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Respiratory Physiology & Neurobiology 154 (2006) 89–106

On the origin of avian air sacs�

C.G. Farmer ∗

Department of Biology, University of Utah, 257 South 1400 East, Salt Lake City, UT 84112, USA

Accepted 20 April 2006

bstract

For many vertebrates the lung is the largest and lightest organ in the body cavity and for these reasons can greatly affect anrganism’s shape, density, and its distribution of mass; characters that are important to locomotion. In this paper non-respiratoryunctions of the lung are considered along with data on the respiratory capacities and gas exchange abilities of birds androcodilians to infer the evolutionary history of the respiratory systems of dinosaurs, including birds. From a quadrupedalncestry theropod dinosaurs evolved a bipedal posture. Bipedalism is an impressive balancing act, especially for tall animalsith massive heads. During this transition selection for good balance and agility may have helped shape pulmonary morphology.espiratory adaptations arising for bipedalism are suggested to include a reduction in costal ventilation and the use of cuirassalentilation with a caudad expansion of the lung into the dorsal abdominal cavity. The evolution of volant animals from bipedsequired yet again a major reorganization in body form. With this transition avian air sacs may have been favored because they
nhanced balance and agility in flight. Finally, I propose that these hypotheses can be tested by examining the importance ofhe air sacs to balance and agility in extant animals and that these data will enhance our understanding of the evolution of theespiratory system in archosaurs.
2006 Published by Elsevier B.V.

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eywords: Avian air sacs; Evolution; Dinosaur; Crocodile; Reptile; Bi

. Introduction

The abilities of birds to sustain flight and to fly in thehin air of high altitude are striking evolutionary accom-lishments. The respiratory system is vital to thesetrenuous feats and thus most research on the form,

� This paper is part of a special issue entitled “Frontiers in Compar-tive Physiology. II. Respiratory Rhythm, Pattern and Responses tonvironmental Change”, Guest Edited by William K. Milsom, Frank. Powell, Gordon S. Mitchell.∗ Tel.: +1 801 581 4236; fax: +1 801 581 4668.

E-mail address: [email protected].

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569-9048/$ – see front matter © 2006 Published by Elsevier B.V.oi:10.1016/j.resp.2006.04.014

s; Pneumaticity; Agility; Cuirassal breathing; Alligator; Ventilation

unction, and adaptive significance of the avian lungas rightly focused on adaptations that enable rapidates of gas exchange (reviewed in Maina (1989)). Thevian respiratory system consists of a compact lungestled dorsally amongst and immediately ventrad tohe thoracic ribs and connected to a number of sacs dis-ributed literally from head to tail throughout the body.

hile volume changes of the sacs cause air to flow
n one direction through the parabronchial part of theungs where gas exchange occurs, the sacs themselveso not exchange gases with the blood (Magnussen etl., 1979).
mailto:[email protected]

dx.doi.org/10.1016/j.resp.2006.04.014

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When and how did the avian respiratory systemvolve? The roots of both the avian and mammalianung lie in an ancient reptilian ancestor from whichhe extant pulmonary architecture is derived. Fromhis ancestral form the lungs evolved in very diver-ent courses into the alveolar morphology in mammalsnd the air sac–lung system in birds. What factorsnfluenced the course of this evolution? A numberf creative and sometimes provocative articles haveddressed the question of the origin of the avian lungDuncker, 1989; Perry, 1989, 1992; Ruben et al., 1997,999; Jones and Ruben, 2001; Paul, 2001; Perry, 2001;ander and Perry, 2004; O’Connor and Claessens,005). Traditionally, the key selective factors shapinghe lung have been thought to relate to gas-exchange.owever, the differences in the efficacy of the mam-alian and avian systems are quite small and probably

ot a significant determinant in the evolutionary his-ory of the organs (Scheid, 1982). Furthermore, a modelf the gas exchange potential of the cardiorespiratoryystems of ectothermic reptiles suggests that factorseside gas exchange played critical roles in the evo-utionary history of these lungs (Hicks and Farmer,998, 1999). In this model key elements of the oxygenransport capacity of extant reptiles were consideredn detail, such as the volume of lung devoted to gasxchange (parenchymal volume), the fraction of thisolume involved in gas exchange, the barrier to diffu-ion between the air and capillaries, etc. The resultsndicate that the lungs of extant reptiles contain allhe elements requisite to the rates of gas exchange of

any extant endotherms. To expand this gas exchangeapacity to the high rates typical of volant forms (birdsnd bats) would require only a few modifications, pri-arily an increase in the gas-exchange surface area

nd some thinning of the barrier to diffusion betweenir and blood. Adaptations of the avian and mam-alian lung that facilitate the rapid exchange of gases

etween blood and air and therefore support the aerobicemands of sustained flight have been reviewed else-here (Maina, 1989). The point I want to make here

s that because the alveolar morphology is as capablef gas exchange as the parabronchial lung (see discus-ion of bats in Maina (1989)), selective factors other
han gas-exchange per se may have influenced theseivergent evolutionary courses.
For many vertebrates the inflated lung is the largestnd lightest organ in the body and in consequence

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Neurobiology 154 (2006) 89–106

ffects the shape of the body, the manner in whichass is distributed, the density, and the center of mass;

hese characters are important to locomotion. Recogni-ion of the importance of the lungs to locomotion datesack to the time of Darwin who suggested the originaldaptive significance of this structure was its role asflotation device and that only later in the course of

ertebrate evolution did the lung (gas bladder) evolveunctions as an accessory to auditory organs and as a gasxchanger (Darwin, 1859). A better understanding ofhe phylogeny of fishes indicates that lungs originatedn osteichthyan fishes some 450 million years or morego, and that they originally served in gas-exchangereviewed in Farmer (1999)). However, the importancef the lung to balance, density, and locomotion in fishess undisputed (Webb, 2002). To understand the evolu-ionary history and adaptive significance of this organ,ts function in both locomotion and in gas-exchangeeeds to be considered. The relative importance ofhese functions will of course depend on a variety ofcological, morphological, behavioral, and historicalactors that will differ between lineages. For example,mongst Euteleost fishes the importance of the lung togility and buoyancy predominated over its role in gas-xchange, which has been lost in most groups of theseshes. In the plethodontid salamanders the lungs haveeen entirely lost and thus serve neither locomotionor gas-exchange. Numerous features of the respira-ory system of manatees (Sirenia) serve locomotionRommel and Reynolds, 2000) and below are discussedn detail. In summary, for many vertebrates the lungserve gas-exchange and locomotion and consideringoth functions provides a more integrated view of theistory of this organ than focusing on gas-exchangelone. This broader perspective may provide a founda-ion to explain many of the divergences seen amongstertebrate lineages in pulmonary morphologies andentilatory mechanics.

Avian ancestry nests within bipedal theropodinosaurs (Huxley, 1870; Gauthier, 1986). Bipedalisms an impressive balancing act; the taller and more top-eavy the animal the more difficult it is to balance.volving bipedalism from a quadrupedal ancestry man-ates many changes in the body plan and even greater
hanges are required to adapt a terrestrial animal toight. In these new forms the mechanics of ventilationnd the size, shape, and position of the lung would haveeen significant determinants in the center of mass,

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ody-shape, and the distribution of mass. I hypothesizehat many features of the avian respiratory system areresult of selection that facilitated the balancing acts

equired by bipedalism and flight rather than resultingolely from selection for gas-exchange requirements.or example, I suggest that a dorsal location of the

ung served to stabilize terrestrial theropod dinosaursy moving the center of mass ventrad while an expan-ion of the lung into the abdominal cavity facilitatedurning. Similarly, volant animals are more stable whenhe center of mass is ventrad to the center of lift. Iypothesize that the use of air sacs for ventilation wasavored in Aves because this mechanism facilitated sta-ility and agility in flight. Fore and aft movementsf the center of mass impact angle of attack stability;ateral shifts affect roll. Ventilation of cranially and cau-ally located air sacs with a dorsoventral rocking of theternum minimizes fore and aft shifts in the center ofass. In distinction to most vertebrates in which costal

entilation shifts the heavy viscera fore and aft, in birdshe costal contribution to ventilation can empty and fillhe laterally positioned air sacs leaving the center of

ass undisturbed. Thus the respiratory system of birdsay have undergone selection in ways that facilitated

etter control of the center of mass.

. How did dinosaurs breathe?

.1. Combining functional and historical data:essons from pneumaticity

Integrating mechanistic with historical data canreatly strengthen inferences regarding the evolution-ry history of characters and their adaptive significanceAutumn et al., 2002). It is especially important tonclude a mechanistic dimension to the study of the evo-ution of correlated characters to distinguish betweenpurious and causative correlations. The use of corre-ations is very common and important in paleontologyhere the lack of extant animals precludes the direct

tudy of many characters (e.g., ventilation, metabolism,hermoregulation). This point is well illustrated by thetudy of pneumaticity of the bones of extinct organ-
sms. Pneumaticity is the presence of air-filled cavitiesithin bone. In the head these cavities (sinuses) are
ormed as epithelial outgrowths (diverticula) of otherir-filled cavities, e.g., arising from the nasal or tym-

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Neurobiology 154 (2006) 89–106 91

anic cavity (reviewed in Witmer (1997)). In birds theost-cranial skeleton is pneumatized by diverticula ofhe air sacs, which are themselves diverticula of theung (Duncker, 1971). The idea that post-cranial pneu-

aticity was also present in extinct archosaurs, such asterosaurs and dinosaurs, dates back to the early 1800s.neumaticity was suggested to be an adaptation foright (pterosaurs) and evidence that the bones receivedarts of the lungs in the living animal (Von Meyer,837; Owen, 1856; reviewed in Britt (1997)). It has alsoeen suggested that because post-cranial pneumatic-ty in extant birds is correlated with the air sac–lungystem and endothermy, that pneumaticity in extinctinosaurs is therefore evidence of an avian style lungSeeley, 1870; reviewed in Britt (1997) and O’Connornd Claessens (2005)) and also the elevated metabolicates of endothermy (O’Connor and Claessens, 2005).owever, without integrating functional data into the

tudy, the most that can be inferred from post-cranialneumaticity in extinct animals is that, as pointed outy Owen (1856), the pneumatized bones received partsf the lung in the living animal. In contrast, inclusionf functional data enables much stronger inferences toe made about the adaptive significance and the his-ory of pneumaticity than hypotheses that are based onorrelates.

What is the function of pneumaticity? One of theost robust lines of evidence of the adaptive signifi-

ance of a trait is the convergent evolution of the char-cter in distantly related lineages. Thus the pneumatic-ty of the vertebral column of the osteoglossomorphsh Pantodon (Fig. 1) by the respiratory gas bladderNysten, 1962; Poll and Nysten, 1962; Liem, 1989)s compelling support for the hypothesis that pneu-

aticity functions to reduce mass and density (Nysten,962). Pantadon are surface dwellers capable of leap-ng out of the water and gliding through the air. Theeduction of bone density increases the buoyancy ofhe animal while in the water and the reduction in

ass probably serves to facilitate this aerial locomotionLiem, 1989). The gas-bladders of the flying fish of theamily Exocoetidae are reported to have diverticula farack into the haemopophyses of the caudal vertebrae,lthough it is unclear from this description whether the
iverticula penetrate the bones as they do in PantadonFowler, 1936). Land tortoises also have dorsal divertic-la of the lung that impinge on the sides of the centralnd rib heads and are associated with lightening the

92 C.G. Farmer / Respiratory Physiology & Neurobiology 154 (2006) 89–106

Fig. 1. Pneumaticity in Pantadon, an osteoglossomorph fish. (A) Illustration of multiple dorsal diverticula of the gas-bladder into the vertebralc as bladp bral co( the degt

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olumn; s = stomach, rg = respiratory gas bladder; gt = diverticula of germission of the author and publisher). (B) Photograph of the verteNysten, 1962). (C) Photograph of individual vertebrae illustratingransverse processes (Nysten, 1962).

arapace (D.M. Bramble, unpublished observation).he originating spinal nerves are surrounded by theseneumatic diverticula, and Duncker (1989) has sug-ested that the diverticula increase the flexibility ofhe carapace (Duncker, 1989). Empirical studies areeeded to investigate this interesting suggestion. Whilehe flying ectothermic fish Pantodon has acquired pneu-

aticity of the bones, penguins and many other divingirds have lost or greatly reduced this character, appar-ntly as a mechanism to decrease buoyancy (reviewedn Duncker (2004) and Meister (2005)), but these birdsave maintained both the avian lung and their endother-ic physiology. Because pneumaticity has no known

unctional role in ventilation or thermoregulation oretabolic rates, its usefulness as a hard-part correlate

or lung structure and metabolism is, unfortunately,uestionable. On the other hand, avian pneumaticitys positively correlated with soaring flight and size butegatively correlated with diving (O’Connor, 2004),onsistent with the hypothesis that pneumaticity serveshe function of reduction in mass and density. Historicalata further corroborate this function in the conver-ent evolution four times of post-cranial pneumatic-ty (pleurocoelous presacral vertebrae) in (1) an early
uchian (Effigia okeeffeae), (2) pterosaurs, (3) sauropodinosaurs, and (4) theropod dinosaurs (Gauthier, 1986;esbitt and Norell, 2006). The adaptive advantage ofaving strong light bones for flying animals, such as
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der that penetrate the vertebrae (from Liem (1989); reproduced withlumn illustrating the extent of pneumaticity throughout the columnree to which the bone has been hollowed including the centra and

terosaurs, and for the massive skeletons of sauropodss immediately apparent, but the adaptive advantage ofightening the skeleton is less obvious for the theropodinosaurs (reviewed in Britt (1997)) and for Effigia, yethis is the function for pneumaticity supported by theata. Hypotheses for the importance of pneumaticity tohese latter lineages that are consistent with these datarom fish and birds are more plausible than those basedn correlations with gas-exchange, because pneumatic-ty has no known function in gas-exchange in extantineages.

.2. Cervical pneumaticity reduces rotationalnertia, decreases torque, and improves agility

The idea that pneumaticity served the functionf reducing mass of theropods is strengthened byhe co-evolution of numerous other characters inhis lineage with the same apparent adaptive signifi-ance. For example the forearms of many theropodse.g., Allosaurus, Albertosaurus, Tyrannosaurus) werereatly reduced in mass and size (Molnar et al., 1990;akker et al., 1992), the hands were lightened by reduc-

ion of the number of digits, and the head was lightened
n several lineages by the loss of teeth, e.g., ornithomi-
osaurs, oviraptorosaurs, and several lineages of AvesGauthier, 1986; Carrier et al., 2001). The adaptivedvantage of these changes has been hypothesized to

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e improved agility (Carrier et al., 2001). To turn annimal must overcome rotational inertia, which is aunction of mass multiplied by the square of the dis-ance between the mass and the axis of rotation. Thusotational inertia of a body depends upon the axis abouthich it is rotating, on the shape of the body as well as

he manner in which the mass is distributed (Hallidaynd Resnick, 1978). The fact that rotational inertia isfunction of the distance squared means that smallasses if located far from the axis of rotation will make

ery large contributions to rotational inertia. Non-avianheropod dinosaurs were terrestrial bipeds; their axis ofotation was therefore the pelvic girdle and the mass ofhe head and the distal tail would make much greaterontributions to their rotational inertia than an equiv-lent mass located close to the pelvic girdle. Thus, toeduce rotational inertia the mass furthest from the axisf rotation would have experienced the most intenseelection to be either lost or redistributed closer to theelvic girdle. This prediction is supported nicely byhe fossil record. For example, pneumaticity in thero-od dinosaurs is most extensively found in the bonesf the head, neck, and anterior thorax (Carrier et al.,001). The evolution of the strong light bones of theeck produced by pneumaticity and reduction in masshrough the loss of teeth have also been proposed toecrease torque of the long necks of theropods (Buller,992).

Theropod dinosaurs were not alone in evolving thisuite of characters. Although the archosaurian grouphat gave rise to extant crocodilians (suchians) is gen-rally considered to have had a more conservative bodylan than the dinosaurs (Nesbitt and Norell, 2006),recently prepared specimen of a suchian archosaur,ffigia okeefeae, is exceptional in showing a large num-er of specialized features that are convergent withheropod dinosaurs, particularly the ornithomimidsNesbitt and Norell, 2006). This suchian may be thexception that proves the rule. It was a biped (reducedrm/leg length ratio) with an elongated pubis and anxpanded pubic boot (discussed below), its forearmsere greatly reduced in mass and size, the hands were

ightened by reduction of the number of digits, and theead was lightened by the loss of teeth. Importantly,
t had pleurocoelous cervical vertebrae (pneumaticity).hese iterative patterns of morphological evolution inistantly related archosaurs suggest selective forcesirected this evolution (Nesbitt and Norell, 2006). This
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Neurobiology 154 (2006) 89–106 93

uite of character changes makes sense from the per-pective of selection for increased agility in a bipedalnimal.

.3. Sacral pneumaticity lowers the center of massnd improves balance

In some dinosaurs pneumaticy extends beyondhe cervical and thoracic vertebra into the sacralegion (abelisauroid, spinosauroid, allosauroid,rnithomimid, tyrannosauroid and maniraptoranlades; O’Connor and Claessens, 2005 and referencesherein). Pneumaticity of sacral bones indicates thathere was selection for lightening the sacral skeleton inhis region. This would have been of little importanceo rotational inertia about the vertical axis of the pelvicirdle, but it would have served to move the center ofass ventrad, as did the evolution of a large heavy

oot on the distal end of the long pubes. Just as theeel of a ship lowers its center of mass and improvests stability, a lower (ventrad) center of mass caused byhese changes was undoubtedly a more stable situationor a biped.

.4. From pectoral to pelvic girdles: the decline ofostal and rise of cuirassal breathing

Was the respiratory system affected by the manyhanges of the trunk entailed in the evolution of an agileiped? The answer to this question is almost certainlyes, if changes in shape entailed decreases in thoracicolumes and if lung volumes and capacities scaled sim-larly amongst the Archosauria. Data on pulmonaryolumes and capacities of extant crocodilians and birdsTable 1 and Fig. 2) suggest these traits have been wellonserved amongst the Archosauria. These data indi-ate that compared to mammals both crocodilians andirds have very large lungs (+air sacs) for their bodyass (about 150 ml kg−1); mammals have lungs aboutthird or quarter of this volume. Pulmonary capaci-

ies of birds and alligators are also similar. The avianelationship between tidal volume (ml) and body masskg) is VT = 20.3M1.06 (Frappell et al., 2001). Tidalolumes of American alligators fit this avian scaling
elationship remarkably well: VT = 20.7M1.06 (Fig. 2).he similarity in lung volumes and tidal volumes is
ntriguing in and of itself because the underlying physi-logical reasons for these relationships are not yet clear.


Table 1Respiratory capacities of extant archosaurs and an outgroup (mammals)

Specific volume(ml kg−1)

Functional residualcapacity (ml kg−1)

Vital capacity(ml kg−1)

Source

Birds (air sac + lung) 100–200 Reviewed in Scheid and Piiper (1989)Pigeon (air sac + lung) 140a 19 139 Perry (1983)Crocodile 140a 20 136 Perry (1983)

Mammals (0.020–100 kg)34–37 Based on 20 terrestrial species with similar weight

range to birds (Maina, 1989)42–71 14–44 48–68 Based on humans, cats, rats, dogs (Stahl, 1967)

Bats (0.02–0.2 kg) 45–53 Maina (1989)

Birds and crocodiles have very similar functional residual capacities and vital capacities.by the f

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hus a very fruitful area of experimental research mayie in studies designed to illuminate the mechanisticasis of these relationships. Furthermore, additional
ata are wanted relating lung volume to body mass andtudies of pulmonary capacities in a broader range ofuchian species (e.g. caiman, more crocodiles, gavials)o shore up these trends. Nevertheless, even if not fully
ig. 2. Scaling of tidal volume (VT) with body mass (M) for extantrchosaurs and mammals. The solid grey line is the avian scal-ng relationship between tidal volume (ml) and body mass (kg),

T = 20.3M1.06, which is based on data from 50 species of birdsFrappell et al., 2001). The black dots indicate mean tidal volumeseasured for American alligators from three different studies. The

caling equation of the alligators is given by VT = 20.7M1.06. Theata for the largest mass (N = 4) are from Hicks and White (1992).he data for the intermediate mass (N = 5) are from Farmer andarrier (2000b). The data for smallest mass (N = 10) are computed

rom unpublished observations of vital capacities, T.J. Uriona and.G. Farmer. The solid black line is the mammalian relationship

T = 7.7M1.04 (Stahl, 1967).

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ollowing: lung volume = vital capacity + functional residual capac-ps (Frappell et al., 2001; Fig. 3). The lungs of crocodiles and thels. Respiratory capacities of extant archosaurs are also remarkably

nderstood, these data on lung volumes and pulmonaryapacities suggest that amongst the archosaurs phylo-enetically bracketed by crocodilians and birds, lungolumes and pulmonary capacities scaled comparably.ertainly there is no basis to assume extinct archosaursad diminutive respiratory systems compared to thextant taxa.

Was there enough space for the respiratory sys-em within the thorax to house these large lungs andould costal ventilation alone power similar pulmonaryapacities in extinct archosaurs? Perhaps not in theipedal forms. The Ornithodira (Fig. 3) evolved shorterrunks than those in outgroup taxa (reviewed in Padian1997)). Short trunks reduce the distance between theelvic and pectoral girdles and thus reduce rotationalnertia of the trunk (Carrier et al., 2001). However, ifhe reduction in the length of the trunk was not fullyompensated by increased height and breadth, then thisrend reduced thoracic volume. To preserve lung vol-me, the lungs would have had to expand beyond theounds of the thorax into the abdominal cavity. Smallerhoraxes also would have reduced the costal contribu-ion to tidal volumes and the retention of pulmonaryapacities would have mandated compensation throughhe active expansion and contraction of the abdominalolume. This hypothesis makes two predictions thatan be tested with the fossil record. First, fossil indica-ors of a reduced thoracic volume (a relatively smalleribcage) will be mirrored by indicators of an increased
bdominal volume, such as elongation of the pubes andlaboration of the cuirassal basket. Second, pneumatic-ty of the sacral region of the body will be found mostften in lineages with a small thorax and large abdomen

C.G. Farmer / Respiratory Physiology & Neurobiology 154 (2006) 89–106 95

Fig. 3. Relationship of the Ornithodira and outgroup taxa (top panel). The bottom panel illustrates typical body-shape differences betweentheropods such as Gorgosaurus and Struthiomimus and non-ornithodiran archosaurs such as Alligator and Euparkaria. The illustrations weretaken from scaled reconstructions. The photograph (Struthiomimus) is from a panel mount of a specimen placed approximately as found. Thesespecimens illustrate several of the changes in morphology that accompanied bipedalism in theropods compared to their quadrupedal ancestorsthat are discussed in the text. Pubic bones are marked with arrows. Compared to the basal archosaurian pattern the theropod pubes are elongatedrelative to the trunk lengths. The shoulder girdle is reduced in the theropods with small forelimbs and loss of digits (Gorgosaurus) and/or throughthe thinning the glenoid and other bones (Struthiomimus). Euparkaria was found with gastralia but they were not included in the reconstruction(Ewer, 1965, reproduced with permission of the publisher). Gorgosaurus (Lambe, 1917); Struthiomimus (Osborn, 1916); Alligator (Reese, 1915).

96 C.G. Farmer / Respiratory Physiology &

Fig. 4. Photograph of holotype Ornithomimus edmontonicus(CMNFV 8632) reproduced courtesy of the Canadian Museum ofNature, Ottawa, Canada. The specimen was not greatly distorted byoverburden and the entire set of gastralia is preserved (Sternberg,1933). These bones meet at the midline in a simple V much as thegastralia of American alligators do. The elements close to the pelvicgirdle are more robust than those near the pectoral girdle, suggest-ing these elements may have experienced more mechanical stress inthe living animal than the more craniad elements. The distal ribs arevvt

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ery slender and appear not much more robust than the gastralia. Theolume of the thorax appears small compared to the abdomen, as ishe case for other specimens of ornithomimids.

large pubis to trunk length ratio) because caudallyocated respiratory structures are more likely to haveeen present. The reader is also referred to Paul (2001,002) for an interesting perspective of how changes inrunk design may have affected the positions of air sacsnd lungs in archosaurs.

Quantification of changes in thoracic and abdom-nal volumes in fossils is problematic on a numberf accounts. The accuracy of measurements of trunkimensions can be hampered by distortion of the fos-ils from overburden, disarticulation of the skeletallements, incomplete skeletons, omission of informa-ion in descriptions of the fossil, and the worldwideeographic distribution of specimens that make directeasurements of a large number by a single group of

esearchers using a consistent methodology quite dif-cult. Nevertheless, the case is not hopeless and therere a number of well articulated specimens that do notppear to have been greatly distorted during fossiliza-
ion and that are either complete or near enough toharacterize these changes in body shape. Such a spec-men is illustrated in Fig. 4, a photograph of an articu-ated skeleton of the theropod dinosaur Ornithomimus
west


dmontonicus. The specimen consists of the distal por-ions of most of the left thoracic ribs and portions fromhe right as well, a complete set of gastralia, most ofhe pubes, a complete right forelimb, etc. The dorsalibs, gastralia, and pubes are preserved very close toheir natural positions (Sternberg, 1933). Several char-cters of this specimen are consistent with the hypoth-sis of a decrease in reliance on costal ventilation andn increase in reliance on cuirassal ventilation in thisineage. The thoracic ribs are very slender relative tohe cuirassal basket, which becomes increasing robustlose to the pubes where more mechanical stress wouldave occurred with cuirassal breathing. Furthermore,he curvature of the ribs and cuirassal basket suggesthis animal had a very small thoracic volume relativeo its abdominal volume. Other ornithomimids have aimilar shape.

To assess the relationship between thoracic andbdominal volumes, I quantified the length of the tho-acic vertebral column and the length of the pubis on

number of fossils and one recent taxon (Table 2).measured these lengths directly on an articulated

keleton of a juvenile American alligator. The restf the data, however, were culled from the literaturend although the measurements will inherently have aot of variation that reflects measurement inaccuraciesather than real variations in the animals’ proportionse.g., noise), if the signal is large enough, real trendsay still be recognized. The length of the thorax was

stimated in two ways: If the lengths of the dorsalertebrae were reported in the literature, then theseengths were simply summed. If this information wasot available, then for articulated and nearly completekeletons, measurements were made on photographsf the specimen. Measurements were also made onllustrations if they had been drawn to scale. Thesentailed measurement of the length (usually a straightine) through the center of vertebral column from theranial edge of the first dorsal vertebra to the caudaldge of the last dorsal vertebra. Measurements of thehotographs and illustrations were made using calipershat are accurate to 0.01 mm. Pubic length was eitheraken from the reported values or measured from theseame photographs or illustrations. The measurement
as the distance from the distal pubis to the cranial
dge of the symphysis of the pubis and illium. If theymphysis was not discernable from the photographhen the pubic length was determined to the center of


Table 2The ratio of the length of the pubis to the length of the trunk

Non-ornithodirans Pubis trunk−1 Source Non-ornithodirans Pubis trunk−1 Source

Alligator mississippiensis 0.3 Personal observation Megalancosaurus 0.1 Paul (2002)Euparkaria 0.2 Ewer (1965) Euparkaria 0.2 Paul (2002)Terrestrisuchus 0.3 Crush (1984) Terrestrisuchus 0.2 Paul (2002)

Postosuchus 0.4 Paul (2002)Riojasuchus 0.3 Paul (2002)

Mean ± S.E. 0.27 ± 0.03 0.24 ± 0.05

Ornithodiransa Pubis trunk−1 Source Ornithodirans Pubis trunk−1 Source

Eoraptor 0.4 Paul (2002)Herrerasaurus 0.5 Paul (2002)Syntarsus 0.4 Paul (2002)

Carnotaurus sastrei 0.7 Bonaparte et al. (1990) Allosaurus 0.6 Paul (2002)Gorgosaurus libris 0.6 Lambe (1917) Gorgosaurus 0.5 Paul (2002)

CompsognathidsHuaxiagnathus orientalis 0.6 Hwang et al. (2004) Compsognathus 0.4 Paul (2002)Sinosauropterus prima 0.6 Chen et al. (1998) Paul (2002)Ornitholestes 0.5 Osborn (1916) Ornitholestes 0.5 Paul (2002)Scipionix samniticus (juvenile specimen) 0.4 Del Sasso and

Signore (1998)Scipionix 0.4 Paul (2002)

Struthiomimus altus (no. 5339) 0.9 Osborn (1916) Gallimimus 0.6 Paul (2002)Alxasaurus 0.4 Paul (2002)

Archaeopteryx lithographica 0.6 Wellnhofer (1992) Archaeopteryx 0.5 Paul (2002)Deinonychus 0.6 Paul (2002)Caudipteryx 0.7 Paul (2002)Oviraptor 0.5 Paul (2002)

Sinornithoides youngi 0.5 Russell and Dong (1993) Troodont 0.5 Paul (2002)Mononykus 0.4 Paul (2002)Avimimus 0.6 Paul (2002)Confuciusornis 0.5 Paul (2002)Cathayornis 0.6 Paul (2002)Messelornis 0.5 Paul (2002)

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ean ± S.E. 0.6 ± 0.05

a This ratio was significantly greater in the ornithodirans (p < 0.05

he acetabulum. The ratio of the lengths of the pubiso the thoracic vertebral column was rounded to theearest tenth. The data were then binned into tworoups: Group A composed of archosaurs excludinghe Ornithodira, and group B composed of members ofhe Dinosauria (Fig. 3). The length of the pubes withespect to the dorsal vertebral column is significantlyreater in the Ornithodira compared to the outgroupaxa (p < 0.05; unpaired t-test; Table 2). Proportionsbtained from these measurements made on articulated
nd well-preserved specimens described in the primaryiterature are close to those obtained by making theame measurements on illustrations of these or closelyelated species found in Paul (2002). If these ratios indi-
tLtr

0.5 ± 0.02

d t-test).

ate changes in trunk shape, then as the trunk shortenednd the thorax became smaller relative to the mass ofhe animal, the respiratory system would have had toxpand caudad or diminished in volume.

If the respiratory system expanded beyond theounds of the ribs into the abdominal cavity, the ribsould have been incapable of ventilating this portion of

he lung (or air sac). Thus to preserve pulmonary capac-ties and ventilate lung tissue outside the bounds ofhe ribs these animal would have needed a mechanism
o actively expand and contract the abdominal cavity.ambe (1917) proposed that the rugosities of the gas-
ralia (Fig. 5) of a theropod dinosaur, Gorgosaurus lib-is, indicate that there was considerable play between


F pods ill( he midlb tation (d

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ig. 5. Ventral view of the cuirassal baskets in several groups of tetraA) An outgroup to archosaurs, Sphenodon, where the elements at tasal archosaur Euparkaria with goosenecks and a herring bone orieninosaur Gorgosaurus libris (Lambe, 1917). S = sternum; P = pubes.

he elements and that this flexibility evolved in con-ection with the animals breathing. Other authors haveubsequently also proposed a role in ventilation forastralia (Perry, 1983; Claessens, 1997; Carrier andarmer, 2000a).

.5. Cuirassal breathing-a putative mechanism

Gastralia are primitive for amniotes and are proba-ly homologous with the ventral body armor of basalaleozoic tetrapods (Romer, 1956; reviewed in Carriernd Farmer (2000a)). In early amniotes gastralia haveenerally been thought to function for mechanical pro-
ection of the ventral body wall. They are present as
series of chevrons composed of a variable num-er of long slender bones and with the apex of thehevron pointing craniad. The central chevrons in ani-

sIta

ustrating the v-shaped elements that may have served in ventilation.ine are fused (illustration from Lambe (1917)). (B) Gastralia of thebased on Ewer (1965)). (C) Complete cuirassal basket of a theropod

als such as Sphenodon are composed of fused laterallements that cross the midline of the belly and havencinate processes (Fig. 5). In other taxa, for exam-le Alligator mississippiensis, the central chevronsre composed of two bones that meet at the mid-ine (Fig. 6) and this is also the case in the thero-od O. edmontonicus (Sternberg, 1933; Fig. 4). Inhe basal archosauromorpha, Euparkaria, the gastraliaave goosenecks that are highly variable in shapend form a herringbone pattern at the ventral mid-ine (Fig. 5). A herringbone pattern is also found in E.keefeae (S.J. Nesbitt, unpublished observation). Werehese gastralia actively recruited for ventilation and, if
o, what sort of mechanics might have been employed?nsight into these questions has come from studies ofhe role of the pelvic girdle in ventilation in extantrchosaurs.


F e Ameri ia allowm muscled caudad.

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ig. 6. Ventral view of the musculature and skeletal elements of thn the midline in a simple V. The symphyses of the pubes and isch

uscles, which are active during exhalation. (C) and (D) show threeuring inspiration and cause the pubes and gastralia to rotate ventro

Ventilation in alligators is accomplished by severalechanisms, one entailing the rotation of the gastralia

entrocaudad. Volume changes of the thorax are pro-uced by intercostal muscles that cause the ribs towing primarily either craniolaterally or caudomedi-lly. This movement should be capable of producingconsiderable proportion of the tidal volume becausef the elongate body cavity of the animals (Hartzlert al., 2004). However, crocodilians supplement costalnspiration by contraction of the diaphragmaticus mus-le (Gans and Clark, 1976) that pulls the liver andungs primarily caudad. Simultaneously, the volumef the abdomen is expanded by the contraction ofhe ischiopubic and ischiotruncus muscles that rotatehe pubes and gastralia ventrocaudad (Fig. 6) (Farmernd Carrier, 2000). Expiration is produced by thentercostal musculature and by the contraction of theransversus abdominis and the rectus abdominis thatush the liver forward and pull the gastralia and pubesorsocraniad (Farmer and Carrier, 2000).

A mechanism for expansion of the cuirassal basketf other archosaurs has been proposed that is based onhis anatomy and physiology in the American alligatorCarrier and Farmer, 2000a,b). If archosaurs ancestrally

aiat

ican alligator. (A) Skeletal elements showing the gastralia meetingmobility. (B) The gastralia are embedded in the rectus abdominis

s, the ischiopubis, ischiotruncus, and truncocaudalis, that are activeFrom Farmer and Carrier (2000a).

ad an ischiotruncus muscle with the activity patternf that seen in alligators and a similar orientation, itould have pulled on the gastralia during inspiration,ausing the apex of the chevrons to rotate ventrocau-ad. This mechanism was proposed to be analogouso expansion of the buccal cavity by the hyoid pullingn the hyobranchials. If such a mechanism existed, theubes would have served as a fulcrum and their lengthould have directly impacted the volume of expansionf the abdominal cavity. Thus the longer the pubes, thereater the potential for abdominal volume changes toontribute to pulmonary capacities. The pubes in basalrchosaurs (e.g., Euparkaria) were slightly elongatedompared to outgroup taxa, but not nearly as long asn the theropod dinosaurs (Fig. 3, Table 2). Hence themportance of this putative mechanism for inspiration

ay have increased in theropods in connection with theody shape changes that accompanied bipedalism.

In alligators the lung occupies the thorax while theiver, stomach and other intestines are positioned in the
bdomen dorsad to the gastralia, which are imbeddedn the rectus abdominis muscles. Because these viscerare incompressible contraction of the rectus along withhe transversus abdominis squeezes the abdominal vis-

100 C.G. Farmer / Respiratory Physiology &

Fig. 7. Lateral view illustrating the mechanisms of ventilation inAmerican alligators. Inspiration is accomplished by the intercostalmuscles that rotate the ribs craniolaterally while the diaphragmati-cus muscle pulls the liver caudad. The ischiopubis, ischiotruncus, andtruncocaudalis pull on the gastralia and pubes to rotate them ventro-caudad and expand the abdominal cavity. Exhalation is accomplishedbtca

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y the rectus abdominis and transversus abdominis (not shown here)hat squeeze the viscera craniad to push air out of the lung. Thus theenter of mass primarily shifts fore and aft with ventilation. Farmernd Carrier (2000a).

era causing them to move primarily craniad into theung during exhalation (Fig. 7). Thus each breath pro-uces primarily a fore and aft shift in center of mass.owever, if the lungs were positioned dorsad to the

uirassal basket in theropods, as has been proposed,hen cuirassal ventilation would have resulted in the

ovement of the viscera, and thus the center of mass,n a dorsoventral plane as well. Below the potentialmpact on locomotion of these movements of center of

ass with breathing is discussed.

.6. The swing of the pendulum: the fall ofuirassal and rise of avian breathing mechanics

Birds are amongst the fasted and most nimble ofertebrates. The evolution of birds entailed a major
eorganization in the body plan; many of these changesre elegant solutions to problems of physics imposedy flight. To evolve aerial dexterity from a terres-rial, bipedal ancestry entailed many changes besides
mfpT


he evolution of wings. For example, mass was lostnd/or redistribution closer to the axis of rotation, theings, by the following mechanisms: (1) reduction of

he number of caudal vertebrae (Carrier et al., 2001),2) in many species the pelvic girdle (synsacrum), cau-al vertebrae and hind-limb bones were pneumatizedMcLelland, 1989), and (3) the heavy gastrointestinalrgans evolved a more craniad location. For examplehe crop, which is an organ used to store food, evolvednd sits craniad to the sternum outside the coelomicavity (Fig. 8). The liver, one of the heaviest organsf the body evolved a craniad location, closer to theectoral girdle. All of this reorganization in body formakes sense from the perspective of agile locomotion

entered about the wings rather than the pelvis.The respiratory system was also involved in these

hanges in trunk design. Although ancestral birds hadcuirassal basket, these bones were reduced and even-

ually lost in the lineage leading to modern birdsreviewed in Carrier and Farmer (2000a,b)). In extantineages, the trunk skeleton is a capsule made of rigidlynterconnecting and even fused bones (Ruppell, 1975).

large, ventrally located keel provides for the attach-ent of powerful flight musculature (Figs. 8 and 9). A

endulum like swing of this keel and its attendant ribsn a dorsoventral orientation produces most of the tidalolume; there is very little lateral displacement of theibs (Zimmer, 1935). Evolutionary biology is preem-nently concerned with questions of why. Why was aocking keel a more favorable mechanism for breathinghan rotation of the ribs in a craniolateral and caudo-

edial manner?

.7. Changing directions to understand thedaptive significance of the avian air sacs

Although the avian respiratory system, like that ofammals, is capable of rapid rates of gas exchange, it

s clear that there are many alternative ways to evolveuch a system (Hicks and Farmer, 1999). Thus factorsesides gas exchange may have directed the evolutionf the avian air sac system. The idea that pulmonaryiverticula serve non-respiratory functions is not new.or example, Duncker (1989) has pointed out that pul-
onary diverticula of snakes and lizards may serve the
unction of enlarging the body for defensive display orlay roles in enabling large prey items to be swallowed.he lung and its diverticula can also serve locomotion.

C.G. Farmer / Respiratory Physiology &

Fig. 8. Anatomy of a chicken. (A) Lateral view showing the positionof the lung nestled dorsally amongst the ribs, which can be seen incross-section (number 1). The lungs are held in this position by adiaphragm. Both the abdominal and cranial air sacs (C) are outlinedin white. The crop (2) is exterior to the body cavity and sits on thefurcula craniad to the sternum (3). (B) Ventral view illustrating thepas

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osition of the viscera such as the liver (9) and stomach, which occupycranial location compared to the basal condition. M.S. muscular

tomach (Sisson and Grossman, 1953).

Terrestrial mammals control their locomotion byushing against the earth but birds accelerate, decel-rate, and many species can turn on a dime withouthe benefits of an immobile ground upon which to baseheir movements. Rather than contact with a solid sub-trate, movement in air involves deflection of airflow,
hich produces lift and drag. Much of the physics
nvolved with moving through air is similar to move-ent through water and therefore it is not surprising tond similar adaptations (e.g., airfoils and hydrofoils)

absN

Neurobiology 154 (2006) 89–106 101

o these physical problems in the design of aquaticnd volant organisms (Vogel, 1981). Both lift and dragased maneuvers depend on speed; the slower the speedhe less force that is generated through these mecha-isms (Alexander, 1990). Thus, stability and maneu-erability is most difficult at slow speeds (Alexander,990); yet control of pitch, roll, and yaw are essentialegardless of the speed the animal is traveling (Dudley,002; Webb, 2002). In aquatic animals the lung andts diverticula affect center of mass, center of buoy-ncy, and the distance between these centers (meta-entric height), and appear to be especially importantor slower swimmers (Alexander, 1990). This locomo-or role of the lungs no doubt underlies much of theariation in lung structure seen amongst aquatic ani-als. The lung and its diverticula may provide a certain

mount of evolutionary flexibility regarding the wayass and air are distributed in the body to facilitate

ocomotion. For example, in Luciocephalus, and allnabantoid fish, caudal expansions of the gas blad-er appear to counteract air that is held in the headuring a breath hold (K.F. Liem, unpublished observa-ion). Many other fishes have caudal, cranial, dorsal orentral diverticula whose functions may well relate toocomotion. Manatees also show specialization of theungs that appear to serve locomotion.

The organization of the body cavity of manateess very distinct from all other mammals but markedlyimilar to birds. In most mammals the body cavitys subdivided at the level of the heart and liver by a

usculotendinous diaphragm in a diagonal transverselane; the thorax (the cranial portion) is bounded byhe ribs and contains the lungs (housed in the pleuralavities) and heart (housed in the pericardial cavity)hile the abdominal cavity is caudad to the diaphragm

nd contains most of the other viscera (housed in theeritoneal cavity). Attachment sites for the diaphragmnclude the sternum, the distal tips of the vertebral ribs,nd a small region of the vertebral column. In con-rast, manatees have two muscular hemidiaphragmshat subdivide the body cavity horizontally nearly itsntire length (Fig. 10). Laterally the diaphragms attacho the ribs, extending craniad from the level of the sixthervical vertebra (affiliated with the first thoracic rib)
nd caudad to the level of the third post-thoracic verte-ra. Medially these diaphragms attach to hypapophy-es (bony ventral extensions of the vertebral centra).early the entire volume of the lungs is contained


F mal) ilfl ses the

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ig. 9. Skeleton of a bird and a representative of an outgroup (mamight musculature. Note the small thorax of the mammal, which hou

ithin the dorsally arched ribs, extending ventrad onlyo the level of the vertebral bodies. The rest of the ribage encases not only the heart, but also much of theiscera of the peritoneal cavity (liver, stomach, etc.),hich is referred to by Rommel and Reynolds (2000) as

he intrathoracic abdominal cavity (Fig. 10). Birds haveonvergently evolved dorsally located lungs that areupported ventrally by a musculotendinous diaphragm,nown as the horizontal septum, that attaches laterallyo the ribs and medially to hypapophyses (Duncker,971). Other than birds and manatees, I know of noxamples of this striking convergent evolution amongstetrapods. In both birds and manatees the diaphragm isomposed primarily of an aponeurosis but has a skirt ofuscle (M. costopulmonalis and M. sternopulmonalis

n birds, pars muscularis in manatees). In birds the mus-ular fibers extend about a third of the width of theeptum in its middle part (Duncker, 1971); in manatees
he fibers extend about a quarter of the transverse extentf the hemidiaphragm (Rommel and Reynolds, 2000).he ostia to the avian air sacs, particularly the poste-
ior thoracic and abdominal air sacs, are surrounded

aa

a

lustrating the large sternum that is important for the attachment ofrelatively small lungs (Table 1). Figures from Ruppell (1975).

y the M. costopulmonales. Furthermore, in birds as inanatees the liver, stomach, and other peritoneal con-

ents are located craniad, in many species within theounds of the ribs and sternum, within an intrathoracicbdominal cavity. The reorganization of the viscera, thepecialized lungs, and the hemidiaphragms of manateesppear to enable the animals to distribute air withinhe lungs to affect aspects of their locomotion suchs roll and pitch (Rommel and Reynolds, 2000). Thextremely dorsal location of the lungs places the centerf mass cranioventrad compared to where it would bef the coelomic cavity were partitioned obliquely like its in other mammals. This organization apparently pro-ides stability. The similarity in the organization of theiscera of birds raises the question of the importancef the dorsal location of the avian lung and its divertic-la to balance and stability. In aquatic vertebrates theuoyancy of the lung and its diverticula affect balance
nd locomotion but how could the respiratory systemffect balance and locomotion of volant birds?
Changes in center of mass can greatly affect flightnd are not only relevant to agility but also to glid-

C.G. Farmer / Respiratory Physiology &

Fig. 10. Photographs of ventral views of a manatee (from Rommeland Reynolds (2000)) illustrating adaptations in the lungs anddiaphragms serving posture and locomotion. The basal mammaliancondition where the diaphragm separates a craniad thorax from a ven-trad abdomen has been lost. The lungs have evolved an extremelydorsal location and extend caudad nearly the full length of thecoelomic cavity. The liver and other viscera have shifted craniad.The diaphragm has evolved into two hemidiaphragms that appear tobe able to modulate independently the volume of air in the right andleft sides of the lung to control roll. (A) Ventral view after removalof the skin, fat and musculature. (B) Photograph after removal ofthe gastrointestinal tract. (C) Photograph after removal of the heart,liver, and kidney. The two central tendons (C) of the hemidiaphragmsa(t

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gammrtsftii(bsdaeatwaws

istctttamnbHbadimoma

ttach medially to the hypapophyses. Large intestine (LI), stomachS), liver (L), heart (He), hemidiaphragms (H), right kidney (K),ransverse septum (T).

ng and soaring. For example, a person hanging inharness at the center of mass of a hang glider

an steer it simply by a slight change in positionf his or her body (center of mass). Movement ofhe center of mass craniad decreases pitch and viceersa while a shift to the right or left causes a turno the right or left. Birds are built a lot like high-ing monoplanes; the body hangs from the wings

ike a pendulum (Ruppell, 1975). Birds have achievedreat stability in flight; changes in speed or direc-
ion of the wind do not deflect gliding and soar-ng birds from their course unless the gust is verytrong. This stability is accomplished through the tiltf the wings, but it is not beyond reason to sug-
eim

Neurobiology 154 (2006) 89–106 103

est the air sacs facilitate it. Breathing in vertebratesffects the center of mass of the body by the displace-ent of bones, muscles, and viscera. As previouslyentioned, in crocodiles and most mammals inspi-

ation moves the viscera caudoventrad, while expira-ion moves the mass of the heavy viscera craniodor-ad. Thus the center of mass moves primarily in aore and aft orientation (Farmer, personal observa-ion). In contrast in birds inspiration and expirationncrease and decrease respectively the volume of airn the anterior and posterior air sacs fairly similarlyScheid and Piiper, 1989) and this occurs primarilyy the dorso-ventral rocking of the sternum and amaller contribution from craniolateral and caudome-ial movements of the ribs (Zimmer, 1935). The lateralnd medial movements of ribs would tend to fill andmpty the lateral air sacs rather than shift the livernd other viscera. Thus most of the changes in cen-er of mass appear to occur in the dorso-ventral planeith the rocking of the sternum rather than fore and

ft or laterally and medially. Breathing in this wayould not affect pitch or roll and would facilitate

tability.Alternately, if some air sacs could be preferentially

nflated more than others the center of mass could behifted by displacement of the viscera and muscles andhus have affects on pitch, role and yaw. For exampleontraction of the M. costopulmonales (also known ashe costoseptal muscles) theoretically could alter resis-ance to flow through the ostia of the air sacs wherehey pierce the diaphragm (horizontal septum) and thuslter flow to and from the air sacs. It is known that theseuscle contract during exhalation, perhaps to prevent

arrowing of the ostia or distortion of the lung duringreathing (King and McLelland, 1975; Fedde, 1987).owever, these muscles appear to be somewhat over-uilt for these purposes alone, it is estimated they gener-te 300 times more force than is required to prevent lungistortion during quiet breathing (Fedde, 1987). Dur-ng flight, asymmetrical contractions of these robust

uscles could alter airflow and therefore the volumesf the sacs and in this way change center of mass. Toy knowledge, these putative locomotor effects of the

vian air sacs have never been investigated.
The hypothesis that the system of air sacs that
volved in archosaurs was in response to selection formproved balance and agility is testable in extant ani-

als. There are approximately 9000 species of birds

1 logy &

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ith diverse lifestyles, modes of locomotion, and bodyorms. Furthermore, great variation exists in the rel-tive sizes, numbers, and orientations of the air sacsithin the thoraco-abdominal cavity (Duncker, 1971;cLelland, 1989). For example, while storks have

1 sacs the domestic turkey has but 7 (King andcLelland, 1975). In some birds the caudal thoracic

ir sac is the largest (e.g., hummingbirds) while inther birds the abdominal air sac is most capaciousKing and McLelland, 1975). The hypothesis that their sacs serve locomotion is corroborated if this vari-tion makes sense with respect to balance and agility.or example, if improved agility in flying birds by theeduction in mass in the caudal body was a determinantn the evolution of abdominal air sacs, then abdomi-al air sacs should be larger in agile flyers than theyre in flightless forms (e.g., ratites; penguins). Agileunners would be expected to have redistributed theeight from the pectoral girdle toward the pelvic gir-le, providing another reason to have a large groupf cranial sacs but relatively small abdominal sacs.nother approach to testing these ideas is to experi-entally manipulate the air sacs directly (occlude or

therwise impair) and study the consequences of theanipulations on balance and movement.

. Summary

Most research on the form, function, adaptive signif-cance, and evolutionary history of the avian respiratoryystem has focused on gas-exchange. However, the dif-erences in the efficacy of the mammalian and avianespiratory systems are quite small and probably not aignificant determinant in the evolutionary history ofhe organs (Scheid, 1982). In this manuscript I haveypothesized that the evolution of bipedal posture ofinosaurs may have initiated selection for a caudalxpansion of the respiratory system from the thoracicnto the dorsal abdominal cavity to facilitate balancend agility. Pneumatization of the sacrum and verte-ral column lowered the center of mass and improvedtability whereas a reduction in costal ventilation andn increase in cuirassal ventilation improved agility.
olent theropods may have experienced selection foriverticula of the lungs (air sacs) that facilitated controlf the pitch, roll, and yaw so important in this form ofocomotion.
D

D


cknowledgements

This paper has benefited from conversations I havead with D.R. Carrier and D. Bramble and the insightfulomments of two anonymous reviewers. I am gratefulo C. Janis for asking hard questions. This work wasupported by NSF-IBN 0137988.

eferences

lexander, R.M., 1990. Size, speed and buoyancy adaptations inaquatic animals. Am. Zool. 30, 189–196.

utumn, K., Ryan, M.J., Wake, D.B., 2002. Integrating historicaland mechanistic biology enhances the study of adaptation. Quart.Rev. Biol. 77, 383–408.

akker, R.T., Siegwarth, J., Kralis, D., Filla, J., 1992. Edmarka rex, anew, gigantic theropod dinosaur from the middle Morrison For-mation. Late Jurassic of the Como Bluff outcrop region. Hunteria2, 1–24.

onaparte, J.F., Novas, F.E., Coria, R.A., 1990. Carnotaurus sastreiBonaparte, the horned, lightly built carnosaur from the middlecretaceous of patagonia. Contrib. Sci. 416, 1–42.

ritt, B.B., 1997. Postcranial pneumaticity. In: Currie, P.J., Padian,K. (Eds.),Postcranial pneumaticity. Encyclopedia of Dinosaurs.Academic Press, San Diego, pp. 591–593.

uller, P., 1992. Light bones in birds. In: Campbell, E.J. (Ed.),Lightbones in birds. Papers in Avian Paleontology Honoring PierceBrodkorb. Natural History Museum of Los Angeles, Los Ange-les, pp. 385–393.

arrier, D.R., Farmer, C.G., 2000a. The evolution of pelvic aspirationin archosaurs. Paleobiology 26, 271–293.

arrier, D.R., Farmer, C.G., 2000b. The integration of venti-lation and locomotion in archosaurs. Am. Zool. 40, 87–100.

arrier, D.R., Walter, R.M., Lee, D.V., 2001. Influence of rota-tional inertia on turning performance of theropod dinosaurs: cluesfrom humans with increased rotational inertia. J. Exp. Biol. 204,3917–3926.

hen, P., Dong, Z., Zhen, S., 1998. An exceptionally well-preservedtheropod dinosaur from the Yixian formation of China. Nature391, 147–152.

laessens, L.P.A.M., 1997. Gastralia. In: Currie, P.J., Padian, K.(Eds.),Gastralia. Encyclopedia of Dinosaurs. Academic Press,San Diego, pp. 269–270.

rush, P.J., 1984. A late upper triassic sphenosuchid crocodilian fromWales. Palaeontology 27, 131–157.

arwin, C., 1859. The Origin of Species by Means of Natural Selec-tion; or, the Preservation of Favoured Races in the Struggle forLife. Signet Classic, New American Library.

el Sasso, C., Signore, M., 1998. Exceptional soft-tissue preser-vation in a theropod dinosaur from Italy. Nature 392, 383–387.

udley, R., 2002. Mechanisms and implications of animal flightmaneuverability. Integr. Compar. Biol. 42, 135–140.

logy &

D

D

D

E

F

F

F

F

F

F

F

G

G

H

H

H

H

H

H

H

J

K

L

M

M

M

M

M

N

N

O

O

O

O

P


uncker, H.R., 1971. The lung air sac system of birds. A contributionto the functional anatomy of the respiratory apparatus. Ergebnisseder Anatomie und Entwicklungsgeschichte 45, 1–171.

uncker, H.R., 1989. Structural and functional integration acrossthe reptile-bird transition: locomotor and respiratory systems. In:Wake, D.B., Roth, G. (Eds.),Structural and functional integrationacross the reptile-bird transition: locomotor and respiratory sys-tems. Complex Organismal Functions: Integration and Evolutionin Vertebrates. John Wiley and Sons, Chichester.

uncker, H.R., 2004. Vertebrate lungs: structure, topography andmechanics. A comparative perspective of the progressive integra-tion of respiratory system, locomotor apparatus and ontogeneticdevelopment. Resp. Physiol. Neurobiol. 144, 111–124.

wer, R.F., 1965. The anatomy of the codont reptile Euparkariacapensis Broom. Phil. Trans. R. Soc. London B 248, 379–435.

armer, C.G., 1999. The evolution of the vertebrate cardio-pulmonary system. Annu. Rev. Physiol. 61, 573–592.

armer, C.G., Carrier, D.R., 2000. Pelvic aspiration in the Amer-ican alligator (Alligator mississippiensis). J. Exp. Biol. 203,1679–1687.

armer, C.G., Carrier, D.R., 2000a. Ventilation and gas exchangeduring treadmill-locomotion in the American alligator (Alligatormississippiensis). J. Exp. Biol. 203, 1671–1678.

armer, C.G., Carrier, D.R., 2000b. Pelvic aspiration in the Amer-ican alligator (Alligator mississippiensis). J. Exp. Biol. 203,1679–1687.

edde, M.R., 1987. Respiratory muscles. In: Brackenbury, J.H.(Ed.),Respiratory muscles. Bird Respiration. CRC Press, BocaRaton, pp. 3–37.

owler, 1936. Marine fishes of West Africa. Bull. Am. Museum Nat.History LXX, 413–414.

rappell, P.B., Hinds, D.S., Boggs, D.F., 2001. Scaling of respiratoryvariables and the breathing pattern in birds: An allometric andphylogenetic approach. Physiol. Biochem. Zool. 74, 75–89.

ans, C., Clark, B., 1976. Studies on ventilation of Caimancrocodilus (Crocodilia: Reptilia). Resp. Physiol. 26, 285–301.

authier, J.A., 1986. Saurischian monophyly and the origin of birds.In: Padian, K. (Ed.),Saurischian monophyly and the origin ofbirds. The Origin of Birds and the Evolution of Flight. MemoirsCalifornial Academy of Sciences, San Francisco, pp. 1–55.

alliday, D., Resnick, R., 1978. Physics. John Wiley and Sons, NewYork.

artzler, L.K., Munns, S.L., Hicks, J.W., 2004. Contribution of thehepatic piston to ventilation in the American alligator, Alligatormississippiensis. FASEB J. 18, A238.4.

icks, J.W., Farmer, C.G., 1998. Lung ventilation and gas exchangein theropod dinosaurs. Science 281, 45–46.

icks, J.W., Farmer, C.G., 1999. Gas exchange potential in reptil-ian lungs: implications for the dinosaur-avian connection. Resp.Physiol. 117, 73–83.

icks, J.W., White, F.N., 1992. Pulmonary gas exchange during inter-
mittent ventilation in the American alligator. Resp. Physiol. 88,23–36.
uxley, T.H., 1870. Further evidence of the affinity between thedinosaurian reptiles and birds. Quart. J. Geol. Soc. London 26,32–38.

P

Neurobiology 154 (2006) 89–106 105

wang, S.H., Norell, M.A., Qiang, J., Keqin, G., 2004. A large comp-sognathid from the early Cretaceous Yixian formation of China.J. Syst. Palaentol. 2, 13–30.

ones, T.D., Ruben, J.A., 2001. Respiratory structure and functionin theropod dinosaurs and some related taxa. In: Gauthier, J.A.,Gall, L.F. (Eds.),Respiratory structure and function in theropoddinosaurs and some related taxa. New Perspectives on the Originand Early Evolution of Birds: Proceedings of the InternationalSymposium in Honor of John H. Ostrom. Peabody Museum ofNatural History, Yale University, New Haven, pp. 443–461.

ing, A.S., McLelland, J., 1975. Birds—Their Structure and Func-tion. Bailliere Tindall, London.

iem, K.F., 1989. Respiratory gas bladders in teleosts: func-tional conservatism and morphological diversity. Am. Zool. 29,333–352.

agnussen, H., Wilmer, H., Scheid, P., 1979. Gas exchange in airsacs: contribution to respiratory gas exchange in duck lungs.Resp. Physiol. 27, 129–146.

aina, J.N., 1989. The morphometry of the avian lung. In: King,A.S., McLelland, J. (Eds.),The morphometry of the avian lung.Form and Function in Birds. Academic Press, London, pp.307–368.

cLelland, J., 1989. Anatomy of the lungs and air sacs. In: King,A.S., McLelland, J. (Eds.),Anatomy of the lungs and air sacs.Form and Function in Birds. Academic Press, London, pp.221–279.

eister, W., 2005. Histological structure of the long bones of pen-guins. Anatom. Rec. 143, 377–387.

olnar, R.E., Kurzanov, S.M., Dong, Z.M., 1990. Carnosauria.In: Currie, P.J., Padian, K. (Eds.),Carnosauria. Encyclopedia ofDinosaurs. Academic Press, San Diego, pp. 3917–3926.

esbitt, S.J., Norell, M.A., 2006. Extreme convergence in thebody plans of an early suchian (Archosauria) and ornithomimiddinosaurs (Theropoda). Proc. R. Soc. London B (publishedonline).

ysten, M., 1962. Etude anatomique des rapports de la vessieaerienne avec l’axe vertebral chez Pantodon buchholzi Peters.Ann. Mus. R. l’Afrique Cent. Sci. Zool. 8, 187–220.

’Connor, P.M.O., 2004. Pulmonary pneumaticity in the postcranialskeleton of extant Aves: a case study examining anseriformes. J.Morphol. 261, 141–161.

’Connor, P.M.O., Claessens, L.P.A.M., 2005. Basic avian pul-monary design and flow-through ventilation in non-avian thero-pod dinosaurs. Nature 436, 253–256.

sborn, H.F., 1916. Skeletal adaptations of Ornitholestes,Struthiomimus, Tyrannosaurus. Bull. Am. Museum Nat. History35, 733–771.

wen, R., 1856. Monograph on the fossil reptilia of the Wealdenand Purbeck Formations. Part III. Dinosauria (Megalosaurus).Palaeontogr. Soc. Monogr. 9, 1–26.

adian, K., 1997. Ornithodira. In: Currie, P.J., Padian, K.(Eds.),Ornithodira. Encyclopedia of Dinosaurs. Academic Press,
San Diego, p. 498.
aul, G.S., 2001. Were the respiratory complexes of predatorydinosaurs like crocodilians or birds? In: Gauthier, J.A., Gall, L.F.(Eds.),Were the respiratory complexes of predatory dinosaurslike crocodilians or birds? New Perspectives on the Origin and

1 logy &

P

P

P

P

P

P

R

R

R

R

R

R

R

S

S

S

S

S

S

S

VV

W

W

WP.J., Padian, K. (Eds.),Craniofacial air sinus systems. Ency-


Early Evolution of Birds: Proceedings of the International Sym-posium in Honor of John H. Ostrom. Peabody Museum of NaturalHistory, Yale University, New Haven, pp. 463–482.

aul, G.S., 2002. Dinosaurs of the Air. John Hopkins UniversityPress, Baltimore.

erry, S.F., 1983. Reptilian Lungs: Functional Anatomy and Evolu-tion. Springer-Verlag, Berlin.

erry, S.F., 1989. Mainstreams in the evolution of vertebrate respira-tory structures. In: King, A.S., McLelland, J. (Eds.),Mainstreamsin the evolution of vertebrate respiratory structures. Form andFunction in Birds. Academic Press, London, pp. 221–279.

erry, S.F., 1992. Gas exchange strategies of reptiles and the originof the avian lung. In: Wood, S., Weber, R., Hargens, A., Millard,R. (Eds.),Gas exchange strategies of reptiles and the origin ofthe avian lung. Physiological Adaptations in Vertebrates; Respi-ration, Circulation, and Metabolism. Marcel Dekker, Inc., NewYork.

erry, S.F., 2001. Functional morphology of the reptilian and avianrespiratory systems and its implications for theropod dinosaurs.In: Gauthier, J.A., Gall, L.F. (Eds.),Functional morphology of thereptilian and avian respiratory systems and its implications fortheropod dinosaurs. New Perspectives on the Origin and EarlyEvolution of Birds: Proceedings of the International Symposiumin Honor of John H. Ostrom. Peabody Museum of Natural His-tory, Yale University, New Haven, pp. 429–441.

oll, M., Nysten, M., 1962. Vessie natatoire pulmonoıde et pneuma-tisation des vertebres chez Pantodon buchholzi Peters. Bull. desSeances 8, 434–454.

eese, A.M., 1915. The Alligator and Its Allies. G.P. Putnam’s Sons,New York.

omer, A.S., 1956. The Osteology of the Reptilia. University ofChicago Press, Chicago.

ommel, S., Reynolds III, J.E., 2000. Diaphragm structure and func-tion in the Florida Manatee (Trichechus manatus latirostris).Anatom. Rec. 259, 41–51.

uben, J.A., Jones, T.D., Geist, N.R., Hillenius, W.J., 1997. Lungstructure and ventilation in theropod dinosaurs and early birds.Science, 1267–1270.

uben, J.A., Dal Sasso, C., Geist, N.R., Hillenius, W.J., Jones, T.D.,Signore, M., 1999. Pulmonary function and metabolic physiol-ogy of theropod dinosaurs. Science 283, 514–516.

uppell, G., 1975. Bird Flight. Van Nostrand Reinhold Company,New York.

Z


ussell, D.A., Dong, Z.M., 1993. A nearly complete skeleton of anew troodontid dinosaur from the Early Cretaceous of the OrdosBasin, Inner Mongolia, People’s Republic of China. Can. J. EarthSci. 30, 2163–2173.

ander, M., Perry, S.F., 2004. Reconstructing the evolution of therespiratory apparatus in tetrapods. Resp. Physiol. Neurobiol. 144,125–139.

cheid, P., 1982. A model for comparing gas-exchange systems invertebrates. In: Taylor, C.R., Johansen, K., Bolis, L. (Eds.),Amodel for comparing gas-exchange systems in vertebrates. ACompanion to Animal Physiology. Cambridge University Press,Cambridge.

cheid, P., Piiper, J., 1989. Respiratory mechanics and air flow inbirds. In: King, A.S., McLelland, J. (Eds.),Respiratory mechanicsand air flow in birds. Form and Function in Birds. AcademicPress, London, pp. 369–391.

eeley, H.G., 1870. On Ornithopsis, a gigantic animal of the ptero-dactyle kind from the Wealden. Ann. Mag. Nat. History (Ser. 4)5, 279–283.

isson, S., Grossman, J.D., 1953. The Anatomy of the DomesticAnimals. W.B. Saunders Company, Philadelphia.

tahl, W.R., 1967. Scaling of respiratory variables in mammals. J.Appl. Physiol. 22, 453–460.

ternberg, C.M., 1933. A new ornithomimus with complete abdom-inal cuirass. Can. Field-Nat. XLII, 79–83.

ogel, S., 1981. Life in Moving Fluids. Willard Grant Press, Boston.on Meyer, H., 1837. Die Bayreuthen Petrefakten-Sammlungen.

Neues Jahrbuch Mineral. Geognosie Geol. Petrefakten-Kunde,314–316.

ebb, P.W., 2002. Control of posture, depth, and swimming trajec-tories of fishes. Integr. Compar. Biol. 42, 94–101.

ellnhofer, P., 1992. A new specimen of Archaeopteryx from theSolnhofen limestone. In: Campbell, E.J. (Ed.),A new speci-men of Archaeopteryx from the Solnhofen limestone. Papers inAvian Paleontology Honoring Pierce Brodkorb. Natural HistoryMuseum of Los Angeles, Los Angeles, pp. 3–23.

itmer, L.M., 1997. Craniofacial air sinus systems. In: Currie,

clopedia of Dinosaurs. Academic Press, San Diego, pp. 151–159.

immer, K., 1935. Beitrage zur Mechanik der Atmung bei denBogeln in Stand und Flug. Zoologica 33, 1–69.

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