Integrative Comparative Biology

Volume 55 Number 6 December 2015www.icb.oxfordjournals.org

Volume 55 Number 6 December 2015

CONTENTS

Integrated Biology of the CrocodiliaOrganized by Valentine Lance

949 Crocodilian Forebrain: Evolution and DevelopmentMichael B. Pritz

962 Similarity of Crocodilian and Avian Lungs Indicates Unidirectional Flow Is Ancestral for ArchosaursC. G. Farmer

972 The Good, the Bad, and the Unknown: Microbial Symbioses of the American AlligatorSarah W. Keenan and Ruth M. Elsey

986 Alligators and Crocodiles Have High Paracellular Absorption of Nutrients, But Differ in Digestive Morphology andPhysiologyChristopher R.Tracy, Todd J. McWhorter, C. M. Gienger, J. Matthias Starck, Peter Medley, S. Charlie Manolis,Grahame J. W. Webb and Keith A. Christian

Origins of Neurons and Parallel Evolution of Nervous Systems: The Dawn of Neuronal OrganizationOrganized by Leonid L. Moroz

1005 Biodiversity Meets Neuroscience: From the Sequencing Ship (Ship-Seq) to Deciphering Parallel Evolution of NeuralSystems in Omic’s EraLeonid L. Moroz

1018 Sensory Flask Cells in Sponge Larvae Regulate Metamorphosis via Calcium SignalingNagayasu Nakanishi, Daniel Stoupin, Sandie M. Degnan and Bernard M. Degnan

1028 Unbiased View of Synaptic and Neuronal Gene Complement in Ctenophores: Are There Pan-neuronal and Pan-synapticGenes across Metazoa?Leonid L. Moroz and Andrea B. Kohn

1050 Cnidarian Nerve Nets and Neuromuscular EfficiencyRichard A. Satterlie

1058 The Sea Slug, Pleurobranchaea californica: A Signpost Species in the Evolution of Complex Nervous Systems and BehaviorRhanor Gillette and Jeffrey W. Brown

1070 Molecular Evidence for Convergence and Parallelism in Evolution of Complex Brains of Cephalopod Molluscs: Insightsfrom Visual SystemsM. A.Yoshida, A. Ogura, K. Ikeo, S. Shigeno,T. Moritaki, G. C.Winters, A. B. Kohn and L. L. Moroz

1084 Employing Phylogenomics to Resolve the Relationships among Cnidarians, Ctenophores, Sponges, Placozoans, andBilateriansNathan V. Whelan, Kevin M. Kocot and Kenneth M. Halanych

1096 DNA Methylation in Basal Metazoans: Insights from CtenophoresEmily C. Dabe, Rachel S. Sanford, Andrea B. Kohn, Yelena Bobkova and Leonid L. Moroz

1111 Parallel Evolution and Lineage-Specific Expansion of RNA Editing in CtenophoresAndrea B. Kohn, Rachel S. Sanford, Masa-aki Yoshida and Leonid L. Moroz

Towards a General Framework for Predicting Animal Movement Speeds in NatureOrganized by Robbie S. Wilson and Jerry F. Husak

1121 Introduction to the Symposium: Towards a General Framework for Predicting Animal Movement Speeds in NatureRobbie S. Wilson and Jerry F. Husak

1125 Predicting the Movement Speeds of Animals in Natural EnvironmentsRobbie S. Wilson, Jerry F. Husak, Lewis G. Halsey and Christofer J. Clemente

1142 Balancing Biomechanical Constraints: Optimal Escape Speeds When There Is a Trade-off between Speed and ManeuverabilityC. J. Clemente and R. S. Wilson

1155 Sex Differences in Incline-Walking among HumansCara M. Wall-Scheffler

1166 How Fast Should an Animal Run When Escaping? An Optimality Model Based on the Trade-Off Between Speed and AccuracyRebecca Wheatley, Michael J. Angilletta Jr, Amanda C. Niehaus and Robbie S. Wilson

1176 An Individual-Based Simulation Approach to the Evolution of Locomotor PerformanceAnn M. Cespedes and Simon P. Lailvaux

1188 Outrun or Outmaneuver: Predator–Prey Interactions as a Model System for Integrating Biomechanical Studies in aBroader Ecological and Evolutionary ContextTalia Y. Moore and Andrew A. Biewener

1198 Book ReviewAnimal Social Networks. Jens Krause, Richard James, Daniel Franks, and Darren Croft, editors.Reviewed by Harold Gouzoules

1200 Erratum

IntegrativeComparative Biology&

IntegrativeComparative Biology&

ISSN 1540-7063 (PRINT)ISSN 1557-7023 (ONLINE)

Integrative &C

omparative Biology

Volume 55

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Editor-in-Chief

Harold Heatwole, North Carolina State University, Raleigh,NC, USA and University of New England, Armidale, NSW,Australia

Assistant Editors

Suzanne C. Miller, North Carolina State University

Editorial Board

Divisional RepresentativesAnimal Behavior (DAB)

Matthew Grober (2018), Georgia State UniversityComparative Biomechanics (DCB)

Anna Ahn (2017), Harvey Mudd CollegeComparative Endocrinology (DCE)

Henry John-Alder (2018), Rutgers UniversityComparative Physiology and Biochemistry (DCPB)

Dane Crossley (2016), University of North DakotaEcoimmunology and Disease Ecology (DEDE)

Ken Field (2020), Bucknell UniversityEcology and Evolution (DEE)

Michael Sears (2017), Clemson UniversityEvolutionary Developmental Biology (DEDB)

Robert Zeller (2018), San Diego State UniversityInvertebrate Zoology (DIZ)

Bruno Pernet (2020), California State University,Long Beach

Neurobiology (DNB)Richard A. Satterlie (2018), University of NorthCarolina at Wilmington

Phylogenetics and Comparative Biology (DPCB)Lars Schmitz (2019), W.M. Keck Science Department ofClaremont McKenna, Pitzer, and Scripps Colleges

Vertebrate Morphology (DVM)Lara Ferry (2016), Arizona State University

Associates

Dominique Adriaens (2016), University of Ghent,Ghent, BelgiumChristopher R. Bridges (2016), Heinrich-HeineUniversitat, Dusselforf, GermanyBerry Pinshow (2016), Ben Gurion University of theNegev, IsraelJulia Sigwart (2018), Queen’s University Belfast

Executive Officers, Society for Integrative andComparative Biology

PresidentPeter Wainwright (2017)

President-ElectLouis Burnett (2017)

Past PresidentBillie Swalla (2016)

SecretaryKathy Dickson (2018)

Program OfficerSherry Tamone (2016)

Program Officer ElectRichard Blob (2016)

TreasurerKaren Martin (2019)

Members-At-LargeCheryl Wilga (2016)L. Patricia Hernandez (2017)Jennifer Bunaford (2018)

Divisional ChairsDAB Chair: Diana K. Hews (2016)DCB Chair: Melina Hale (2017)DCE Chair: Mary Mendonca (2016)DCPB Chair: Stephen Secor (2016)DEDB Chair: Sally Leys (2016)DEDE Chair: Lynn Martin (2017)DEE Chair: Michael Sears (2017)DIZ Chair: John Zardus (2018)DNB Chair: Paul Moore (2018)DPCB Chair: Michael E. Alfaro (2016)DVM Chair: Callum Ross (2017)

Editor-in-Chief, ICB: Harold F. Heatwole (2016)SPDAC Chair: Sean Lema (2016)Ed. Council Chair: Bram Lutton (2018)BPC Chair: Michele Nishiguchi (2016)Executive Director: Brett J. Burk

Cover image: Top panel: Lateral view of a parasagittal section of computed tomography (CT) data of the lung of an Americanalligator (Alligator mississippiensis) with three of the conducting airways rendered in color. During both inspiration andexpiration, airflow in the green bronchus is caudad, toward the right of the image, and craniad in the yellow and blue airways.Middle panel: lateral view of CT data of alligator showing position of the lungs in the thoracic cavity. Bottom panel: An adultalligator in South Carolina is photographed in the high walk. See the article, ‘‘Similarity of Crocodilian and Avian LungsIndicates Unidirectional Flow Is Ancestral for Archosaurs’’ by C.G. Farmer for more information. Photo by Phil Wilkinson.

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SYMPOSIUM

Similarity of Crocodilian and Avian Lungs Indicates UnidirectionalFlow Is Ancestral for ArchosaursC. G. Farmer1

257 S 1400 E, Salt Lake City, UT 84112, USA

From the symposium ‘‘Integrated Biology of the Crocodilia’’ presented at the annual meeting of the Society for

Integrative and Comparative Biology, January 3–7, 2015 at West Palm Beach, Florida.

1E-mail: [email protected]

Synopsis Patterns of airflow and pulmonary anatomy were studied in the American alligator (Alligator mississippiensis),

the black caiman (Melanosuchus niger), the spectacled caiman (Caiman crocodilus), the dwarf crocodile (Osteolaemus

tetraspis), the saltwater crocodile (Crocodylus porosus), the Nile crocodile (Crocodylus niloticus), and Morelet’s crocodile

(Crocodylus moreletii). In addition, anatomy was studied in the Orinoco crocodile (Crocodylus intermedius). Airflow was

measured using heated thermistor flow meters and visualized by endoscopy during insufflation of aerosolized propolene

glycol and glycerol. Computed tomography and gross dissection were used to visualize the anatomy. In all species studied

a bird-like pattern of unidirectional flow was present, in which air flowed caudad in the cervical ventral bronchus and its

branches during both lung inflation and deflation and craniad in dorsobronchi and their branches. Tubular pathways

connected the secondary bronchi to each other and allowed air to flow from the dorsobronchi into the ventrobronchi. No

evidence for anatomical valves was found, suggesting that aerodynamic valves cause the unidirectional flow. In vivo data

from the American alligator showed that unidirectional flow is present during periods of breath-holding (apnea) and is

powered by the beating heart, suggesting that this pattern of flow harnesses the heart as a pump for air. Unidirectional

flow may also facilitate washout of stale gases from the lung, reducing the cost of breathing, respiratory evaporative water

loss, heat loss through the heat of vaporization, and facilitating crypsis. The similarity in structure and function of the

bird lung with pulmonary anatomy of this broad range of crocodilian species indicates that a similar morphology and

pattern of unidirectional flow were present in the lungs of the common ancestor of crocodilians and birds. These data

suggest a paradigm shift is needed in our understanding of the evolution of this character. Although conventional

wisdom is that unidirectional flow is important for the high activity and basal metabolic rates for which birds are

renowned, the widespread occurrence of this pattern of flow in crocodilians indicates otherwise. Furthermore, these

results show that air sacs are not requisite for unidirectional flow, and therefore raise questions about the function of

avian air sacs.

Introduction

Thomas Huxley, with his usual sagacity, pointed outthe importance of the similarity of the respiratorysystems of crocodilians and birds when he wrote,

Thus, not withstanding all the points of difference,there is a fundamental resemblance between the re-spiratory organs of Birds and those of Crocodiles;pointing to some common form (doubtless exem-plified by some of the extinct Dinosauria), of whichboth are modifications (Huxley 1882).

More than a hundred years after Huxley’s work, adeeper understanding of the striking similarity

between these lungs became evident with the discov-ery that crocodilians share with birds a rather re-markable pattern of unidirectional airflow, in whichgases move throughout most of the conducting air-ways in the same direction during both inhalationand exhalation due to the presence of aerodynamicvalves (Farmer 2010; Farmer and Sanders 2010). Theimportance of this discovery lies not only in expand-ing our understanding of the fundamental resem-blance of these respiratory systems, adding to thepreponderance of evidence that allies these clades,but also in the broader context of demonstratingagain the fallacy of the argument of irreducible

Integrative and Comparative BiologyIntegrative and Comparative Biology, pp. 1–10doi:10.1093/icb/icv078 Society for Integrative and Comparative Biology

! The Author 2015. Published by Oxford University Press on behalf of the Society for Integrative and Comparative Biology. All rights reserved.For permissions please email: [email protected].

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complexity, for which the avian lung has been heldup as an example (Denton 1985).

The avian respiratory system is certainly complex(Duncker 1971; Maina 2000): Akester (1960) statedthat it is, ‘‘..the most complicated respiratory systemthat has ever evolved’’. This complexity appears tohave led to a number of erroneous views. Most no-table is the error of linking patterns of skeletal pneu-maticity to patterns of airflow and efficiency of gasexchange. King (1957), in his study of patterns ofpneumaticity of the domestic chicken, noted thatthese patterns vary widely from one individual tothe next, and even between different sides of thebody of the same individual, and that a lack of com-prehension of this variability has led to invalid gen-eralizations about pneumaticity. King (1957) arguedthat it is paramount to understand this variability inorder to ascertain the limits of generalizations.Indeed, he stated, ‘‘It is a remarkable fact that afterthree centuries of research all the great questions ofthe functional anatomy of the avian respiratory tractstill remain unanswered’’ and attributed the slowprogress to a failure to recognize fundamental vari-ations in structure and function in different avianspecies. Further evidence against linking patterns ofpneumaticity to patterns of airflow and efficiency ofgas exchange is discussed elsewhere (Farmer 2006).Another problem that has plagued understanding ofthese respiratory systems is that numerous authorsuse anatomy alone to extrapolate informationabout physiology, when what is needed are empirical,physiological data to draw conclusions based on ev-idence. For example, numerous publications statethat the anatomy of crocodilians is consistent withcrosscurrent gas exchange and therefore this mecha-nism of gas exchange was probably present in dino-saurs too (see discussion of this topic by Perry andSander (2004) and references therein). However,crosscurrent gas exchange cannot be determined bystudies of the anatomy. Measurements on blood andlung gases are requisite to elucidate the mechanismof gas exchange in these lungs. A third area of con-fusion is the role of the air sacs in the aerodynamicvalves. In a brilliant and technically extraordinarystudy, Brackenbury (1989) bilaterally occluded theabdominal air sacs, as well as the cranial andcaudal thoracic air sacs, and found no effect on theaerodynamic valve in resting or in exercising chick-ens. However, other workers conclude, ‘‘abdominalair sacs . . . are crucial for unidirectional flow in thepaleopulmo of birds’’ (Perry and Sander 2004) eventhough the abdominal sacs in some birds, such as thekiwi, are so reduced in size their existence has beendebated (Huxley 1882).

The avian respiratory system consists of a networkof conducting airways that anastomose to form acircuit: this architecture lies in stark contrast to themore familiar blindly ending bronchial tree of mam-mals. The avian airways connect to avascular air sacs,which effect ventilation. The functional underpin-nings of this design are not understood in spite ofa long history of study, which is reviewed byDuncker (1971) dating back to work by the Dutchanatomist and physician, Volcher Coiter (1573), andby Allen (1951) for avian studies dating back toAristotle (Coiter 1573; Allen 1951). Initially, studiesand speculations about patterns of airflow throughthis circuit attributed the unidirectional flow tophysical valves, either passive leaflets such as thosefound in the heart or the veins, or active sphincters(Brandes 1924; Bethe 1925; Portier 1928;Dotterweich 1930, 1936; Wolf 1933; Vos 1934).However, Hazelhof (1951) demonstrated that thisflow can arise from the topography of the airwaysand that mechanical valves are not requisite, norhave they been found (Hazelhoff 1951). Hazelhoff’sexperiments and ideas have been refined and vali-dated by a number of investigations (Brackenbury1971, 1972, 1979; Bret and Schmidt-Nielsen 1972;Scheid and Piiper 1972, 1989; Scheid et al. 1972;Banzett et al. 1987, 1991; Butler et al. 1988; Kuethe1988; Wang et al. 1992; Brown et al. 1995; Mainaand Africa 2000). Butler et al. (1988) suggested fourpossible mechanisms governing gas flow in birds: (1)elastic pressures associated with the changes involume of the air sacs, (2) resistive pressures arisingfrom gas friction, (3) unsteady inertial pressures aris-ing from the acceleration and deceleration of airwaygas during the inspiratory–expiratory cycle, (4) dy-namic pressures arising from convective momentumof gas. Gases of differing densities and velocity wereused to gain insight into the importance of convec-tive inertia, especially for the inspiratory valve (Wanget al. 1988; Brown et al. 1995). These studies showedthat convective momentum, which is a function ofthe density of the gas multiplied by the square of itslinear speed, is key to the inspiratory valve (Wanget al. 1988). The mechanical underpinnings of theexpiratory valve are less well understood.Furthermore, the importance of certain anatomicalfeatures for the functioning of both the inspiratoryand expiratory valves is still unclear.

Duncker (1971) reviewed and discussed features ofthe anatomy that may play essential roles in theaerodynamic valves. He listed:

(1) The point of origin of the ventrobronchi, withrigidly extended openings directed cranially, so

2 C. G. Farmer

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that these airways form an acute angle with theintrapulmonary bronchus. These bronchi dilateremarkably in width.

(2) The origin of the dorsobronchi in the region ofthe primary bronchus that arches with the con-cave side mesial. The initial portions of thedorsobronchi are narrow and their diameterscan be regulated. The dorsobronchi also formacute angles with the primary bronchus.

(3) The origin of the laterobronchi opposite to theanterior dorsobronchi, their initial angle alsoforming an acute angle with the intrapulmon-ary bronchus.

(4) Connection of the posterior air sacs to the pri-mary laterobronchus.

Other features that have been suggested to play a rolein the aerodynamic valves include a narrowing of theprimary bronchus proximal to the opening of theventrobronchi, the segment accelerans (Wang et al.1992), and an expansion of the width of the intra-pulmonary bronchus prior to the openings ofthe dorsobronchi. Finally, as previously mentioned,the air sacs have been purported to play a role in thevalve (see Perry and Sander 2004).

The discovery of the same pattern of airflow incrocodilians with similar anatomical features asbirds provides an opportunity to identify common,conserved features that may be important to theaerodynamic valves. Although this study focuses ondocumenting patterns of airflow in crocodilians, Ihave also attempted to identify common anatomicalcharacters of crocodilians and birds to help throwinto sharp relief the features that may be fundamen-tally important for the aerodynamic valves fromthose that are unimportant. I have relied heavilyon Duncker’s (1971) monograph for generalizationsabout avian anatomy. These comparisons are meantto stimulate and help direct further empirical re-search, which will perhaps expand our understandingof the aerodynamic valves both of birds and of croc-odilians, as well as elucidate selective drivers for thesepatterns of flow. In the summary, I speculate onseveral testable hypotheses for these selective drivers.

Materials and methods

In vivo experiments

In vivo procedures were approved by the Universityof Utah Animal Care and Use Committee and werecarried out on the American alligators. I measuredintrapulmonary airflow by implanting a dual therm-istor flow meter (HEC 132 C, Hector Engineering,Ellettsville, IN, USA). I visualized airflow using an

endoscope with a diameter of 0.9 mm (Modelnumber HSF 009 1000 NVK, Hawkeye Pro MicroflexBorescope, Gradient Lens Corporation) and with afield of view of 55 degrees. I held the scope in onelocation while animals insufflated an aerosolized mix-ture of propylene glycol and glycerol (Froggy’s Fog—Swamp Juice, Froggys Fog, LLC) and I recorded videosusing a Luxxor Video Camera System (LXX-VBSM)that was interfaced to a computer with a USB 2.0Image Capture Interface (VC-USB2). I recorded thevideos with Debut Video Capture software at a rateof frame capture of 29.97 frames per second and deter-mined the direction of airflow visually. I recorded air-flow at the nares with a pneumotachograph (HansRudolph Inc.). I amplified this signal with an AC/DCstrain gauge amplifier (P122, Grass Instruments,Warwick, RI, USA) and converted all analog signalsto digital (Biopac Systems, Goleta, CA, USA) at a sam-pling rate of 60 Hz and recorded these signals on acomputer using AcqKnowledge software (BiopacSystems). I measured the electrocardiogram using cu-taneous leads, sampling at 200 Hz and filtering andamplifying the signals (P122, Grass Instruments).

Ex vivo experiments

I measured airflow in separate experiments in excisedlungs by implanting a dual thermistor flow meter(HEC 132 C, Hector Engineering) or by visualizationof aerosolized propylene glycol and glycerol as de-scribed in the in vivo methods. I intubated the tra-chea and ventilated the lung with a syringe. Imeasured tracheal flow with a pneumotachograph(Hans Rudolph Inc.) as described in the in vivomethods. Sample sizes varied depending on species.The largest sample sizes were obtained for theAmerican alligator (N¼ 11), the saltwater crocodile(N¼ 10), and the spectacled caiman (N¼ 5), and soconclusions are weighted toward these species.Sample size was 3 or less for the remaining species.Information on mass was not available for all theindividuals because of variation in the way theywere obtained. For example, in many of the animalsonly torsos were available, having been donated byabattoirs. Where this information is known it isreported.

Anatomy

To visualize the anatomy I used both gross dissec-tions and computed tomography. I reconstructedthese CT data into images with OsiriX (v.5.8.264-bit).

Unidirectional flow in crocodilian lungs 3


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Results and discussion

Much of the anatomy of the lungs of alligators andcrocodiles has been described previously (Huxley1882; Perry 1989, 1990; Farmer and Sanders 2010;Sanders and Farmer 2012; Schachner et al. 2013).The focus here is investigating whether or not uni-directional flow is common throughout the crocodil-ians and highlighting features that have not beendescribed previously in detail, or features that arecommon to all the crocodilians I have studied todate and which can be compared with similar fea-tures in birds. I also noted differences that corrobo-rate or cast doubt on the role of aspects of aviananatomy in the aerodynamic valve.

In many crocodiles (e.g., Crocodilus niloticus,Crocodylus porosus, Crocodylus palustris, Crocodylusintermedius), this study (Huchzermeyer 2003; Griggand Kirshner 2015); and some birds (Clench 1978;Fitch 1999), the trachea and primary bronchi do nottravel a straight course to the lungs, but form loopsin larger individuals (Fig. 1). In birds this loop isthought to play a role in sound production (Fitch1999). Its function in crocodilians is unknown. Incontrast, the trachea of alligators, spectacledcaiman, black caiman, and the dwarf crocodile runin a straight course to the carina and the primarybronchi also course directly toward their respectivelungs (this study; also Grigg and Kirshner 2015).Sound production in alligators occurs in the larynx(Riede et al. 2011, 2015) but a role for the tracheahas not been ruled out. Unidirectional flow occurredindependently of the presence or absence of a loop-ing trachea.

The position of the lungs within the thoraciccavity was consistent across all species examined.The dorsal mesentery, a median vertical sheet oftissue, forms a septum in the thoracic cavity andcranial abdominal cavity. The alimentary canal runsthrough the middle of the sheet while the lungs andtwo halves of the liver lay to either side. The lungsoccupy the right and left sides of the cranial regionof the thoracic cavity, the pleural cavity, the apexextending to the eighth or ninth cervical vertebraand the base extending in its dorsal portion to ap-proximately the ninth thoracic vertebra (Fig. 1A–C)(Mushonga and Horowitz 1996). Here the lungattaches to the liver through the pulmohepatic liga-ment, which forms part of the wall (mainly lateral)of a recess between the liver and the lung, the hepa-topulmonary bursa (Fig. 1) (Butler and Parker 1889;Mushonga and Horowitz 1996). These bursae com-municate through a narrow passage with the pleuralcavities. The hepatopulmonary ligament passes into a

membranous tract that merges with the caudal lungand the mediastinal tissue. It has been proposed thatthis serous tissue is homologous with the avian obli-que septum (Huxley 1870; Butler and Parker 1889;Pool 1909), which fuses with the dorsal pericardiumand together with the dorsal portion of the sternumseparates the avian body into a cavum respiratorium,containing the lungs and all air sacs except the ab-dominal air sac, and caudoventrally into a cavumcardioabdominale, containing the heart, liver, ali-mentary tract, and abdominal air sacs. In birds, thecavum respiratorium is subdivided by the horizontalseptum (avian diaphragm), the lungs, and intrapul-monary bronchi lying dorsal to the horizontalseptum in the cavum pulmonale, and all the airsacs except the abdominal air sacs lying ventral tothe horizontal septum in the cavum subpulmonale(Duncker 1971). In birds the oblique and horizontalsepta are formed when portions of the lung invadethe pulmonary folds and divide them, the ventralportion of the fold giving rise to the obliqueseptum and the dorsal portion giving rise to thehorizontal septum (Pool 1909; Duncker 1971). Incrocodilians a similar topography exists with thegas-exchange parenchyma lying dorsal to the ventralaspects of the intrapulmonary bronchus and the sac-cular regions of the lung lying dorsal to the repre-sentative of the oblique septum (Fig. 1C) but ventralto the intrapulmonary bronchus, in the topographi-cal position of the avian horizontal septum. Figure 1illustrates the topographical location in the bodycavity of the avian horizontal and oblique septa,superimposed on the lateral image of an Americanalligator.

In crocodilians the parietal pleura attaches dorsallyto the longus colli muscles, the bodies of the lastcervical and the thoracic vertebral bodies, and tothe intercostal muscles and ribs. Deep sulci areformed in the lungs by the ninth cervical ribs and,to a lesser degree, the subsequent thoracic ribs.Ventromedially the lung attaches directly to the me-diastinal pleura and ventrally to the esophagus. Thepleural space, where the visceral and parietal pleuraare readily separated, completely surrounds theapical region of the lung to the root of the lung,demarcated by the hilus, but is found only dorsallyand laterally caudal to the hilus (Fig. 1). The primarybronchus and pulmonary vessels enter the ventrome-dial aspect of the lung approximately half way be-tween the apex and the dorsal portion of the base(Fig. 1). At the hilus, the pulmonary artery is cranialand the pulmonary vein caudal to the bronchus. Themedioventral surface of the lung caudal to the hilusdoes not float freely in the pleural cavity but adheres

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Fig. 1 Anatomy and patterns of airflow in crocodilians. American alligator (A–G) in lateral view (A–D), dorsal view (E–F), and ventral

view (G). The apex of the lung can be seen underling cervical vertebrae 8 and 9 while the dorsal part of the base of the lung extends

to thoracic vertebra 9. View of transection in the parasagittal plane without (B) and with (C) colored voxels illustrating the airways.


(continued)


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to the underlying structures of the pericardial sac,portions of the liver, left and right aorta, and esoph-agus, except where there are bursae, as noted aboveand by Mushonga and Horowitz (1996).

The intrapulmonary bronchus retains cartilaginoussupport in its most proximal portion, but this is lostas the bronchus courses laterally, caudally, and dor-sally. In alligators, the bronchus increases in diameteralong this path until it approaches the level of ver-tebral centra at which point it curves medially andgradually decreases in diameter as it continues to thedorsal base of the lung (Fig. 1). The first secondarybronchus to arise from the primary bronchus does sofrom its lateral aspect very near the midline of thelung in the sagittal plane (Fig. 1). The opening tothis bronchus is a conical, cartilaginous structurethat contains smaller ostia in its walls. The conicalportion of the CVB opens into a secondary bronchusthat is poorly vascularized and widens remarkably asit courses craniad. It is the largest of the secondaryairways, and extends to lie alongside the cervical ver-tebra. This bronchus has been termed the cervicalventral bronchus (CVB) (Farmer and Sanders 2010;Sanders and Farmer 2012) and postulated to be ho-mologous to the avian embryonic mesial moiety ofthe first ventrobronchus that develops into the cer-vical air sac and to the first avian ventrobronchus.Measurements of flow have been made in this bron-chus in all species and the flow is always caudad (Fig.1). The volume of this bronchus indicates it is serv-ing both a storage function and as a major conduct-ing airway. It is the same airway termed D1 byBroman (1940). The ostia of the conical portion ofthe CVB connect to several other poorly vascularizedbronchi that run in tandem along the CVB, althoughnot as far craniad.

On the dorsal aspect of the intrapulmonary pri-mary bronchus, very near the ostium to the CVB, alarge and long bronchus arises that courses dorsally

and then cranially (M1 of Broman 1940, and redbronchus of Fig. 1), coursing medially and parallelto the CVB (Fig. 1). There is very little distance be-tween the ostium of M1 and the CVB and yet theflow runs craniad in M1, as it does in the remainingdorsobronchi (Fig. 1). M1 has clear connections tomedioventral locules (chambers) that overlie theheart. These locules occupy the location of the inter-clavicular and thoracic air sacs of birds. There is nofusion of the locules at the midline, as there is withthe avian interclavicular sacs. The intimate connec-tion of these chambers to the heart implicates themin generating the cardiogenic unidirectional airflowmeasured during apnea (Farmer 2010) (Fig. 2). Asthe heart beats it may mechanically agitate these loc-ules, which are firmly attached to the pericardium,producing airflow. However, cardiogenic flow mayalso arise from the pulsations of the blood vesselswithin the lungs. Further experiments are neededto sort out the mechanisms underlying cardiogenic,unidirectional flow.

Small parabronchi connect the ventrobronchusand its branches to the network of dorsobronchi,conducting air through the majority of gas-exchangeparenchyma (Fig. 1). The minimum diameters ofthese connections are approximately 1 mm, whichfalls within the size range of the diameters for theavian parabronchi (Duncker 1971).

Besides the region of the lung that overlies theheart, the caudoventral aspect of the lung is alsocomposed of poorly vascularized locules (Fig. 1).The diameters of the ostia to these chambers tendto be much smaller than those leading to the dorso-bronchi and they lie opposite the ostia to the dorso-bronchi, perhaps serving to direct flow into thedorsobronchi during exhalation. Based on their to-pographical position in the body and the patterns offlow in these locules, which is primarily tidal, they

Fig. 1 Continued

Dashed lines (C) illustrate purported homologs of the oblique septum (small dots) and the topological position corresponding to the

avian diaphragm ¼ horizontal septum (large dots). Arrows indicate direction of airflow. Ventral view (G) illustrates the intimate location

of the pericardium with the lungs. (H) Dorsal view of spectacled caiman showing the position in the body and the CVB and

caudoventral locules. (I) Ventral view of adult female Orinoco crocodile showing looping trachea and primary bronchi. (J–L) Saltwater

crocodile. (J) Ventral view of juvenile shows looping trachea whereas the trachea is straight in a hatchling (K). (L) Dorsolateral view of

juvenile showing the parietal pleura (reflected back), the visceral pleura, and the pulmohepatic bursa, the roof of which has been

suggested to be homologous to the avian oblique septum. (M, N) Unhatched crocodilian. (M) The plane of section (40) shown in N.

(N) A number of features illustrated in (C) and (L), including parietal and visceral pleura, pleural cavity (cavum pulmonale), pulmo-

hepatic ligament (homolog of avian oblique septum), pulmohepatic recess¼ hepatopulmonary bursa. CVB, cervical ventrobronchus;

c, cervical vertebra; d, dorsal vertebra; D2, dorsobronchi 2; D3, dorsobronchi 3; da, representative (homolog) of avian

diaphragm¼ horizontal septum; h, right lobe of the liver; h0, left lobe of the liver lobe; l, laterobronchi¼ caudoventral locules; m.d.,

diaphragmaticus muscle; oe, esophagus; p, parabronchi and gas-exchange parenchyma; pe, pericardium; p.p., parietal pleura; pul, lung;

spl0, fatty ‘‘spleen’’, st., stomach cavity; t, trachea; !, pulmohepatic ligament¼ homolog of avian oblique septum; ", omental septum

(ventral portion of posthepatic septum); 2, right pulmohepatic recess¼ hepatopulmonary bursa; 20, left pulmohepatic recess; 3, peri-

toneal cavity; 4, pleural cavity; 48, pulmohepatic portion of body-cavity; M, N after, Butler and Parker (1889); D, E after, Farmer and

Sanders (2010).

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Fig. 2 Cardiogenic unidirectional flow. (A–C) Electrocardiograms and flow traces collected from the cervical ventrobronchus and a

dorsobronchus for three different animals. (A) and (B) were collected during a period of apnea. No breathing is shown. The trace

shown in (C) was collected shortly after the animal ran on a treadmill and includes a recording of airflow at the nares recorded with a

pneumotachograph.



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appear to be homologous to the avian laterobronchiand air sacs.

Summary

In this study unidirectional flow was measuredduring ventilation in excised lungs in all speciesstudied, with flow in the CVB running caudad andflow in the dorsobronchi running craniad (Fig. 1). Inaddition, unidirectional flow was measured in vivo inAmerican alligators. This unidirectional flow contin-ued during periods of apnea, powered by the beatingheart (Fig. 2).

Birds and crocodilians share a number of pulmo-nary features that are strikingly similar, suggestingthat a similar topography was present in theircommon ancestor. These features include the separa-tion of the thoracoabdominal cavity by an obliqueseptum into a cavum respiratorium and a cavumcardioabdominale. The cavum respiratorium is fur-ther subdivided into a region bounded ventrally bythe oblique septum and dorsally by the ventral floorof the intrapulmonary bronchus. This region is rem-iniscent of the avian cavum subpulmonale and con-tains avascular locules reminiscent of the avian airsacs. The region containing the intrapulmonarybronchus and the dorsobronchi and parabronchilies dorsal, in the pleural cavity, the cavum pulmo-nale. Another striking similarity is the acute angleformed between the intrapulmonary bronchus andthe ventrobronchi, with rigidly extended openingsinto the ventrobronchi, which dilate remarkably.This topography seems well conserved and may beimportant to the aerodynamic valve.

However, several observations of the anatomy ofcrocodilians also suggest that we do not fully under-stand the aerodynamic valves in either crocodiliansor birds. Duncker (1971) reviewed and discussed fea-tures of the anatomy of birds’ lungs that may playroles in the aerodynamic valves (see the above dis-cussion). However, many of these characters are notpresent in crocodilians. For example, avian style airsacs and a segment accelerans are not present incrocodilians. Duncker (1971) proposed that theorigin of the dorsobronchi in the region of the pri-mary bronchus where it arches in a convex mannernear the lateral body wall is important. However, thefirst dorsobronchus of crocodilians arises very nearthe ostium to the CVB, well before the intrapulmon-ary bronchus begins its curve toward medial in themidline, suggesting that the topographical positionof the dorsobronchi in birds at the medial bend ofthe intrapulmonary bronchus may not play a role inthe valve. However, the relationship between the

ostia of the dorsobronchi and the avascular loculesin crocodilians and the avian dorsobronchial ostia tothe air sacs is very consistent, and supports a role ofthis topography in the expiratory valves. Finally, inboth clades the intrapulmonary bronchus dilatesconsiderably in its caudal course, also suggesting anaerodynamic function. The sensitivity of the aerody-namic valves to these features may be revealed bycomputational studies of fluid dynamics. These dif-ferences may mean that the same mechanisms do notunderpin the aerodynamic valves of crocodilians andbirds. The differences certainly underscore the needfor additional research into this fascinating area ofbiology.

The looping pattern of flow seen in birds andcrocodilians shares so many remarkable featuresthat the parsimonious explanation for this similarityis shared inheritance as originally proposed byHuxley (1882). This discovery begs the question ofthe functional significance for this pattern of flow. Ithas recently been postulated (Farmer 2015) that theunidirectional pattern of flow is serving to efficientlyflush gases from the lung, thereby reducing thenumber of breaths required compared with the ex-ponential wash out seen in mammals. For example,in humans a tidal volume of about 0.5 L is mixedwith a residual lung volume of about 3 L with eachbreath, diluting the freshly inspired air (West et al.2007). In contrast, with unidirectional flow a bolusof air moves from one compartment of the lung tothe next, reducing the mixing of stale and freshlyinspired air. Thus, unidirectional flow could reducerates of ventilation for a given rate of gas exchange,thereby reducing the work of breathing, reducing re-spiratory water loss, conserving heat, and improvingcrypsis. It has also been postulated that cardiogenic,unidirectional flows facilitate gas exchange duringapnea (Farmer 2010).

Acknowledgments

I am grateful to Valentine Lance for organizing thissymposium and for the invitation to speak and tothe Society of Integrative and Comparative Biologyfor supporting the symposium. I thank CraigFranklin, Rebecca Cramp, the University ofQueensland, and the Natural History Museum ofUtah for assistance obtaining CITES permits. Ithank Robert Cieri, Jim Dicks, Ruth Elsey, JohnHutchinson, Adam Huttenlocker, Suzy Munns,Essie Rodgers, Kent Sanders, Emma Schachner,Kent Vliet, and Tobias Wang for help in obtainingspecimens or scans. I thank Gordon Grigg for manyinsightful conversations.

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Funding

This work was supported by the National ScienceFoundation (IOS 1055080).

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