DOI: 10.5061/dryad.3xsj3txdh
title: Anatomy, ontogeny, and evolution of the archosaurian respiratory system: a case study on Alligator mississippiensis and Struthio camelus

description: The avian lung is highly specialized and is both functionally and
 morphologically distinct from that of their closest extant relatives, the
 crocodilians. It is highly partitioned, with a unidirectionally ventilated
 and immobilized gas-exchanging lung, and fully decoupled, compliant,
 poorly vascularized ventilatory air-sacs. To understand the evolutionary
 history of the archosaurian (birds, crocodilians and their common
 ancestors) respiratory system, it is essential to determine which
 anatomical characteristics are shared between birds and crocodilians and
 the role these shared traits play in their respective respiratory biology.
 To begin to address this larger question, we examined the anatomy of the
 lung and bronchial tree of ten American alligators (Alligator
 mississippiensis) and eleven ostriches (Struthio camelus) across an
 ontogenetic series using traditional and micro-computed tomography (µCT),
 three-dimensional (3D) digital models, and morphometry. Intraspecific
 variation and left to right asymmetry were present in certain aspects of
 the bronchial tree of both taxa but was particularly evident in the
 cardiac (medial) region of the lungs of alligators and the caudal aspect
 of the bronchial tree in both species. The cross-sectional area of the
 primary bronchus at the level of the major secondary airways and
 cross-sectional area of ostia scaled either isometrically or negatively
 allometrically in alligators and isometrically or positively
 allometrically in ostriches with respect to body mass. Of fifteen lung
 metrics, five were significantly different between the alligator and
 ostrich, suggesting that these aspects of the lung are more
 interspecifically plastic in archosaurs. One metric, the distances between
 the carina and each of the major secondary airways, had minimal
 intraspecific or ontogenetic variation in both alligators and ostriches,
 and thus may be a conserved trait in both taxa. In contrast to previous
 descriptions, the 3D digital models and CT scan data demonstrate that the
 pulmonary diverticula pneumatize the axial skeleton of the ostrich
 directly from the gas-exchanging pulmonary tissues instead of the air
 sacs. Global and specific comparisons between the bronchial topography of
 the alligator and ostrich reveal multiple possible homologies, suggesting
 that certain structural aspects of the bronchial tree are likely conserved
 across Archosauria, and may have been present in the ancestral
 archosaurian lung.
description: CT scans were obtained from ten specimens of American alligator
 (<i>A. mississippiensis</i>)<i>, </i>and eleven
 ostriches (<i>S. camelus</i>) (see Table 1 in the associated
 manuscript for specifics on the size, age and details on individual
 specimens used in this study). The alligators were obtained from the
 Louisiana Department of Wildlife and Fisheries at the Rockefeller Wildlife
 Refuge; deceased animals were harvested for purposes unrelated to this
 study. Five scans were performed on lungs stained with potassium iodide
 (I<sub>2</sub>KI) (four <i>A. mississippiensis</i>
 and one <i>S. camelus</i>). The <i>S. camelus</i>
 specimens were obtained from the OK Corral Ostrich Farm in Southern
 California and acquisitioned into the collections of the University of
 California Museum of Vertebrate Zoology (MVZ) and the Royal Veterinary
 College, London. The juvenile ostriches died of natural causes and were
 donated to the MVZ for research purposes. With the exception of the
 alligator hatchling and the adult ostrich, all animals were scanned at
 either the University of Utah Medical Center, Research Park, or the South
 Jordan Medical Center on a 164 slice dual energy Siemens SOMATOM
 Definition computed tomography unit. Image acquisition parameters
 included: slice thickness 0.6–1 mm, 120 kVp, 200–400 MA (Table 1). The
 data scanned at the University of Utah were filtered in soft tissue and
 lung algorithm and edge-enhanced with a high-resolution lung
 algorithm.
description: <b>Ostrich 1:</b> Computed tomography
 (CT) scan of an intact deceased <i>Struthio camelus</i>
 juvenile (0.861 kg) with the respiratory system artificially inflated.
 This specimen was scanned at the University of Utah South Jordan Medical
 Center (UUSJMC) on 10-26-2012 on a 164 slice dual energy Siemens SOMATOM
 Definition CT unit (kV 100, mA 400; slice thickness 0.6 mm). The data were
 filtered in soft tissue and lung algorithm and edge-enhanced with a
 high-resolution lung algorithm.<br>   
 <b>Ostrich 2:</b> CT scan of a deceased <i>S.
 camelus</i> juvenile (0.823 kg) with the lungs artificially
 inflated. This specimen was scanned at the UUSJMC on 10-26-2012 on a 164
 slice dual energy Siemens SOMATOM Definition CT unit (kV 100, mA 400;
 slice thickness 0.6 mm). The data were filtered in soft tissue and lung
 algorithm and edge-enhanced with a high-resolution lung algorithm. This
 individual specimen does not have a head.<br>  
 <b>Ostrich 3:</b> CT scan of a deceased <i>S.
 camelus</i> juvenile (1.125 kg) with the respiratory system
 artificially inflated. This specimen was scanned at the UUSJMC on
 10-26-2012 on a 164 slice dual energy Siemens SOMATOM Definition CT unit
 (kV 100, mA 400; slice thickness 0.6 mm). The data were filtered in soft
 tissue and lung algorithm and edge-enhanced with a high-resolution lung
 algorithm. This individual specimen did not stay inflated.<br>
   <b>Ostrich 4:</b> CT scan of a
 deceased <i>S. camelus</i> juvenile (1.341 kg) with the
 respiratory system artificially inflated. This specimen was scanned at the
 UUSJMC on 10-26-2012 on a 164 slice dual energy Siemens SOMATOM Definition
 CT unit (kV 100, mA 400; slice thickness 0.6 mm). The data were filtered
 in soft tissue and lung algorithm and edge-enhanced with a high-resolution
 lung algorithm.<br>   <b>Ostrich 5:
 </b>CT scan of a deceased <i>S. camelus</i> juvenile
 (1.801 kg) with the respiratory system artificially inflated. This
 specimen was scanned at the UUSJMC on 10-26-2012 on a 164 slice dual
 energy Siemens SOMATOM Definition CT unit (kV 100, mA 400; slice thickness
 0.6 mm). The data were filtered in soft tissue and lung algorithm and
 edge-enhanced with a high-resolution lung algorithm. This individual
 specimen did not stay inflated.<br>   
 <b>Ostrich 6:</b> CT scan of a deceased <i>S.
 camelus</i> juvenile (2.58 kg) with the respiratory system
 artificially inflated. This specimen was scanned at the UUSJMC on
 10-26-2012 on a 164 slice dual energy Siemens SOMATOM Definition CT unit
 (kV 100, mA 400; slice thickness 0.6 mm). The data were filtered in soft
 tissue and lung algorithm and edge-enhanced with a high-resolution lung
 algorithm. The lungs of this specimen were stained with
 I<sub>2</sub>KI prior to scanning.<br>  
 <b>Ostrich 7:</b> CT scan of a deceased <i>S.
 camelus</i> juvenile (3.538 kg) with the respiratory system
 artificially inflated. This specimen was scanned at the UUSJMC on
 10-26-2012 on a 164 slice dual energy Siemens SOMATOM Definition CT unit
 (kV 100, mA 400; slice thickness 0.6 mm). The data were filtered in soft
 tissue and lung algorithm and edge-enhanced with a high-resolution lung
 algorithm. The intubation tube in this specimen was tied into the
 trachea.<br>   <b>Ostrich 8:</b>
 CT scan of a deceased <i>S. camelus</i> juvenile (5.715 kg)
 with the respiratory system artificially inflated. This specimen was
 scanned at the UUSJMC on 10-26-2012 on a 164 slice dual energy Siemens
 SOMATOM Definition CT unit (kV 100, mA 400; slice thickness 0.6 mm). The
 data were filtered in soft tissue and lung algorithm and edge-enhanced
 with a high-resolution lung algorithm.<br>   
 <b>Ostrich 9:</b> CT scan of a deceased <i>S.
 camelus</i> juvenile (4.471 kg) with the respiratory system
 artificially inflated. This specimen was scanned at the UUSJMC on
 10-26-2012 on a 164 slice dual energy Siemens SOMATOM Definition CT unit
 (kV 100, mA 400; slice thickness 0.6 mm). The data were filtered in soft
 tissue and lung algorithm and edge-enhanced with a high-resolution lung
 algorithm.<br>   <b>Ostrich
 10:</b> CT scan of a deceased <i>S. camelus</i> juvenile
 (6.599 kg) with the respiratory system artificially inflated. This
 specimen was scanned at the UUSJMC on 10-26-2012 on a 164 slice dual
 energy Siemens SOMATOM Definition CT unit (kV 100, mA 400; slice thickness
 0.6 mm). The data were filtered in soft tissue and lung algorithm and
 edge-enhanced with a high-resolution lung algorithm.<br>
   <b>Ostrich 11:</b> CT scan of the
 torso of a deceased <i>S. camelus</i> adult (71.3 kg) with the
 respiratory system open to atmosphere. This specimen was scanned at the
 Royal Veterinary College, London on 2-3-2014 (kV 120, mA 100; slice
 thickness 1.25 mm).<br>   <b>Alligator
 AM041315-1:</b> MicroCT scan of the torso of a deceased hatchling
 <i>Alligator mississippiensis</i> (0.0757 kg) with the lungs
 artificially inflated. This specimen was scanned on 07-01-2015 at the
 Louisiana State University School of Veterinary Medicine on a Scanco µCT
 40 (kV 55 uA 145).<br>   <b>Alligator
 15</b>: CT scan of the torso of a live and unsedated <i>A.
 mississippiensis</i> (1.7 kg) in the prone position. This specimen
 was scanned on 03-16-2012 at the University of Utah Research Park (UURP)
 on a Siemens SOMATOM Definition CT unit (kV 120, mA 200; slice thickness
 0.6 mm).<br>   <b>Alligator 9</b>:
 CT scan of the torso of a live and unsedated <i>A.
 mississippiensis</i> (1.75 kg) in the prone position. This specimen
 was scanned on 03-16-2012 at the UURP on a Siemens SOMATOM Definition CT
 unit (kV 120, mA 200; slice thickness 0.6 mm).<br>  
 <b>Alligator 739:</b> CT scan of the torso of a
 live and unsedated <i>A. mississippiensis</i> (2.8 kg) in the
 prone position. This specimen was scanned on 03-16-2012 at the UURP on a
 Siemens SOMATOM Definition CT unit (kV 120, mA 200; slice thickness 0.75
 mm).<br>   <b>Alligator 12:</b> CT
 scan of excised and artificially inflated lungs of a deceased <i>A.
 mississippiensis</i> (5.44 kg). This specimen was scanned on
 12-22-2011 at the University of Utah Hospital (UUH) on a Siemens SOMATOM
 Definition CT unit (kV 120, mA 200; slice thickness 0.6 mm). These excised
 lungs were stained with I<sub>2</sub>KI prior to
 scanning.<br>   <b>Alligator
 54</b>: CT scan of excised and artificially inflated lungs of a
 deceased <i>A. mississippiensis</i> (imputed mass of 10 kg;
 total length of 54 inches). This specimen was scanned on 02-06-2012 at the
 UUH on a Siemens SOMATOM Definition CT unit (kV 120, mA 200; slice
 thickness 0.6 mm). These excised lungs were stained with
 I<sub>2</sub>KI prior to scanning.<br>  
 <b>Alligator 11:</b> CT scan of the thorax of a
 live and unsedated <i>A. mississippiensis</i> (11 kg) in the
 prone position. This specimen was scanned on 03-12-2009 at the UUH on a
 Siemens SOMATOM Definition CT unit (kV 120, mA 200; slice thickness 0.6
 mm).<br>   <b>Alligator
 Stumpy</b>: CT scan of a live and unsedated <i>A.
 mississippiensis</i> (imputed mass of 13.4 kg) in the supine
 position. This specimen was scanned on 05-05-2013 at the UUSJMC on a
 Siemens SOMATOM Definition CT unit (kV 100, mA 400; slice thickness 0.6
 mm). This specimen is missing a forelimb.<br>  
 <b>Alligator 64:</b> CT scan of the torso of an
 <i>A. mississippiensis</i> (imputed mass of 14.5 kg; total
 length of 64 inches) in the prone position with the lungs artificially
 inflated. This specimen was scanned on 08-20-2012 at the UURP on a Siemens
 SOMATOM Definition CT unit (kV 120, mA 200; slice thickness 0.6 mm). These
 excised lungs were stained with I<sub>2</sub>KI prior to
 scanning.<br>   <b>Alligator
 81:</b> CT scan of excised and artificially inflated lungs of a
 deceased <i>A. mississippiensis</i> (imputed mass of 31.5 kg;
 total length of 81 inches). This specimen was scanned on 12-22-2011 at the
 UUH on a Siemens SOMATOM Definition CT unit (kV 120, mA 200; slice
 thickness 0.6 mm). These excised lungs were stained with
 I<sub>2</sub>KI prior to scanning.