Evidence for Endothermic Ancestors of Crocodiles at the Stem of Archosaur Evolution linger S. Seyniblir1 ln(roduc<ion Christ/mi 1.. Hertnett-Stanijifcr' The distinction between endolluTmv and cctntherniy is one of Stuiya 13. lolini-Lon1 the central characteristics that divkks vertebrate li no rials Al­ Dm id R. Can ier though there is variability in flie liiuuig, precision, and k-vtil of Gordon L . Grijig' [he endolhctniit Mate amonp biuls ami niammaU, bolli gnuipi 'UtpafHittfrit of' F.iiviionniental Biology, University ol are clearly distinguished from the niaionly i '1 ^(rrftleitriie ivp- Adelaide, AdtJf-aiit'#, South Austnlia 3i$5, Australia; S illie r lilo, itjipMhiaui, aiul li'h. Bird1, and mammals lypticafly hitvf for Mu 1 logical Microscopy, University of t.’.incinn;ni, 3'135 cnnsitlerahh' higliti htjtly rempciiiiures, nn'inbolic rates, :nid Eden Avrnlir, P.O. Llox 671 1, Cincinnati, Ohio 4li*67- vtimniii. Their body temperainrfs an: usually physiNlogitally reg­ (152k llepartnnent of tlioiogy, University of Utah, Sail Lake ulated wiltim (i nam'iv ran^t’, :mcl lheir metabolic jjailuvays are' (lily, L'.tojrf K4I 12; ^tttpartnjEflE of Zoology, University flf generally aeonbi: linring neit and jiarvity. b.ctiitheiTn!) sir* ib.rr- Queensland. Brisbane, Queensland 4072, Australia ncterised by environ men tally dependenl bruJy. temperatures, lou- meijboiic rates, am! relianie on anaerobic (wihways for intense lud imSuslfimabie acln il y. I’robahly because of (Ik1 parcelved di- choloiny bftween livLdfe fiidoiheiTns and eLloiln'nns, lhe t|uts- lion Of The nKt.ibolic .statu.', of v^lincl vertebrate ^poujhs ha,s liten e\tens|vtly dc.bmlet! fThoma.s and i )Koti Kjtker I9^f>; 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:<my|icntrans- ptiri capaeit\'L which Ihey a'.iiise ^vitli higjier blood liq(W rates and hcmttglftbin levels. Llf/ated cardiac onlpul in endotherms is .issHicialed with mai'kuilb higher *.ystemic a fprifll Itiood prc'S' t \'i i v ■■ i .-i ■ . fit,- <!,i i i ■ i 'i! Z i * t t i TTtfil | ] -I M Ks < '■'< K ^ v 2(H M by The sure (Kodbard et at. 1^49; lolian^'n 1^72. fig. I i. The e.Tpl.i- University nf dtfc^i\ All rcsen-cd. nanoii (hit rhi'ii high systemic hliitrtl pressure and app!'ci.iabli.' 1052 R. S. Seymour, C, L Beimel I-Stamper, S. D. Jufiristoh, IX R. Carrier, nntl G. <irig^ 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 <jjl1 ireK- clear, bur vh: will present above n I'sllmates flf .sysicmic arteriiil bliN>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<iurs were capable flf producing wstemic th;it biff!) pulmonary biood pjwtsijftis uld m use fluid Ipi'mMSitres ivifU xvithin thn- endulherniic range, which would have [ill ration into the air spase.-, (pulmonary ctli.-m.i!> and inhibit :ei|lih'l'i! the lunctkmal se|:ar.ilion of systemic and pulmonary ga> exchange i.Wrtrig tt al. I yyH>. Although fb<r .ui;itiimic,-illy blond in a lour, chambered heart. However, the jnalvsis c.mnol undivided lien US of some <jTs,\-c;piIlieuI reptiles (e.g., nvmilpi determine ivhat led tt) die evrhlutlnn ol sui'h .i beau and high and large teTWfi.MiTi snakes) cun generate ;ipprccia hiond pressLire; thest features could have evolved initially in ble pressure separation and moderately hijih pressuies (burg- support of ei idol her my, large tnnly size, or both- If It can be grcn and lobftiHen 1983; Seymour I9S7; Wdrtg et al. ZOfiL shown that they Ociilrred first in shHirt animals, it wouid be most reptiles have sysiemic systolic pressures thill faTl consistent witb etidotbevmy as the primary e<.trrti,itf. o'msiderjhiv tftulrt o ftfe mammalian or n via it itcmm* (cf. Hick* I his report expands .m earlier presentation and provides 1WK for reptile"-, and Seymour ,md filaylilck i(Hjt) lor birds ithd evidence that the small ancestors of crocodiles possessed |uuf- rtiiitttrtiitlij, Hearts nf min<;ruk.[>dliian 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<ik" avian and mammalian fr)Uf- Ironically, tbe hearts oi livingectothermic crotodilians pmvidt; cbiimbened hearts do not.