10.5061/DRYAD.3XSJ3TXDH
Schachner, Emma
0000-0002-8636-925X
Louisiana State University Health Sciences Center New Orleans
Hedrick, Brandon
Louisiana State University Health Sciences Center New Orleans
Richbourg, Heather
0000-0002-4081-1073
University of California, San Francisco
Hutchinson, John
0000-0002-6767-7038
University of London
Farmer, CG
University of Utah
Anatomy, ontogeny, and evolution of the archosaurian respiratory system: a
case study on Alligator mississippiensis and Struthio camelus
Dryad
dataset
2020
European Research Council
https://ror.org/0472cxd90
695517
National Science Foundation
https://ror.org/021nxhr62
IOS -1055080
National Science Foundation
https://ror.org/021nxhr62
IOS-0818973
2020-08-16T00:00:00Z
2020-08-16T00:00:00Z
en
5882620011 bytes
4
CC0 1.0 Universal (CC0 1.0) Public Domain Dedication
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.
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.
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. 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. 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. 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. 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. 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. 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. 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. 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. 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.
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). 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). 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). 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). 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). 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.
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. 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). 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. 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. 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.