13-1999 respirphys117

Respiration Physiology 117 (1999) 73–83

Frontiers review

Gas exchange potential in reptilian lungs: implications forthe dinosaur–avian connection

James W. Hicks *, Colleen G. FarmerDepartment of Ecology and E6olutionary Biology, Uni6ersity of California, Ir6ine, Ir6ine, CA 92697, USA

Accepted 1 June 1999

Abstract

The theory that birds evolved from a group of small terrestrial theropod dinosaurs has created much controversy.One argument proposed against this theory is that the lungs of early theropods were incapable of sustainingendothermic gas exchange requirements and could not have given rise to the lungs of birds. A reexamination of thecomparative physiological and morphological literature combined with a theoretical analysis of gas exchangepotential indicates that non-avian lungs would not constrain the gas exchange requirements of early endotherms.Furthermore, our analysis suggests that factors besides diffusive gas exchange were important in the evolution of thedistinct morphology of the highly effective avian and mammalian lungs. © 1999 Elsevier Science B.V. All rightsreserved.

Keywords: Endothermy, dinosaurs; Evolution, dinosaurs to birds; Exercise, maximum O2 uptake, dinosaurs; Metabolism, dinosaurs;Theropoda, dinosaurs

www.elsevier.com/locate/resphysiol

1. Introduction

A major controversy in paleontology, that hasreceived considerable attention, concerns the evo-lution of birds and their relationship to theropoddinosaurs (Ruben et al., 1997; Padian and Chi-appe, 1998; Unwin, 1998). Much of this debateresults from the analysis and interpretation of

anatomical features shared in both birds andtheropods (reviewed in Ruben et al., 1997; Chenet al., 1998; Unwin, 1998). The description of arecently discovered fossil of a small theropoddinosaur, Sinosauropteryx prima, from northeast-ern China adds fuel to this debate (Chen et al.,1998). This fossil exhibits well preserved integu-mentary structures that may provide the first evi-dence of simple feathers (Chen et al., 1998;Unwin, 1998); suggesting an insulative functionand an endothermic physiology (Unwin, 1998).

One requirement of endothermy is a continuoushigh rate of oxygen delivery to rapidly metaboliz-

* Corresponding author. Tel.: +1-949-824-6386; fax: +1-949-824-2181.

E-mail address: [email protected] (J.W. Hicks)

0034-5687/99/$ - see front matter © 1999 Elsevier Science B.V. All rights reserved.

PII: S 0034 -5687 (99 )00060 -2

J.W. Hicks, C.G. Farmer / Respiration Physiology 117 (1999) 73–8374

ing tissues, thus requiring a highly effective oxy-gen transport system. Ruben and colleagues(Ruben et al., 1997) examined photographs ofSinosauropteryx prima and noted the possiblepresence of a liver or liver-like structure. Thisobservation combined with specific aspects of thepelvic structure lead them to suggest thattheropod dinosaurs used a hepatic piston breath-ing mechanism similar to that found in extantcrocodilians. These investigators concluded, there-fore, that the lung of Sinosauropteryx was mostlikely a non-avian (reptilian) septate lung (Rubenet al., 1997). In addition, they proposed that sucha lung would have been incapable of sustainingthe high oxygen exchange rates associated withendothermy (Ruben et al., 1997).

More recently, an examination of the fossiltheropod, Scipionix samniticus, lead these authorsto suggest that the liver subdivided the visceralcavity into a thoracic and abdominal space(Ruben et al., 1999). This finding was purportedto provide additional evidence that theropod di-nosaurs may have used either a diaphragmatic ora hepatic piston breathing mechanism (Ruben etal., 1999). In response to Ruben and colleagues,we presented a preliminary analysis that arguedthat high gas exchange rates in theropods wouldnot have been constrained by the presence of anon-avian septate lung (Hicks and Farmer, 1998).

In the present paper we present, in detail, ouranalysis of the gas exchange capacity of the non-avian septate lung and address whether the car-diopulmonary system of reptiles is capable ofsupporting the metabolic rates of active en-dotherms. This analysis used two approaches.First, we examined the comparative physiologicalliterature and determined that the cardiopul-monary system of reptiles does not constrain en-dothermy because in some extant species theoxygen delivery rate is as great or even greaterthan in some endotherms. Second, we used anintegrative oxygen transport model combinedwith morphological and physiological values fromthe literature to calculate the oxygen transportcapacity of the reptilian cardiopulmonary system.Our theoretical analysis shows that conservativemodifications at each step in the oxygen cascaderesults in gas exchange rates approaching ‘typical’

endothermic values. However, during the courseof evolution natural selection gave rise to themorphologically distinct but functionally similaravian and mammalian lungs. It appears that theevolution of these distinct structures was notdriven by gas exchange requirements alone, butwas influenced by selection on other factors. Thedistinct morphology of the avian and mammalianlungs may reflect historical differences in ventila-tory mechanics that were present in bipedal ar-chosaurs and quadrupedal synapsids.

2. Overview of the oxygen transport cascade

Vertebrates meet their long-term energy de-mands by aerobic metabolism, dictating a contin-uous and adequate supply of oxygen. Thetransport of O2 from the surrounding air to thesites of ATP production (mitochondria) resultsfrom the co-ordinated interactions of four transfersteps. These steps function in series and includelung ventilation, diffusion of O2 from the lung gasinto the pulmonary blood, bulk transport of O2 tothe tissues by the cardiovascular system and diffu-sion of O2 from the tissue capillaries into the cellsand ultimately the mitochondria (Fig. 1). Thetransfer rate of O2 (V: O2

) at each step is repre-sented by two convective and two diffusive equa-tions (Fig. 1). Each equation can be simplified byexpressing the physiological variables necessary toproduce a given V: O2

for a given partial pressuredifference as a conductance (G). Consequently,the two diffusive steps express the diffusion capac-ity of the lung and the tissues (DLO2

and DMO2,

respectively) as Gdiff. The products of convectiveflow rates (ventilation and cardiac output) andtheir respective capacitance coefficients for oxygenin the lung gas and blood (bgas and bblood) areexpressed as Gvent and Gperf, respectively (Piiperand Scheid, 1975; Fig. 1).

Generally, during resting conditions, V: O2is in-

dependent of O2 delivery. However, when tissueoxygen demands are increased, for example dur-ing activity, G at each step in the oxygen cascadeis increased to meet the new energy demands. Asmetabolic demands continue to increase, this pro-cess continues until structural and functional con-

J.W. Hicks, C.G. Farmer / Respiration Physiology 117 (1999) 73–83 75

straints at each step limit continued increases anda maximum V: O2

(V: O2max) is reached. These con-straints include convective transport by the lungs,the diffusive limitations in the lungs, convectivetransport by the cardiovascular system and diffu-sive limitations in the tissues.

3. Oxygen transport capacity of extant reptiles:does the reptilian cardiopulmonary systemconstrain endothermy?

The Mesozoic Era (240 to 65 million years ago)ancestors of birds and mammals most likely pos-sessed a reptilian-like oxygen transport system(Fig. 1; Perry, 1983). Consequently, these animalsare often considered to have been incapable ofsupporting endothermic rates of restingmetabolism or activity metabolism (Ruben, 1995;Ruben et al., 1997). This idea was based, in part,

on a purported unalterable constraint on the pul-monary anatomical diffusion factor of the non-avian septate lung. This constraint was suggestedto be due to a large blood–gas diffusion barrier inseptate lungs and the passive participation ofediculae or faveoli in lung ventilation (Ruben etal., 1997). However, in a number of active rep-tiles, the rate of respiratory gas exchange duringactivity surpasses the resting and activity VO2

ofseveral endotherms. For example, the monitorlizards (genus Varanus) are exceptionally activeectotherms with relatively complex lungs and afunctional four-chambered heart (Bennett, 1978;Perry, 1983; Hicks, 1998). Measurements of V: O2

during treadmill exercise indicate that the car-diopulmonary system of these lizards is capable ofsupporting a V: O2

, during exercise, equivalent to orgreater than that found in several similar sizemammals walking at similar speeds (Fig. 2). Otherhighly active reptiles with multicameral lungs (e.g.

Fig. 1. Schematic of the four step process in oxygen delivery. Each step is represented by two transfer equations. The Fick Principledescribes the movement of oxygen by the lungs and circulation. Fick’s Law of Diffusion describes the diffusion of oxygen from airto blood or from the capillaries to the mitochondria. Modified from Wang and Hicks (1999).


Fig. 2. (A) V: O2in selected mammals walking at 1–1.5 km h−1. Data for mammals from (Crompton et al., 1978; Taylor et al., 1980).

Range of V: O2values for monitor lizard walking at 1–1.5 km h−1 (hatched bar) from (Mitchell et al., 1981; Wang et al., 1997a;

Owerkowicz et al., 1999). (B) V: O2max in a hypothetical lizard calculated from the integrative oxygen transport model (see text fordetails). Regression line represents the predicted V: O2max of mammals (Lindstedt and Thomas, 1994).

sea turtles) also have oxygen consumption ratessimilar to endothermic values during activity (Jack-son and Prange, 1979; Paladino et al., 1990). Hencean explanation for the ectothermic physiology inthese reptiles lies somewhere besides their lungmorphology. Clearly if the cardiopulmonary sys-tem of the Mesozoic ancestor of birds and mam-mals was similar to that in extant reptiles, it cannotbe concluded that it constrained them from achiev-ing or supporting endothermic-like rates of gasexchange. However, there is a wide range in V: O2max

among endotherms and ectotherms of similar sizeat similar body temperatures (Bennett, 1978). Forexample a 1 kg banded mongoose has a V: O2max of117 ml kg−1 min−1 (Taylor et al., 1980) while a 1kg monitor lizard has a V: O2max of 20–30 ml kg−1

min−1 (Mitchell et al., 1981; Owerkowicz et al.,1999). Therefore, we addressed the question ofwhat modifications in the oxygen delivery systemof an ectotherm would be necessary to supporthigher rates of oxygen consumption.

4. Theoretical analysis of the reptilian oxygentransport system

The transfer potential of the oxygen transport

system can be increased by modifications in thedesign properties or morphological features thatdetermine each of the four conductances (Weibel,1984); e.g. increasing stroke volume of the heart,oxygen carrying properties of the blood, diffusivecapacity of the lungs and tissue). Recently, Wagner(1996) described an integrative model of oxygentransport that can be used to determine the effectsof modifying each transfer step on V: O2max. Animportant aspect of this model is that it takes intoaccount that PO2

at any given point in the O2

transport cascade is dependent on the O2 transferin the previous step. For example, at V: O2max, the PO2

of the blood leaving the lung is determined by thePv̄O2

entering the lung and the conductance ratio,Gdiff /Gperf (Piiper and Scheid, 1991). Simulta-neously, the Pv̄O2

entering the lung is determinedby the arterial PO2

(PaO2) entering the tissues and

the diffusive and perfusive conductance ratio in thetissues. Thus, PaO2

is dependent on PvO2, andPv̄O2

is dependent on PaO2. The analytical approach used

in the Wagner model inherently satisfies the cou-pling and mutual dependency between gas ex-change in lungs and tissues.

A detailed description of the integrative oxygentransport model is reported elsewhere (Wagner,


1996; Wang and Hicks, 1999). Three equationsdefine this analytical approach. First is the stan-dard mass conservation equation or Fick Princi-ple. This principle states that the differencesbetween the rates of O2 inhaled and exhaledequals the product of cardiac output and arte-rio-venous O2 concentration difference acrossthe lung. Second, a differential equation, Fick’sLaw of Diffusion, represents O2 flux from alve-olar gas into pulmonary capillary blood. Thisequations takes into account diffusional conduc-tance of the lung for O2 (DLO2

), transient timeavailable for O2 diffusion, total pulmonaryblood flow, alveolar PO2

(PAO2), and the profile

of blood PO2along the pulmonary capillary.

This second equation is integrated over the totalcapillary length to determine the end-capillaryPO2

, which is taken to equal PaO2(Bohr integra-

tion). The third equation is analogous to thesecond and represents the unloading of O2 bydiffusion from the capillaries within the muscleto the site of aerobic metabolism, the mitochon-dria.

Briefly, the model simultaneously calculatesthe oxygen flux at three levels: (1) in the lungsbetween the inspired air and the lung gas; (2)between lung gas and pulmonary blood; and (3)between systemic blood and the tissues. Atsteady state, V: O2

is identical at all three steps.Many of the parameters used to calculate V: O2

ateach step are determined by V: O2

at the twoother steps. This coupling and mutual depen-dency between gas exchange in the lung and tis-sues requires that the solution to the equationsare iterated by estimating and entering valuesfor PAO2

, PaO2and Pv̄O2

until a unique solutionfor all three compartments is achieved.

5. Oxygen transport potential of the reptiliancardiopulmonary system: results of the theoreticalanalysis

To address the question of what modificationsin the oxygen delivery system of a reptile wouldbe necessary to support higher oxygen consump-tion rates, we determined the effects of modify-ing several parameters in the oxygen cascade on

V: O2max in the monitor lizard Varanus exanthe-maticus. We chose this animal because the re-quired input parameters for the model (initialconditions) have been experimentally determinedat V: O2max (e.g. cardiac output, hematocrit, lungPO2

and PCO2, oxygen carrying properties of the

blood, etc; Table 1). From these initial condi-tions (first column Table 1), we modified threebasic parameters either separately or in combi-nation. These included an increase in the maxi-mum cardiac output, blood oxygen capacity andpulmonary diffusion capacity (DLO2

). We deter-mined the V: O2max that could be supported byincreasing maximum cardiac output by 25% andexamined a greater range of values for oxygencarrying capacity of the blood, with an upperlimit set by values found in endotherms. Finally,it is important to note that because we wantedto gauge the gas exchange potential of the lungof a theoretical reptilian-like Mesozoic animalwe constrained all pulmonary morphologicalmodifications within a range of values measuredin extant reptiles (Perry, 1983).

The analytical approach was straightforward;increasing the diffusional conductance of themuscle (DLO2

) simulated an increase in tissueoxygen demand. In response to the increasedoxygen flux rate we adjusted the variousparameters at each transfer step so that gas ex-change in the lungs and tissues were matched.The individual parameters were adjusted tomaintain arterial oxygen saturation above 95%.The assumptions for the analysis were similar tothose previously described (Wagner, 1996; Wangand Hicks, 1999), and included no ventilation/perfusion inhomogeneity, no perfusion/metabolism inhomogeneity in the muscle, steadystate at all points in the O2 pathway, and thePO2

in the mitochondria is zero at V: O2max. Wealso assumed that during intense activity thelung ventilation increased to maintain a lungPO2

of 127 torr (Mitchell et al., 1981; Hopkinset al., 1995), and that no significant intracardiacmixing of oxygenated and deoxygenated bloodoccurred during exercise (Mitchell et al., 1981;Wang et al., 1997b; Hicks, 1998).


Table 1The effects of modifying oxygen delivery system on VO2max in a 1 kg lizard, Varanus exanthematicus at 35°Ca

Initial 25% increase inPhysiological variable Doubling oxygen carrying Increase DLO2oxygen carrying

cardiac outputcondition capacity of blood capacity and cardiac output

0.683Ventilation (L kg−1 min−1) 1.24 1.47 2.30.350Cardiac output (L kg−1 min−1) 0.438 0.350 0.438b

127 127127 127PAO2(torr)

23PACO2(torr) 23 23 23

105 9895 97PaO2(torr)

24 24Pv̄O2(torr) 2034

10 2010 20[O2]cap (vol.%)3.5Hills n 3.5 3 3

40 3040 30P50 (torr)0.42DLO2

(ml min−1 mmHg−1 kg−1) 0.42 0.59* 1.06c

DMO2(ml min−1 mmHg−1 kg−1) 0.810.42 0.94 2.02

96 9796 97Arterial (Sat%)7.3 12.3(a–v)O2 (vol.%) 155.8

35 3535 35Temp32V: O2max (ml kg−1 min−1) 4320 67

a Physiological parameters: initial conditions are from measured values in this species at VO2max (Gleeson et al., 1980; Mitchell etal., 1981); DLO2

are estimated from morphometric data (Perry, 1983) and assumed to double during heavy exercise.b DLO2

increases from the effects of hemoglobin concentration (Marrades et al., 1997).c DLO2

estimated from modifications of multicameral lung. Ventilation calculated by assuming a gas exchange ratio (RE) of 1.1at VO2max (Mitchell et al., 1981; Wang et al., 1997a). VO2max calculated after model from (Wagner, 1996).

5.1. Increasing the maximum cardiac output

We first determined that a V: O2max of 32 mlkg−1min−1 could be supported by increasingmaximum cardiac output by 25%. This VO2max isapproximately 30% of the value usually quotedfor a ‘typical’ 1 kg active endotherm (V: O2max=100 ml kg−1 min−1; (Bennett, 1978). Intuitively,to support the typical V: O2max of a 1 kg endotherm,the maximum cardiac output could have beenincreased 5–10-fold. This modification in maxi-mum cardiac output is appealing for its simplicity.The Fick principle indicates that for a given oxy-gen extraction, higher levels of oxygen transportwill be supported by higher cardiac outputs. Fur-thermore, higher cardiac outputs are usually cor-related with higher a V: O2max in all tetrapods.However, as previously discussed (Ruben et al.,1997), increasing the maximum pulmonary bloodflow 5–10-fold above normal ectothermic values,without additional modifications of the pul-monary vasculature, would increase the possibilityof pulmonary capillary stress failure (West andMathieu-Costello, 1995). In addition, such high

blood flows would significantly decrease the tran-sit time of blood through the lung, allowing lesstime for diffusion of oxygen and resulting indesaturation of arterial blood. For example, usingthe input values for Varanus exanthematicus andthe integrative oxygen transport model, we predictthat increasing maximum cardiac output 10-foldresults in a reduction in the arterial oxygen satu-ration to values below 80%. Since arterial desatu-ration does not normally occur at V: O2max inlizards, we concluded that a 10-fold increase inmaximum cardiac output, without modificationsof the other transfer steps, would not haveoccurred.

5.2. Increasing the maximum oxygen carryingcapacity

Second we determined that a V: O2max of 43 mlkg−1min−1 could be supported by only modify-ing the oxygen carrying properties of the bloodfrom the values normally measured in varanidlizards to those more typical of endotherms. Wedoubled the oxygen carrying capacity from 10 to


20 vol.% and changed the shape and position ofthe oxygen equilibrium curve (Hill’s n decreasedfrom 3.5 to 3 and P50 decreased from 40 to 30torr to insure adequate O2 loading in the lung;Table 1). In our theoretical approach, the parame-ters describing the oxygen dissociation curve arewithin the range measured in extant reptiles(Wood and Lenfent, 1976). The larger oxygencarrying capacity could be achieved either bydoubling hematocrit from the typical ectothermicvalues of 20% to the values normally measured inextant endotherms or by increasing mean cellhemoglobin values. Hematocrits approaching 40%and hemoglobin concentrations of 12.5 g/100 mlblood have been reported in extant reptiles (Gar-land, 1993).

5.3. Modifying the oxygen cascade

Finally, we considered the effects of simulta-neously modifying several components in the oxy-gen cascade, increasing oxygen carrying propertiesof the blood, increasing maximum cardiac output,and modifying two parameters in lung morphol-ogy; surface area and diffusion barrier.

Three basic lung types occur in the reptiles:unicameral, paucicameral (transitional) and multi-cameral (Perry, 1983; Dunker, 1989). The multi-cameral lung is the most complicated, with thecentral lumen divided into numerous smallerchambers (Perry, 1983). Reptiles do not necessar-ily have a thicker air to blood gas barrier thanmammals, as has been claimed (Ruben et al.,1997); the barrier to diffusion between air and thecapillaries in the lung is, on average, about thesame for mammals and many reptiles. In reptilianlungs, the harmonic mean thickness (tht) rangesfrom 0.46 to 1.0 m compared to a range of 0.26 to0.62 m in mammals (Perry, 1983). Consequently,the higher diffusive conductance of the lungs ofmammals is primarily due to a vastly greatersurface area (:10-fold) for gas exchange (Perry,1983; Glass, 1993).

It has been suggested that multicameral lungswere present in the Mesozoic reptilian ancestorsof birds and mammals (Perry, 1983), thus ouranalysis focused on this lung type. In the multi-cameral lung the respiratory gas exchange area,

located in the dorsal region, could be increasedthrough elaboration of the intercameral septawhile maintaining a membranous region in theventral portion of the lung (Perry, 1983). Thismodification could be achieved without significantchanges in total lung volume, producing a highlyeffective gas exchange organ characterized by ahigher DLO2

, high compliance and low work ofbreathing (Perry, 1983).

Our theoretical modification of the multicam-eral lung and calculation of the resulting diffusioncapacity required the following steps. In the lizardVaranus exanthematicus, the parenchymal volume(that volume of the lung devoted to respiratoryfunction) represents 29% of the total lung volume(displacement volume, VL=307 ml kg−1; Perry,1983). However, in multicameral lungs of otherreptiles (turtles and crocodilians) this value can beas high as 45% of VL. Using this upper value forpercent parenchyma increases the total parenchy-mal volume from 83 to 138 ml kg−1. Assumingthat the surface area available for gas exchangeremains a constant fraction of the total parenchy-mal volume, then the respiratory surface area(RSA) will nearly double, increasing from 5.43×103 to 9.01×103 cm2 kg−1. The anatomical diffu-sion factor (ADF) represents the mass specificvalue for the ratio of RSA to tht (Perry, 1983). Inmulticameral lungs, tht ranges from 0.46 to 1.0 m(Perry, 1983) and if we use the lower value of 0.46m, then ADF increases almost 3-fold to 19.6×103

cm2 m−1 kg−1. Morphometric diffusion capacityof the lung (DtO2

) is the product of ADF andKrogh’s diffusion constant for tissue (3.1×10−8

cm2 min−1 torr−1; Perry, 1983) and, in this case,is equal to 6.5 ml min−1 mmHg−1 kg−1. TheDtO2

is always considerably higher than physio-logical estimates of resting DLO2

, with the ratioDtO2

/DLO2ranging from 6 to 25 depending on the

species (Perry, 1983). In varanids, this ratio is 12(Perry, 1983) and consequently we estimate aDLO2

of 0.53 ml min−1 mmHg−1 kg−1 at rest.Measurements of DLO2

during exercise have notbeen made in reptiles, however in mammals andbirds, exercise increases DLO2

2–4-fold (Piiper andScheid, 1980). If we assume that DLO2

doubles inreptiles during heavy exercise, then the modifiedmulticameral lung would have a DLO2

of 1.06 mlmin−1 mmHg−1 kg−1.


Using this modified DLO2and combining it with

an increase in oxygen carrying capacity and anincrease in maximum cardiac output our hypo-thetical reptilian oxygen delivery system supportsa V: O2max of nearly 70 ml kg−1 min−1 (Table 1;Fig. 2). Our analysis indicates that modifyingseveral steps in the oxygen transport system,within a range of values measured in extant rep-tiles, results in an increase in the transport capac-ity to levels approaching a typical 1 kg activeendotherm (Fig. 2).

Our analysis included three major modifica-tions. First, we increased the oxygen carryingcapacity of the blood from 10 to 20 vol.%. Wecan see no reason why reptiles would be con-strained from synthesizing more red blood cells toproduce a hematocrit equivalent to that of extantendotherms. In fact, in examining hematocritsand hemoglobin content in 39 species of extantlizards, Garland (1993) reports the highest valuesfor hemoglobin of 12.5 g/100 ml blood and hema-tocrits of 35%. Second, we increased the cardiacoutput from 350 to 440 ml kg−1 min−1. Becausecardiac output is the product of stroke volumeand heart rate small changes in either or both ofthese parameters could achieve our predictedvalue. For example in a 1 kg varanid lizard, thenew maximum cardiac output could be achievedby a 10% increase in maximum heart rate (HRincreases from 100 to 110 beats min−1) and a14% increase in stroke volume (stroke volumeincreases from 3.5 to 4.0 ml kg−1). Third, weincreased the parenchymal volume in the lung by50% and reduced the mean harmonic thickness16%. This values for surface area and mean har-monic thickness have been measured in multicam-eral lungs from several extant reptiles (Perry,1983) so these changes also seem reasonable.Taken together, these modifications support a235% increase in V: O2max.

6. Conclusion

Mesozoic ancestors of birds and earlytheropods may or may not have approached theintense levels of aerobically sustainable activityseen in extant birds and mammals. However, our

examination of the comparative physiological lit-erature and our theoretical analysis do not sup-port the hypothesis that non-avian multicamerallungs constrain endothermy. Nonetheless, thequestion still remains, if the multicameral lungcould be reasonably modified into an highly effec-tive gas exchange organ, why has this option notbeen realized and what factors drove the evolu-tion of the avian parabronchial lung and themammalian alveolar lung? Theoretically, theavian parabronchial lung is a more effective gasexchange organ than the alveolar lungs of mam-mals (Piiper and Scheid, 1975). This is evidencedby calculations that show in the parabronchiallung the arterial PO2

obtains values that are sig-nificantly higher than expired PO2

(Piiper andScheid, 1975), a result that is not possible in thealveolar lung. However, the actual differences ingas exchange efficacy in real organs under physio-logical conditions are relatively small and proba-bly not a significant determinant in theevolutionary development of the particular gasexchange organs (Scheid, 1982). Instead, otherfactors, such as the mechanics of ventilation mayhave played an important role in the evolution ofthe distinct avian and mammalian lungs.

7. Speculations on the evolution of avian andmammalian lungs

In our analysis, conservative modifications atseveral steps in the oxygen transport system resultin supporting a large increase in O2 flux from airto mitochondria. However, this higher V: O2

re-quires a significantly large increase in lung ventila-tion. Consequently, in our analysis a V: O2max of 67ml kg−1 min−1 requires a lung ventilation of 2.3L kg−1 min−1. This value is 237% greater thanmaximal levels of ventilation measured in Varanusexanthematicus (Table 1). This lung ventilationrate may represent an unreasonably high maxi-mum rate of ventilation for a 1 kg lizard. Extantlizards have a mechanical constraint on simulta-neous running and breathing that arises from thedesign of the axial musculoskeletal system (Car-rier, 1987b). Consequently, even if Mesozoic rep-tiles modified the lungs and cardiovascular system


Fig. 3. A hypothetical cladogram illustrating the relationship of posture, gait, ventilatory mechanics with different lung morpholo-gies in terrestrial vertebrates.

to support higher tissue gas exchange rates, theystill would have been constrained by the inabil-ity to ventilate the lung adequately. Much of theaxial musculoskeletal system of early tetrapods(e.g. Ichthyostega and Eryops) can be deducedfrom studies of their fossils and it seems proba-ble that they too were constrained from simulta-neous running and exclusively costal breathing(Carrier, 1987a). This constraint has been cir-cumvented in the lineages that gave rise to birdsand mammals by the evolution of novel ventila-tory and locomotor mechanics (Carrier, 1987a;Bramble and Jenkins, 1989), and to varying de-grees in some extant lizards (e.g. the use of thegular pump to assist costal ventilation; Ow-erkowicz et al., 1999). The evolution of bothdinosaurs and mammals involved a change inlimb posture from the sprawling configurationof early tetrapods to a more parasagittal ar-rangement in which the limbs were positionedunder the body. One lineage, the archosaurs,were unique among early reptiles in that manyof them tended toward a bipedal (Romer, 1966)in which the entire weight of the body was sup-

ported by the hips. Furthermore, avian ar-chosaurs evolved powered flight. In contrast,mammal-like reptiles (Thrinaxodon, Cynognathus,Lycaenops) retained a quadrupedal stance andevolved a bounding gait in which the trunkflexes and extends in the sagittal plane. It hasbeen proposed that these postural and gaittransformations facilitated increased rates ofventilation in the archosaur and synapsis lin-eages (Carrier, 1987a).

We speculate that the distinct morphology ofthe avian and mammalian lungs reflects not onlyan increased demand for gas exchange, but ishistorically correlated with these divergentmodes of locomotion that facilitated higher ratesof ventilation (Fig. 3). In addition, novel venti-latory mechanics arose in these groups. Mam-mals and crocodilians both evolved adiaphragm. Whether or not dinosaurs also hada diaphragm is unknown, but some may haveused the abdominal cuirassal basket to supple-ment costal ventilation (Perry, 1983; Claessons,1996, 1997). These mechanical factors couldhave provided a selective pressure during the


avian and mammalian radiation that contributedto their divergent lung morphology. Selectionfor higher metabolic rates mandated additionalrespiratory surface area and greater rates oflung ventilation. However, the additional surfacearea was not randomly scattered about the lungbut was organized into the parabronchial andalveolar geometry perhaps because these struc-tures functioned in harmony with the locomotormode. Gas flow patterns within the mammalianlung have been shown to be affected by locomo-tion, and it has been suggested that the uniquelobar structures of these lungs is due to tissuestresses as well as gas distribution requirements(Bramble and Jenkins, 1989). Furthermore, me-chanical factors such as peak ventilatory flowsand tracheal resistance influence lung morphol-ogy (Leith, 1983). Pulmonary parenchymal cellsand connective tissues change their geometrywhen distorted by altered inflation in extantmammals (Rannels, 1989). If the genetic mecha-nisms that are responding to mechanical stressesin the lungs of extant mammals are primitivefeatures of amniotes, it is possible that the me-chanical stresses associated with bipedal locomo-tion in archosaurs, or with flight in avianarchosaurs, gave rise to a different array of lungmorphologies than were present in quadrupedalmammals. Natural selection would have then fa-vored the morphologies that functioned for eachlocomotor mode to support increase oxygenflux.

Acknowledgements

We wish to acknowledge Drs Al Bennett,Beth Brainerd, David Carrier, George Lauder,Kevin Padian, Frank Powell, Shyril O’Steen andTomasz Owerkowicz for critically reading oneor more versions of this manuscript and provid-ing thoughtful comments and criticisms. The au-thors are particularly grateful to Dr TobiasWang for converting the oxygen transportmodel into a useable Microsoft Excel spread-sheet. JWH is partially supported by NSF grantIBN-9630807 and CF is supported by NIHgrant 1F32 HL09796-01.

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