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Anatomy, ontogeny, and evolution of the archosaurian respiratory system: a case study on Alligator mississippiensis and Struthio camelus

Citation

Schachner, Emma et al. (2020), Anatomy, ontogeny, and evolution of the archosaurian respiratory system: a case study on Alligator mississippiensis and Struthio camelus, Dryad, Dataset, https://doi.org/10.5061/dryad.3xsj3txdh

Abstract

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.

Methods

CT scans were obtained from ten specimens of American alligator (A. mississippiensis), and eleven ostriches (S. camelus) (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 (I2KI) (four A. mississippiensis and one S. camelus). The S. camelus 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.

Usage Notes

  1. Ostrich 1: Computed tomography (CT) scan of an intact deceased Struthio camelus 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.
     
  2. Ostrich 2: CT scan of a deceased S. camelus 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.
     
  3. Ostrich 3: CT scan of a deceased S. camelus 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.
     
  4. Ostrich 4: CT scan of a deceased S. camelus 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.
     
  5. Ostrich 5: CT scan of a deceased S. camelus 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.
     
  6. Ostrich 6: CT scan of a deceased S. camelus 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 I2KI prior to scanning.
     
  7. Ostrich 7: CT scan of a deceased S. camelus 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.
     
  8. Ostrich 8: CT scan of a deceased S. camelus 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.
     
  9. Ostrich 9: CT scan of a deceased S. camelus 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.
     
  10. Ostrich 10: CT scan of a deceased S. camelus 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.
     
  11. Ostrich 11: CT scan of the torso of a deceased S. camelus 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).
     
  12. Alligator AM041315-1: MicroCT scan of the torso of a deceased hatchling Alligator mississippiensis (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).
     
  13. Alligator 15: CT scan of the torso of a live and unsedated A. mississippiensis (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).
     
  14. Alligator 9: CT scan of the torso of a live and unsedated A. mississippiensis (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).
     
  15. Alligator 739: CT scan of the torso of a live and unsedated A. mississippiensis (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).
     
  16. Alligator 12: CT scan of excised and artificially inflated lungs of a deceased A. mississippiensis (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 I2KI prior to scanning.
     
  17. Alligator 54: CT scan of excised and artificially inflated lungs of a deceased A. mississippiensis (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 I2KI prior to scanning.
     
  18. Alligator 11: CT scan of the thorax of a live and unsedated A. mississippiensis (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).
     
  19. Alligator Stumpy: CT scan of a live and unsedated A. mississippiensis (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.
     
  20. Alligator 64: CT scan of the torso of an A. mississippiensis (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 I2KI prior to scanning.
     
  21. Alligator 81: CT scan of excised and artificially inflated lungs of a deceased A. mississippiensis (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 I2KI prior to scanning.

Funding

European Research Council, Award: 695517

National Science Foundation, Award: IOS -1055080

National Science Foundation, Award: IOS-0818973