n'ptjlfL-
Fam^/a and i5ng tuoth vjlve .ire eilhtr kinki-ni' t>r contradictory ftratluH in the complete intc-'riiFtrlic septum I Fig. ft), flit fo in iitt' iiiewt□(■(.-. in j monurTerttji atmpjrisoii -il .crtclirafc ramen first append .n .'.Uig<-2 1 I pTifglflPtt 1983) iiti .1 dirtijiji m heart development, irreii I L40>| Jcsi-rihL-d I lie up pen: a nee of the sirpiuTii belund the rnedial vah'e Lu-np ol Mil- tiglu aich. This the funmrrtft ot I’anizza ($ jSefiend^ry perforation lj[ i K<- in- dimple deepens between sht^ei H2 and 2.1 and opens hy leraortic septum in 1 lie- ^jiniiin. Bm Goodrich 1.pro 24 or 25, at abeml rf n f ircuhstinr. HjU.hinc th allij’aliit-, nounced iliat the fiwa'intri Was ntoft: likek loWmfrt by a laiiure ueeurs -it sNij^ 27-28, at about (t!> d, The foremen ol i'ani//a Of 1 lie interaortic septum to LililiiSe completely during hs growl |i wan unfortunately already r>pi:n m the youngest L'. pon>v<< l'ih- mward the he.iri. t.rn l’s description more strongly supports bryo examined, al Smge 25 i>n day h>0 t)| an SO-d imiuhalion (he |typalhrti!ti?f-4 secondary Ji'vt'lojwTiL'iii pctitxi: Hirwwcr, ■serial secliyjis o f the pulmonary ct>mis in li-.c- Irn-.iiiLtii is clearly .1 sin.VL.-l li-.n; 11L-. t iLJodrkh’s explanai Lon hoih !.peeies revealeel leuillike biLiiiptd valves, but nn livid cjfnes not rclute tin- IlfrjOTh^sii (the Joramen to ukl lit p^ifdi)- ol cng-tooih mnltJle.H biflftw it at any stage, karchllnps morphie'i, hnl it i.\ u-c-iikff, because .lSI irpliles gu I hreiuyJn ,1 11-iii. 7). Web!' j1'“ failed to hud nod j lei in (1 po rostis stage nj incomplete division of ihe anrlae. Nolle of the other haLchSings, but fhufy si'erc ap]iarenl in Ll-m -lonj: iiiveitile1,. It ejnbrypbgiy4! accounts comments luriher on the appearance is ^le.u I It a I co^-lootb valves appear ami tiigin to tunelinn svell iit" ihe foramen ol Paui^/tih and sifimlicantfy, none mentions m alter hatching. These ^bsW'i'SltOlV' .'ajpi'OTt a iecond,iry ap itlOHi'i any structure n-HtiJiblirifl f)ie cog tooth vjKw Jo »lvt pearance of ‘ihnnting -in;ii(jiny in croCrtdiUsns. the matter, we have iiives-ti^atcd hear: development in di&fguHJr. The tletail'i af rriembranLtus ieplum developmeni diftjeY be niinK}Jwnsis 1 Hen ret L-Stamper 21)03) and Odoirtj'iffij.'pswwsfHs tween ^roaxltiian:;, birds, and niJinrMh, but ihe pattern of IR. $, Serrrmur, S. D. luhnstoTi, and S. I. G. Kuntimim, un ai'Chlation is cTitiudh d^twn.deju where il joins the three published mannvcnpL). We used .standard wav hi^lol^idcitf-tftiJl^ outflow vessels tSIuner 1962). il joins between the left .md niques 1111 mierinedialr and final t t w 1.11 development. right a llies iit cmocodiles. In binls, il iotns ijelvveen the pul - 111 l‘ results irom tflt alligainr -ilign \veli wjih prcCHyys Lle- imjndi y artery and the left arch. Util ihe latter quickly atrophies, .wriptions, rurm'ly, lhal (he two ^p tm in rliebnllnj^Knf"-' toward le-avine (he nglit litth-tv the i>nly systemic iujipSv. Ti is ..iniulicant rhe heart atid iltar the muscular itilirrvfcmiculaf sepiam pro- ih,u ilk' jh ian heart diies not p.L1^ iIiioil^Jl ,l cuHiodilian stage, ^'L'suvely divides tin’ ventricle They also ckarly confirm Cveil's with the fett areh ii^cnfn]’ ijin> (he right I'entriele. Iml lliis observation ihat the ftnmn-ten 0 ! Manila d> Other Evidence fur Endothermic Ancestors PA LAe RAr, ■ itng Structure
I ;rocodilians have multi chambered lu lujtS with a complex ar- rangemenl of imerual eonnecling lubes. The sinking similarity in design between crocodilian and avian lungs h»i liten well recognised bui difficult to explain references m Ferrv I^Wj. hmbryonic crocodilian lang.s show fiyo sets uf ch ambers growing from tile primary bronchi: a a.-ini a I and ,|nrairhrv ^a^cv In m- venile C i6iudyius hifali'c'jii, ilu- ettixiive exchange surfact area is small ami ihe mean harmonii; lis'iue liiiekneis ia relatively rijjurc 5. xhcm dtk o1 iIll- ^roastliliim tmrTt. wttli jwotriclo completely large, so th jl lhe auaiiiniital diffusing capacity U flick'wist tor separated by I be intervi'nlriLllLur and mrmliTarifHis septa. The luriimeii ut I'aniTya copnccti the L'tt SrtJ liyjit atjnic jiritJicvi H-Aoatld fMo, rc- reptiles (Perry ivytt). Perry 11990.1 recogniicd that the turrenl ^HliIlhl'Iy!, and .1 «ig;tQOlh Wli-W lies beneath leaf vjtirej in lhe pui- c(nriple.'iily touM haw resulted from a tnnservative genome i ■ . ■■ i rlt ■ ■■ but found it difficnll lo rationalise, olher than lo suggest that perhaps lhe complexity in juveniles becomes useful a* life an- iraaJs grow to great iize. I lowcver, we teel thai eroeodilian lung slructure may bean alavislje trail inherited from highly aerobic, embryologies (Hn-mer iSJSJj., The jfoitlinrlfj' between avion and endothermic ancestors. I.luring e^oJutiort as ectoHieriils, lhe reptilian hearls makes il easy tn visualise evolution Imm a surface area iias decreased and harrier ilikkneiis hat increased, common ancestor by a simple shift in the miitibranous septum but the overall strlitHirL1 has not greally changed. (VVebh 1979). Jti nismmils, iailure ofthe tntrmbratioiL5'iseptUJli to jnin in lhe correct place creates the HifWt common congenital septa] defeels, including the Tetralogy of !■ allot otvJ nJirlpjefe ii^rjf ilurifig LocomoiW't transposition qf tli* puimonary artery artd aVirta flfedisr and Cartier (1987(f) described seven characteristics associated wilh AndeiMKi 19fiI). Humans can even ieiain Ixilh right and Jett lhe ability to breathe and enhance stamina during ic>t:omotion: aofltc ardie*, provided that sufficient bkjfiii ii passed through ft} diaphragmatic muscles, (Zj eniarged transverse processes them during development. These cnngeniial abnormalities can and epaxial muscles, (?) bipedai locomolinin f4) upright pi>s- have t mullifactoriai genetic basis, as evidenced by a small, but ture, (51 bounding gait, (6 ) lateral stability o f the verlehrjl significant, risk of familial torurr^rtie (Pierponi and Moller colunui, HiTitl l?) endothermy. I his inile evolved in lhe syn- 19£6 i. The prevalence o fsuch defeLis .suggests that only a minor, apsids, leading to ri«cfe»it mammals, and in the dLapiklj. leading developrotnllill literal io;s die membranous septum ean result to recent birds. Garter (19S7«) pointed out that Lit least ele- tn Urge difference's in (trial cardiac design. Whether a Ie1i aorta irnaiLs J, 2., 4, and S are evidem ii> living cTooodihans and (hilt, persists and what chambcr it connects t*1 may depend on ge alniig wiili a luur-chambered lieart and a rcduced fifth digir net if switches that determine where r In.' membranous septum on the pes, these characleristics are incoirsislent with the present fuses with the walL In- conclusion. (he persistence of lhe left low stamina and ULtolllermy. He proposed that a shift in life aortic arch and its t&nuHfcNuJi lu the right ventricle in croco- style, from terrestrial endo(hurmy lo the amphibious ecio- dilians does nut involve a great modification iii heart devel thermy, eoultl expiain these features of trocodilians. opment. !l srRipfy depends an the site nf attachment ul the Recent observations on American aliigalors fnclicitt that membranous septum, and this location can easily thlfl. In con crocodilians do breathe effectively dm ing terrestrial tocomolion cert w lh the vecondarv development ofthe foramen of Paniicza [Farmer and Ciirrier SQOUn, 2000b, 2(H)(li'j. 1 ung veniilution ol and cog-iooih valve, such a shift completes the appearance of resting alligators is typical of elIOthermic tetrapods, cotliiititlt a novel shunling mechanism in cntcodiliaos consistent with a rtf inlermidenl breaths of moderate tidal vohime. During ex ■ T ■jinII I (0 I1.... "":i_'I mv. ercise, however, lhe veniihilion pattern ol" alligators is mote dimple
Figure fi 'I r.i mvL'rsc iccuofij. tfcjXlLlgh TV dcvfl^,f'tn[4 FtwH ('I .-iJJi^rtNT rtj 't-j.-/ ^ .ll vlccttJ I.JIL- I-lt^u^'il ’ lLJ,Kf'l tfrifji'f I hri't 11 Li Ml in*- v ;Fn' nLtiml: iIil- |>ulmLnur^ .Lnny I M i arul Lhe IcU j]iiJ lijjll Llurftt VHViifs (M o .lriil JMn, riiptLtively I. Thi' !'ur,irrier» nf K in i//* I f'J'l :ls Himplc in Llit sejiluul in rtllljjira 11—2.1, lirc;Lki llircuj^li at nlnnn -^l.iL’f .''-I iim) is L’nhrpeJ Ny faiCclliftp ^tiL^if J7. Nmiv ih.ii the inii iispiJ Ilm) ^dv i i.irrsi nj; i fhn’e lumin.i. rn i-’ vessel '■ l-.: ■■, 10|| jjlh Endothcrnnc AhiVuwaurs IMI
1. ' Ir?nsvifrse seclk>ri Mimui’h [He ric.m .l hflfcWMff L’flei'ddjfJjlf [w rnsu f. '! he lo.ivrs o f th< vnkiyin liie p iih iw tu ry sritfV (f,4) a rt visible ihe rup n^tn, nesi tu the Ltit atjriiL- :irih in Thf lower piiiiel, ih t smmnii w.ilk e d ih r fiifnV atntf/(.uijui lsdoi(> [he le tfv jiltis fetfiiul uinLv ,i. v.:- ! r . : -i ■ ■■ i h ] ■.i.Jr■ i-.e ( I i ; ;■ ■■ 1 iK "
simiJ.ir To ilnii ;,Clints m m mnu: Ih:sn il- :' i " ithi I'tln- This ability Rl KktjIIk1 effectively during tciTtstiLaf ]jMt- lhcTTTt&. !n alligators, in!..I voli 1 it' du i tg ivflUaftg inci^nse-, .li- fUimon is signilitanT, given ilk- iugg^illiin that the ancestors much ab LonrloLd aboVS that before etspRifc. Thu ttiass-spedfk of basal were unahk* to run and breathe at i-da< volinnc tifvoonij, alhgaLors appear t ■ je|■• 11 .,j, '■■■.:• , iht ■ i k. ' ii ■ i r I'-’-S , i . ■ ■ Tier i . I ■ i r 2fltt a. liieilJ . iLj'i i>ci for in1.) ..n:r.i.11 during ijferi: u . .u:J the .. ■ 2000/?!. Tn anintah with a spwvJinK lin|ln| posture, tht ji_1 inns ol - iii' :ijon greatlj c.wed* ii n f■. 111 : ■■' !■ ■ ; nangL. of thf .Liial ifluitjtfi io ]'i nduce cfintd] ventilation Appear to be ! .t i1 R. S. Seymour, C, L. Bennett Stamper, S. D. Johnston, I). R. Carrier, and G. C. Gri^ci
antagonistic to the locom otor Act inns required trom these same rate was jneestral among archosaura and that some early groups ttruidis to produce IfitiiEil bending ot the trunk and postural subseqtiemiy ahandotied the trait. This view is consisteni wiih stability, iiuch j !oi.oruotor constraint on costal ventilation is out hypolbesis that the crocodiliansalso loslcndothenity when present in lizards fCXrrsrt I4K7Ji, 1991; W angetal. 1997; Owcr- I hey became aquatic in the Jurassic. kowiei i't al. 199^j. Nevertheless, the- taclors suggested asdls- rupiing lustill lim itation in running lizards arc also prt'Jtirtt in Mi ■ Zi'i.i walking illijtilHHS Ulbtfit tn a lessor degree]; ,i stJTttccccI poslme anti i.Keral bending of the trunk. Given the conflicting actions It has been argued that the pace o f genellc change is affected of axiai tmnfcles in a sprawling or semispra wling tel rapod, what hy dilfierences in body temperature such thrtt endothermswoLtld lit; to ri allow alligators to breathe during lerrcii rial locomotion? sh[>w higher rates of divergence than ectotherms (Martin and O oaidilians have a highly derived system of lung veiiiilation. I'alumbi M^3'. Crocodilians, in lact. show relatively higher M o fit dramatically, thev possess a specialised ventilatory m usdc, rates o f divergence in lhe n itoc bond rial genome than do other the diaphragmalicus, w i^ h ii josULimenral in the production cctothmfiK lKoma?.awa and N'ishida I y95: Quinn and Mindell flf inspiration and i.s largely. ot entirely, independent o! loco- 19%; Jsnke .md Arnasou 1.997: Janke et aJ, 2001). This t;ict has rnotiun (BbcUttt 1942: !Mossible that the rectus abdominis and trans versus abdominis .■serve pi i- the large divergence is dur to a faster dock during the lirst nwifily a vemilatory timetion in idligjBors t.-h’iittier and Carrier part of crocodilian evolution. On the other hand, because di- 2U(K)df). Finally, crocodilians possess i derived pelvic muscu vergenct1 rates are higher in alligatorids than in nonalligalorids loskeletal system that actively expands the abdominal cavity, JRrochu m i l l ) , (he molecular clock may not depend wholly allowing caudal displacement of lhe viscera during inspiration on body temperature differences. ! Carrier and Farmer 20IH)if, JtlOtib; Farmer and Carrier ’ftllfluj, This Mtitu of derived chatacters associated with venliliuion dur ing locomotion is hard to reconcile wiih (Ik low metabolic Conirary L^idence requirements and sit-and-Wdfl |ife<.tyle of modern crocodilians. These specialisations lor ventilation are associated with selec- Praelieally all living mammals and birds possess ntspiratoty lion early in tile evolution of the crocodilian lineage for jj high tuibmate; in the nasal passages- These 1 bin bones wilh a lat^e aerobic activity m.etabolism anti an ability to run and breathe surface area have been related to endothermy, because they at the y n n iim.:. fijnCitErti to condition the itir breathed hy lhe animal and con serve heat and waLer by temporal couoiercuirent exchange (Schmidl-Ntelsejl el a t 1970). During inspiration, cold air is ■ warmed and hunaidihed before it is drawn into the lungs- ln- Filmilainellrfr hone, Ivpibed by extensive vascularr/.auo:i, If, a spiralion clhjIs the turbinates by direct heat transfer and evap L'lijiraeteristic ot birds and mammals, and ils presence in di oration, Uuring enpiraliun, when rhe warm, humid air from nosaurs was one ot lhe original lines of evidence tor endo- the lungs again passes by the cool turbinates, the air loses heal ihermy (tk' R.niqlfci 1974). However, the t'act that juvenile al and snrue of its water vapor, which condenses on the walls. ligators. produce fihrolamellar bone has been pul lorwaid as The resull is that the exhaled air Is cooler and drier than it one of the Haws of this argument (field 19971. Full-lerm em would h;ive hcvn it lhe turbinates were not present nr rheanimal bryonic alligators have even mure hbrolamellar hone than ju exhaled ihroiigo th-!- monlh veniles t Hom er el a I JOOIi. Tflts teatuie could, in fact, be a The presence or ahsence of respiratory turbinates in tos>ils vestigial I tail front endothermic ancestors, or ii could be coin has been promoted as a solid indicaroi of the endothermic or mon among neonate amiiiotcs ,md have nothing to do with cctotherinie status of fossil animals (Ruhen et al. 1997). Their endolhermy. However, a recent survey of hone histology of absence ill livmg crocodiles has been associated with undeniable lo^sl arehosa ori forms reveals lhat bone structure and growth ectoihermy, and their absence in dinosaurs speaks agjtnst en pail erns of phytosaurs, actosaurs, arid rauisoclllaiis were similar dothermy {Ruben el al. 19%). Similarly! the presumed presence In those in living cmcodih.ms fmi lhat Ifrtytfriiucfim and of turbinates among the cyoodoot gmop of protomammals is f-rvo.rp.'-;,' , 1 i . sin., n: mi e similai v-■ v-.as ni «ii- cunsislem wilh the hrst appearance ot endothermy in mam nnsaHrs. birds., ;mJ mammals Ide Jticqles cl te.tyx was {miSUTtKtbly. an cn- ment in Ihe argument is their four-chambered heart, which dofherm but has nasal profiles siimlai to those of theropod could separate the lliph sysienlic blood pressures fmrn low dinosaurs. Uving nectarivnrous birds and mammals that have ptlllnniun Wood press:! i es i i a sturs. Tb< r;- ;nc ;-m ex .an overabundance of water in their diets possess respiral wry planations fur a high systemic pressure: lo produce ihe iligh turbinates, and cetaceans in polar marine environments where flow rates o f more viscous, high-hemalocril blood associated Water and cold stresses are severe du not. There is also signif with high rates of aerobic aclivily, to enable sufficient ultrafil icant countercurrent exchange in the nostrils of lizards, but not tration in ihe kidneys and (issues, lo force blood through con in the same extent a? in birds and mammals (Mnrrish and tracting muscles, and !o permil greater distributional control Schmidt-Nielsen 1970), Tt is apparem (hat turbinates are not of pei'fusii.m between differently active v,iseuiar beds. Many of a siricl requirement fur endoihermy, especially in equable en- these functions are associated with the high metabolic rates of vi.'o:. rue:its wiih ample water jvjilahility. CrtdoMii-rms. There is no indication that basal archosaui's or early croc Ar.iither function o f high systemic blood pressure is to sup odilian^ were ever well msitlated externally. Howev: r, i e the port a vertical blood column above the heart against gravity turbinate argument, the absence of any ev'denct does nol (Seymour et al. 1993). I he only animals known to have evolved prove that they were not insulated or that ihey could not have large body size and erect stance arc endotherms. No terrestrial been ertttoflicraw. Insulation does nm easily fossilise'; as dem eautherm sustains 3 vertical distance of 1 m or more between onstrated by the malority o f featherles-s Atchntvpif.tyx spet- the heart and head. This distance is equivalent to an arterial imens (Feduceia 1999) and the rarity of feathered theropod blood pfissure £!ad ei i o l'f < i' -.l’n just ir> -.npin s " dinosaur fossils {Xu et al. I'Wrt, I999M. Furthermore, there column, and an additional pressure is required to move the are many endotberms alive today without rnuch external in blood through the vascular beds, because mauv has*) a re ho- sulation, for example, humans, many nther mammals, leath- saurs had erect sTance buT were small, ii seems unlikely l- without ol”- ous insulation. ians as aquatic ambush predators, bul there is no obvious se leclive advantage ft»r some smaller members of the dinosaur lineage to abandon etiuflTlKnny. Manv u| iheiT) fenlaified ftillv terreslrial, active (tredatm.-, that would have been tvel! serve4 Conclusions by cndolhermy, and they gave rise to endothermic birds. By I'hroiiglioul the ipniimiing deb...... tuc evolution o' endo- I he same reasoning, smnll terrestrial herbivorous dinosaurs that thermy and particularly the metabolic status of dinosaurs., a w re preyed upon mi^hl have been disadvantaged il they were common underlying assumption is that endotherms evolved ectothermtc and lacked the pifiteelion that water afforded the from ectotherms. The reverse, ectotherms evolving from en crocodilians. It therefore seems likely that enduthermy evolved dothem is, has r ielv beer. . onsidi-rrd Ricqlts 197H; C.irriet in the stem ardiosauns and vvjs passed on to many of their I9ft7it de Ricqles et al. 20Q3). It is unclear whether this reluc descendants. Having a high systems: blood [ncssure for c:i- tance stems iiom the obvious direc; oi. o! i.vo!ui ir. -.cr.'.'- dothermy in turn permitted terrestrial, bipedal dinosaurs to brates in general (ectothermie fish to endothermic birds rttrd become large and errct, because the tour-chamberec! heart msrrimals) or a chjuvinislic bias that cndoltrij'fiM jtfff somehow coulil develop enough ptessure tu support j vul isl.iitli.il WMirai more advanced ot superior. However, there is no reason why blood ciilumn to the head (Seymour f^7fcl. Xevertheless, en- reverse ev. ution is unlikely, artd in iac* it ;s not utlromn o'‘ dothemiy in dinosaurs may have been reslriclcd to the smaller arnnnn lypual c:uliii|i-n:is. Not cinl ire tfvv mjrneious ex species, which do not have the levd nf inertial hrmieolhermy amples of facultative ectnthermy in mammals and birds that characteristic of ihe giants (Seebachei1 2(H)3). Proposed ecto hibernate or undergo daily torpor, there are mammals with thermy in large sauropods tn hadrosatirs, Ilierclore, may rep highly labile body temperatures and metabolic rates that are resent additional aiecs of evolution from endolhermic .mces- routinely in the eeto-hennic ram::1 J . ir v i: 197S; Sl‘) i iou er ul. tor.s. lfJdi bi. S. Seymour, C. I.. Bennett SfamjHjr, S. I.V fuhtislnu, I). 11. Currier, >iiid f.i. C. GrijJ^
■V !■..EUJVt li^lgTTlCnt** and Biology ot Majnmal Like Reptiles. Sin ith sold an I n.s I i I ilinn W isHington, I ).< . Wt ap|'i<‘dakj [In1 ns, and I rum many Benneu A.F., K.!i. Seymour, P,F. Bradford, und C.J.W, Webb. people iliiii led to this.syndii'Jiifi; Mieliad Benion. Christopher 1^5. Mjss-de|K'ndcnce a i anai.'robic metabolism and acid- Brnchu, Dane Chfjs Haulers, ( ol.k^jv ktmici, tiraijt base [lismrl'ance during aettvtty in [he ,H Hicks, Willem Hfllenkis, Mike f i'h.:. 'piijvyw. 1 l’.i|' Bi[>i 1 l-K: 101-171, Tomas? fchrtfkuwicsi Nicole Phillips, MiefiitJ Richardson, fohn Hennell-SlannTei' C. Slrncmral d(Vitt^vpini(riW rtf liu1 Th>- Ruben, Sue Runcimjn, Prank SeebaeherL lohn Spicer, Lucy:SuJ- lanicn ol’ Pani^/a in embryonic allij^lois, MSt llitsis. Nl^v livan, Tijiljiajt Wang, Sieve Warburton, frrnhiimk. Webb, and Mexii i Sliite L nivci.i! ■■. Craig White. These people did mil nc.ticfeUfily read the man- Benlun M.J. I^'W, Origin and interrelationships of dinosaurs. us>.rip1 or flgxiy with .ill ul 11 llt [hi I ills, bul the) ivvrc influential. Fp. 11*3(J in D.B. Weishampel, P. D.cjdsrtn, and H. Osnn^l.ska, Tile rfc^K'h w.is supported bv 1 In- Airriirjlian Ke^eai-i bC ounui eds. l he t'limiJiauria. University ot Calilornifl Press, Berkeley. ------. Iliv7. Vertebrate Palaeontology. C.hapman Sf Hall, 1 Ifcral ure Cited 11. null hr i ■ —. |‘»9. ifctctiDHOi h h ii tiryivh and (he origin of dinosaurs Alttftfirai ]., C.F.. Franklin, and M. Aitokifiii: 1498. Kelatiim- .1111.1 (jieioriaurs. I’bilns Irans H Soc l.omt t3 35;l: 142.1—1+4f>. shLps. hclwccii blood pretsute and heart rate in the saltwater Hinion M ! and A.O. Walkei. 2Hth2. a mniudik'- crtKudih' Crvtvtlylu.*■■jisit'iUtfsi 1 F.xp Biol ^1> 1.2235—2^42. !lke basal archiisanr fnini lhe Ijte Triassic uf'F.igiu, Scnuland. Av-lsson M. 2001, Th* litytfijdillBti hearl: more con Iml led than >'■ " 1 ,1 inn Soc '■■. ' i ’ iii'i!' . I |■ P. .■ ■:■ :■ i K0:7{) -i v. hislmp t.;,M, 1997. Heart masb aiki ilic liia^iniLim cardiac o u t A-JtetiUnn M. and C.F.. Franklin. I9V7. From anatomy tn an- put ol birds .md niitnnnals; implivaiionH lor eslimntmg ihe gmscopy. In4 years of crocodilian cardiovascular research, maximum aeiohic ptiwer inpui of Hying ^nimjilis* i'!uk>.H recent advances, and speculations. Cam p Biochem Physiol Trans li Soc Lond K .152:447^130. A H&5I**& Hueiaerl R. 1^ 12. Sur la physiologie de la re.s|iiiation de ------. 2UQI. I lk calibre ol Lhe toramcn til Paniz/a in Croc- I'AMijrilur missiiiipimsis. Arch Int Phvsiul Ftiochim 52:57-71. ddylui ftortisui is variable and under adreriergu control. j Bremer |,L. I92S. P;url 1. An interpretatitm of th^ development ' ..ni| ■ . . o! H I: i:J4l—34f>. of the SiiMri. 1’arl II. The Jell aorla b( reptiles. Am 1 Anal Aset'-son \1., C.F.. Franklin. li. I■ riLm'hl’, (J.t.. f.ififiM- Hlld S, 4 ,:.I-u7-3n'!. N’ilsson. 1997. The lUh-puItncHftary conus and lhe aiieri.il FirDthu <.. A. 2itfi I fr. Cjtingruifflit bvt p I i y s i ol ogv, 1111 I o- n n n I h 1111 ^> .is im|’i>r Linl - iii- u f cJmSitivaJkiilljlT re j;i 11 .it i i m grnt’Tics ami ihe ffissil record fin creicodylian hislortcal bio- in the crocodile CntitjiSylrn pQr&iiii, J £ \p Biy! JLfir>;Hi'irn ]4. gtfograj'hy. Pp. 9-2K In tirig^i Ir, Si^'bmhei. and ( .I-. Aselsson M*i S. Itolm, anil S Nilsson. Flow dynamic^ nt i:ran!iliii. edi. Cmcodilian Biology' and FvoluJion. Surrey (he crocodilian heart, Am ) Physml 25b:kK7,i-khl79. ", iljy, ( hr]>})ing -V"' :. Baker LA.., W.W. Weathers, and F.N. White. I '.^72. Temperature - -. 2hH)U>. l'Jrogress- and future d ijx ^ to m in arehosaui' indued peripheral blood I low thtftrgffs in li/jnln. | Comp phyieigenelics. ) PaleonKiJ 75:1 ttt>-l2f)L Phvs.i'. ’ #G:>T i-fS:.1- ■ — . 211(1,i, Pkyloflenelic. .ipproaehes loward crocodylian his Bakker RT. l'98tii The Dinosaur Heresies, Longman Scientific tory. Annu kev F.arth Flanel Sci 32i.157—397. & Technical, Essex. Llurggren W. [982. Pulmonary plasma hlliaiion in llit luille: Baldwin |.. R.S. vmcjur, m J C.l.W. Webb. 1995. Sl.ilin^: ut ,i '.vH.'t verlchraie lungr Science 2 l fy.77 78. anaerobic metabolism during exercise in lhe esluarine cro.. . IV85. Hemodynamics And legulalion of cenlfal car- odile tC rm vtlvIm Comp Biochem Physiol A M2; diovasCLilar shunts in reptiles. Pp. 121-130 in K. [tjh'ittistn ^ntl WAV', burggreii, etls. Clardiovascular Shunts. Munks Bartholomew G.A. and B. Heinrich. 1978. Kndolhermy in At - ii i, \ i,|. lugen. ncan dung ttcerls.iduring llighi, haSl making, ami ;>aU rolling. t>urggren WAV. and K. lohansen. 1982. Ventricular bemodv- I Fxp mo! >i. nainics in lhe monitor li/ard V tujw us c.twi t f t e r > t < A pul- Becker A t. and R.li. Anderson. 1^81. IJatholo^'oK ’^mgeniliii m onan1 and systemic pressure separation. | fjfjj |ii<)i 90:^1 ii— I Ic.irl IJi■,i■.ihi.■. Bill lenvo: ;!k , liirnlnn, i> i Bennetl A.F. and W.R. Daw.son. 1976. Metaholism. ^t. I 27 Hoi^giei; WAV, and Ct: Sheiftirt. 1979. Cas exchange and trans- ^2.'! in L. Cans and W.R. DaWS'itl. eds. Physiology A. Aca puit duiing iuieriniiteui bcrifhtn|j in eheloniint repnle.v j i it1 mii Prr's, I cmdon. . \ p binl *: . -M2. Beiineh A.L .im.1 I.A. Rupert. ITw rtiljt^bhlk ami ilit-1 r- Liarey F.t.i.. J.M. Teil, J.W, Kam^islier, and fs.D. LusfSorv. l4>7l, >nu..g^i:,! ...... tatu1, .il ; ■ ij-isidi. Pb. ,7-.'! H i N.J.Ij. - ...... K;i uh. A ■ 11 / • i : 137— I'I7,. Son, I'.D. MacLean. f ]. Uofh, anti F.I”. Itoth, ids. 'I he l-Liikigy 1 arriei I.J.R. I^H7r;. T'ht* c-volniioii a f k.u.,.»motor stamina in Endot hermit: Ariliosgurs LQ65
retrapods: circumventing a mechaniL.il constraint. Paleu- Fisher P.E., D.A. Russell, .Vt.K. S'lf^knpl’ R.I-. Harrick, M. Ham Inii iJojiv' l'.V32G-3rt!. m e r and A.A. Ku/mit/. 2ClfK). t ..iritiovaseular evidence for — . !W7^j. l.unjj, vemilalion during walking and iinmin^ fin intermediate nr higher metatmlic nite. m ,(n ornilhischian in four .specie* of-]j tatty s. Exp Ilinl '17:33-42. (JiiutfaiiT Scitncc " ' v ------. J ^ l . Conflict in 1 Uc hy.pitiHl n)useuIo-skeletal sys-tein: franklin Cjj. and H* Ajeltson. 2U(H). An jc lively coniiyitcij documenting an eyohUicnGary Cflti8trantt< Am Z vo l 3 j :64-4— hean vaive. \s tn re Hfifi:H-17-B4s1 tibins and H. Clark. I97ti, Sliitlits on ventilation of CaiintiH Cartier D.R. and C.G. Fnrmer. 2uu(hf Vejrebralfs. Dover, N'ew York, in anchosaurs, Am Zool 4(1:K7-I(1U, Gouid S.,. J V77. I )11lojitnv ynd Fhylogeny. Har\rai'd University (Jolt II.U. Scientific results of an Inquiry irtto lhe e^pkigy 1 're -. ■ :i ■' ' ■.■ l, W.i. And sidUUS oi the Mite nocodile rpj'/c?- Greenfield L,|. LindA.Ci. Mnrrnw. IMci 1. Th. Herbert, and I.1A I’oulson. I9S9, lliochem- v.rieklungjgL\schii;h[e des Her/.ens nnd d ti Truncusarteriosui istry ami |>h y ■ii o 11 >gy ot ,i 11 igator metabolism in vivo. Am Zool der Wirbellhiere. Gegtnhauis MijrpUol lnhrb HitAS-5-H), 2^:921 :.:4. Grig^ G. I^H9. The heart and patterns of cardi.ic Huilfli.ihv in (.oulson Ft, A. and T. Heirnande/. 1979. Fraelor:> controlling gly ■ Croeodilin. Prem Aum Physiol Pharmacol ^kic 2l)t43—5-7. cogen breakdown in lhe alligator, Cmnp BtiKthcfr Phyaiol C ------. ITOl. Central cardiovjicul.ir .mammy and lanctionin M-lJ 15-1JK Gmcodiiia. Pp, in S.t,. Wood, K.li. VVVber, A.R. lit Uccr Ti. 195tS. Fmhiyos and AncvMors. Oxford University Harden s. anti R:. W. Millard. eJ.s. Phh'sjo logical Adaptations Pres:*. Oxford'. in Vertehiares: Hes|iir,iiioti, ('irtulntion, and Metabolism. de Rieqles A. 14 74. £vy|uti(in ot endothermy: histological t*V- Pel ker. New York. ■. ■■ i. ^ ill Them y 1.5; hu. Grigg G.C.. and k. Inbansnn. I9H7. (.'ordwjvascular d^namics jn ■ — . I97K. Sur la classification, la signification fonctionndk CiTJfQfiylUi pnrostts breathing air and during vuUintiiiy aer- ct I'histoire des rissu.n nsjettx dcs iftrapodcs. 3ieme partle: ohit dii'cs, I (.iornp Phyiiol Ti IS7:J^I 3^2. evolution. Ann Paieontol 64:H5-I 11. Grigg G.C.f F. Seehacher, I..A. l^vird, and D. Morris. LWM. tie Ricqli's A.j., K. F ^J isBj and i.R. Horner, jfift), On Thermal relations of large crocodiles, QfltfOiMiiS /'(Jnssus! his.tdngy af some Trjaswc pscudosuchian sichoSaiir* and re free-ranging ir a naturalistic sitnalion. E'toc R Sot Lond B lated taxa. Ann Paieontol Ky:fS7—10 1. Biol Sci 265:1793- 17W, DodjSon P. 1S?5. Functional and ecological StgJiH titan ile of rel- Hargens A.P. 19W7. Graviiulkm.il ^irdiov.iiveular adaptation in i 1 il-J. ;:ro'.\ :i 111 A lllffiW J _7.c. ul (l.ondi L‘ ".J15 .-55. ihe grrark-. Ph'. iokigisi ''ii ■ .ir. I '. .. Farlow [.O., P. Dodson, and A. Chtrrjditly 1995. Dinosaur hi- Hijjrtw P. .md L.I.C t.irigy. 19S4. Shivering thermogenesis in Amiu Rev Fcol Svst 26:443 471. the brooding diamond python, Pylhmi spibtCf splbtts. T’armer C.G. jml U.R. L.ijrrtcr, .JQQO'tfi Fdvic aspiration in the G, ■ ■: i I 1:9 -• '.W-. Amrrican alligator (Attifiiltor nii*ihsippk')tiiil. I fo p DioJ 2D3: Flicks |.\V. I99H. I'atdniL shunting in reptiles: mechanisms, l"7V -l(^‘ . regulation, and physiological fjnctmns. F'p. - J —48-3 in C. ------. Ventilation and £ds eKchange during recovery Gflrts and A.S. (j;min, eds. Bi:tS7—73. phibians and Reptii^, hlrac.i, N .'’ ------. ZNtMh:, Ventilation and gas exchange during walking Hicks J.W. and X ^Vang. I9V9. Hyprtific hvfpmireftatiL'frwm in 1)k- in the Anftfitffti nlligalor lAHijjjftidr m itsitfjp p ien iii, ] flxp anfstheti?etl mnie, Trfiittctfvsscripta. AjI,? I F'h^siuJ 277.'5ilrt— Rlol iU3: J f>7 3 - 1 fi7«. R23. Farrell A.lh, A.K.. (lamperl, and F.T.Ft. I'lauci.i,. I99S. Compilr- 1 lillenius W.I. 1WJ. Turhinates m theu^jstvls: evidem.e for Late i jvl! :i‘ipcL l> jiL heart morphology. Pp. 375-424 id C. cTran*; Permian i.irigins of mammalian endorheisny. Hvnluiion 4.^1: and A.fi. t^aunt, Mr.hrfiboJojiy Cl: Vi^era! Orgam. Society 207-2.’' '. lor the Study ot Amphibians und RcjvliTtt. hlirita, N.V. Hnehstetter F, 1^06. Die KulT^ickcrhivij* ties ULnlfjefisssystems. I tducciii A. 199^, The Origin and Evolutii’in of Hijds. Yale Pp. 21-lfit> in O. I lariwig, ed. Mandbuch der vergleichenden ' ■ i■ £■ rSily I1:e ^, Nnv f I.ivi n ( nnn und expenmeniellen fojl^it^Jungwlehri?. ik r Wirlx'ltiere. Ferguson I4W5. Reproductive binlogv and embryology Fischer, kna. oT rtrjj frr'tfidilinns. Pp. '2'>-4LJ2 in C. Cans, 1". Dilletr, and Hornci' I.R., K. F:nlian, and A. f. de Rieqles. 2001. Comparative P.F..^ Vladeiiion, eds. IJevelopmcnl A. Wiley New York. osteohistology <}f some embryomc and uennatitl ^rillosanrij: I0fc>6 R. S. Seymour, (J. L.. iknnell-blrtmpcr. S- I), jolmsfon. !•>. R. Carrier, and G. C. Cirigg
(JevdfJjiWenlat and behavioral i nip] Lear inns tor djnosaurs. Mihller. eds. Geneiies ol CardiovascLikir PilfitsC. Mari Inns 11 ■; 'ibl' jiogy 7 :3 9 -^ Ni.ib.ofL> fepstpn lordanski !^.N. 1973. The skull oflhe Crotodrlia. Pp. I— Platzaek B.and |,W. ] licks. 2001, H(.\1u(.lions in svMcimt I'DTh^en in C, (jfljib and T.S. Fiirwns, tils. biology of iIif Hepiijia, delivery indLKc a hypiMnewlwli^ stat<: ill itic tutiile Academic Press. London, si-njur;. A111 [ Pliysi< il 2,S i ; K129 ] 301. lanke A. and II. Arnascm. 19‘>7. The complete milochundri.il Poyiw jnnl L- ] indstrftrn. I9S3. Conijiaiativi? and waling as- "lh u iiu of An'i/’ijrcr rffit'itsippwrisfc and ihe separ.ninn be I is-: rtf Ijtif.rt liillJ Tifidy weights wiili reference tn bknid supply tween recent archosauria ibirds and cn>a>dik's'i. Mul Riiil megjlies lanke A., P. Hrpenbeck, M. Nilsson, and L\ Arnason, HJtll and "eardinmegalie.s"’ in iree-living aniiifiiLs. Ann N V Acad The mitochondrial genomes pf the iguana t l£nnn:.i igHttfWl Vi ! In i ..- 1^U. and thf caiman (Cmwin.1 r fratfatfylti's'ii implic-jtlii.ins lot am- Qninn tW . and Mindcil. 199fi. VhKxliimdip.il prneoi'dei' hicitr phylogeny. Proc R Soc Lund B Elio) Sci ^ :c>^3 —3 1. itiihicciii in iluj ^wfutpsi rtw in in ciocrwdile, turtle, and tua- Jam s tJJ.M. 197ft. Energetic-, of survival in HettffKephifllffxta- : 1.1. Xlol HIh'Ji'j;:! ifl Hvi' r .544-2-'I. htp (KtippeUli ihe naked mole-rat (Hodeniia; B4tbyptgid4tf I Reese A.M. 19IB, The Alligator and lt.s Allies, knickerbocker. Hull Uamegtc. Mu5 N*t Hfti i—H7. S.evi "..jrk. Johansen K- ).y7i. lieart and circulation in gill, ykjHi rind lung Re ill li.E.H. 19V7. Dinosaurian physiology, the caie lor "in breathing. Respir Physiol 14:193-210. termediate" dinosaurs. Pp. -J'1^^173 in f.O. Fiirluw Hnd M.K.
]o(W!i 1>.R- and ( j. Shell on. l'WJ. Thr physiology of the alligator Hre»-Siirmiin> eds. 1'he Complcle t>lnCfHhijlt, Indiana l.'rii- hrvri: It'll ^trUi' flbw liiifftftii-flint (ighim -left .shunts. I F.xp vi.-rsil',- ■■■■ I ■ . . rvnglnn. bio, l /{>■.Li/—2fr9. KitlMrdson W.k. IW9. Vertebrate evolution: the develop mentai Kumaifj^'a V, and M. Nishida. IU95. Vitiations in rnilochnri- origins m" adult variation. Bit>Essays 2l.:0iM-M3. Richardson .Vl.K., Flanken, M.L. Cmmcratne, Pieau, A. driaJ rR\'A gene organization ol' reptiles as phylogenetic T, C. Riynjud, I-. SelwoiKk Iind U.M. Wri^til. 1^97. I^htw :s ne i aarkers. ' lot bin. : ■vol ’ 2 highly co^SirVisd ctnbryonic it.'sge in the \'eirebrates: fmjfli I fe M.S.Y. 200|. Molreuie-s, morphology, and the irumuphyh unions tor crnrent theories of evolulitm and development. of diupsii.l TepiiSes. GnMrlb /.nol 70:1-22. Anaif Fnihrvi ;9fi:4t I1.n'.. Martin A.P. and S.R. Prilumhi. 1993. ik>dy si/u, mTtflholH r.nc, kichardsHin M.K. and C Ketrck. 2002. l laeckel's ARC of i-vo- generaiion lime, and thu molecular dock. Proc N.ill lutior. and development. Biol Rev 77:^)5-523. S i 1 VA '-■'j.-iJUT JiM I. HoiHvanJ S., F. Bmwii. and L.N. K^tz. 194.5, Ihe pulmoiiai'v Murrish D.F_ and K. Schmidt-Nielsen. 1970. Exhaled air tem .1 fe al pressure. Am l-lear- j “■ 1. perature and water conservation in lizards. Kespir Physiol Ruben I.A.. W,|, Hillenius, N.!.R. (.r.-isi, A, LcReh. T.IX lones, I'' 121 LjH Pi C&rm ).K. Homer, and £Vr 1^ 9*1, The nielabnlie hJiiiTeJ-i Kl'KL, S.I!. Hugpin.t, and H.f;'. Hoff. J970. The nature of .status of some l.ate tjetacetius dinosaurs. Science 273: i 204 tlie ventdatoi y period in crocodilian respiration. Ilespir L'lv. s 1207. in! 10. ■ MS. Ruben f.A., A. I .uiiuh, W. I lillemus, N. tit ist, Lind T. |ones. OfccrkiW'fiw Tn C-C. Fifriitet, I vv. Hicks, .uni RJ.. liraiiieni. 19^7. New insights inlo the nietah^ihc physiology ol d in o i 9'7'm-. t .onlrihiilLOii of gidar pum ping rn |>jn^ vcnnlation in saurs. Pp. 505^518 in I.O. PirrlL'iv.' .iinl M.K. HicK-Siirm.m, monitor ll/ards. Scccnce 2H4:1 661 - it>(-i3. eds. I Ik’ tJeiinpleic Dinosaur. Indian.! l^niveisily Pn I’aladino KY,, M.P. O'Connor, and |.R. Spufila; 19 ^ . LVIi’tdli- tlli :iii iiiy,I1 ■■>. filisiri r>f lefltherback turtles, gijiantothermy, anti thermo ret; 1 ; ■ ■ "I I V ] Vi1 ■ i. ■ . 11 - [ ■ 1. ■ ■ 1 , 1 ■ .| 1 ■ * 1. . . i ■ re- ulation Bf dinehsauj!;.' Nature 34-3L i t —S60. ".iiii u'lsliips tti Their extinction. 1 Paleontul 3V:497-30I. !'nrn!>h 1.M-, I9ft7. The fVfifein uJ Lroindilkrn kvi'Lnnjiiun. Pa Salisbury SAV. and E. Frey. 200 i. A biomeehanical transfor ! iihink-..-.- 13:59^14. mation mtidel fwr ihe cyrjhiUun of sen 1 [-spheroidal .irli( i;------—. 19^7- Evolution (if the ar^hiis-mrs. Pj 1. ]9l-20.^in |.0. iitirrris hiii^een ad^oinin^ verreliral bodies in cri^codilians. Fflriot'-* iind M.K. KTTH-Snrm.ni, eds tlK CiCiiiip.lifte llfun- Pp. ft!">-134 in ti.C. Gngg, F\ Seehacher. and C.E, Franklin, saur. Indiana .Univtrsily Press, Rlofsinin^inn. eds. t.TociKlilian iliology and Evnlution. S.lirre'V ReaHy. Chip- Perry s.F. iy90. tjas cifhafigs; strategy in 1 lie tfj]< iTHa^dlit- a pi 11 \, Norton. rncirp ho metric study. I Comp Physiol Ii I ii9r7fhl-7ft9. Sehmidt Nielsen K.., F R Flainsworth, and D.E. Murrish, P>70- Peters R.H. i'>S3. The Ecological Implications uf [Indy Si^c. Counter-curncnt hear MrHaTijRr in the rrspiriitorv fi.isnsj’cs: Cambridge University Press, ! i^mbritlgc. rifri-i cu Waff)' .md heat balance. Hespir Physii>l 27b. Pierpont and I.FI. Mt)1icT- I9fc. Conacriltal carsliac !>eeh^cher F. 2003. Dinsisaur body tempemmres: theoceurrL'nce nujIfnrniatinns. Pp. I in M-E.M- Pierpont and f.!l. o| endolherm} and et l“ lliermy. Pal**ihiLl]t^y 29 I0.ti- j 22 . Endotti&rmfc AjfthoSfltirs 1067
Seehacber F., (p.C.. firi'gfi iml I,A. fKjipd. 1999. Ctiiccd.lkt Di olisni, enf!gelics, ami ihei iiimiL'^ul.slinn dtiring l^rooding oi dinosaurs: behaviouial tli^lTlQintgllWftli in very Urge ce- sstiikes i>t the genus I'vtlw u ilieptiliii, bniidaei, ^ytiliijiiea loiherrm leads to high and '.table body femperal.uriis- I E*i1 19M1S. l: ■] ’-fift WtJkvT A.I). 1470, A revision of the lurassic replile Jicrcno HC LiSl Basal arehtvsaurs: phylogenetic rd^ttoittfbjps v ia v r I Marsh), wjlh remarks on the class ihcatirtn ot croco- and I ljril I ii irial implications. I Vertehr Palconmi 11.1-53. lili i fi ln ,' i,i t R ,;., Lofii 1 B ” Sereno W;., H.C.l;. (jirsson, QA> Sidor, and B- Gado, 2001. Wang L, f, Aliiniiras, and M. A^eissun. 2002. intracardiac flow The giant trnctsdyJiform SmsHtit'toiS trom lhe Cretaccous oi separation in an in silu perfused he.m frfitn ftiittrwis'f python Africa, Science 244:17s I fi-I"! 9. PyfJrow intjhtnis. I Lip Biol 205:2717-2725. Sevmour R.S. 1976. Dinosaurs, endotiiermy, and fct[eiod jiriis'- Wung T, ). Allimiras, W. Klein, and M. Axel'i^m. 2fi03. W n- '.i-.1. N j urc 2f> j. i) ;;.n'i-!.!ilvriamii *- in .■..'■■■ ■■: jjepajLii .i i — . 1982, Physiological adnptiitionN to aquatic life. Pp. I- ■ ■ irv irl.l ■'■ : i ■ | ■. . [ i. ' : il /' ■ ■ 12-5 L 51 in (',. CuMUi and H.H. P a iiX ts;ls, Biblpgy o fth e Reptilia. I. i. Physiology D: Physiological Kcoltvgy. Academic Press, New Wang T., D.R. Carrier, and J_->Vj Hicks. 1447. Veniilanoii and
' ■ i I k . gns exebange in fi/ards during treadniill exercise. | Lyp Hin I ------. L9S7. Scabne o t cardiovascular phy5KHt>vy ir sjidkcs. ■ . HJ'J \m '£» : ■■ -104. Wang T., AAV. Sniits, and W.W. Burggren. I'Jmfi. Puli nonary ------. 200 i fl, Hjophysiis* and physiology of temperature peg filt^lhjr in reptile*. Pp, 2LJ7-.1?( in C. Gans and A.S. Gaunt, uiatimi in thermogenic (lowers. iiLttsd Rep 2l:223-23ti. eds. Biolop1 ts! the fiejitilia. Morplink.i^y G: Visceral Organs. ------. 2001 fr. Preface til '’Hbysjoliijfy and physiological ecol SiXitty for the Study oi Amphibians and Reptiles, It+iaca, N.Y. ogy'’ Pp. 263—264 in . L Rradfntd. ^35. BkffiuJguy and birds. I M^rphol ltiL22t 2Jl). tL'iiiHin.H jniJ adil-|>.m‘ rc'gl Nation in th? salt-waler crocodile, WtjhVti.jjW, ami t'„ c.ans, ILJ^2. t ".,i 11 r>p ing, i n Crocodylus blm* Cwcildyitfi. punHJfl, at res! and aftei exhansiive weitise. J n relied ion ot terreslrial activity? Rec Aust Mus 34: 1 Bi.nl ’ IK; <-l ■■ ). 6I.U- 'iIp. Seymour R,S. and A. Hlaylock. 20F10, Tile principle ol Laplace Webb G.| ,W., G.C, Sack, R. Buckn ih, and S.G. .Manoiis, 1983. and scaling ol blood pressure and ventricular wall slips') in An examination of Crrvtiffyfid.' fiorrJir;y nests in two northern nianntialii and birds. Physiol Biochem Zool 73:389-403. Au^ii'alia freshwater swamps, wilh an Linalysis ol embryo Seymour R_S., A.R. Hurg&rts, and T.L Pedley 1993. The heart mortal i y. A hist Wiltil i :: 571- 605. works against gravity. Am J Physiol 265:K7J 5-K720. U'ettstein O.V. 1934, t!rocr>di!ia :. tv- 521—424 in W. KOken- Seymour RS- and H.H. Lillywhite. 2. R. [ones. 1991. l he physiology of Ihe alligator dinttsaur with integumenEary structures from C.liina. N.ilLre heart: the cardiac cycle. J Lip Kin! I5?t:539-564, ^99:350-35-1. Thomas R.D.K. and E.G, OLson. L9Hu. A (.'.old Look Jt the Xu X., X.-L. Wang, .uni X . VVu. ] 999t. A dmmaeowjurid VVj mi -Blooded Dinosaur1!. American Association Por the Ad- dinosaur wilh a filamentous inle^utiieill Imni Yijii,m t“or- \ ■ ■ '1'ierii ni Stiem ■, W.t' i nfH.ni 1 '■(!. n u ■ir, n| \ him N. iluj e :2i'. 266 Ulrsch ti.R. and IJ.li. JiHckson, I9K2. lAing-lerm SLjbrTierUfnce Vonrig H.A., ll.B. UlTyiwhitf, and Rij Wassersug. 1493. (.in the at J°C ol the turtle, Chrysitmys pictu /vWri, in normoxlc and .ilniclure nl the anrlK ■.-.'lv:'> in Mkikes [Reptilia: Serpentes). severely hypyx.rc waiter. I. Survival, gas exchange, and acid- 1 ' lorphul 1' 141 ' 54. base status. I Kx.p Biol 9 6 .11-2H. ■' C.,K. 197-1. CrottHjilian g;it1oping: fl.fi ufltqtsJ j:iit for rep Vinegar A., V.l-i. Hutchison, jn d K,CH. D owl int. 1970. Merab lilt1.. ( r.ipeia 1974:550 55i, Copyright of Physiological & Biochemical Zoology is the property of University of Chicago Press and its content may not be copied or emailed to multiple sites or posted to a listserv without the copyright holder's express w ritten permission. However, users may print, download, or email articles for individual use.