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

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 functionally decoupled, compliant, poorly vascularized ventilatory air‐sacs. To understand the evolutionary history of the archosaurian 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 10 American alligators (Alligator mississippiensis) and 11 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 15 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.

A new Heterodontosaurus specimen elucidates the unique ventilatory macroevolution of ornithischian dinosaurs

“…This recent research shows that some presumed ‘bird-like’ respiratory features, such as unidirectional air flow, are actually plesiomorphies characterizing much larger groups ( Schachner et al, 2014 ; Farmer and Sanders, 2010 ) and highlights the diversity of ways in which multiple anatomical systems interlink to effectively ventilate the lungs. New work on the pulmonary anatomy of the ostrich ( Struthio camelus ) has demonstrated that PSP relationships with the respiratory system in extant birds may not be as straightforward as previously thought ( Schachner et al, 2021 ), and reconstructions of dinosaur lungs that directly follow a standardized avian bauplan may need to be reconsidered. Additionally, primitive features like gastralia, simple sterna, and ‘propubic’ pelves impede attempts at completely superimposing the highly derived physiology of birds onto comparatively less-specialized clades like non-avian theropods and sauropods.…”

Architecture of the bronchial tree in Cuvier's dwarf caiman (Paleosuchus palpebrosus)

“…3D surface models were segmented in Avizo 7.1 and 2020.3 (Thermo Fisher Scientific) following the methods established for extant archosaur lungs (Farmer & Sanders, 2010; Lawson et al, 2021; Sanders & Farmer, 2012; Schachner et al, 2013, 2017, 2021). For a detailed description of the segmentation methodology used, see Lawson et al (2021).…”

“…Quantitative measurements of the airways were collected from the DICOM editor and viewer OsiriX MD (http://www.osirix-viewer.com) and are included in Table S1. These measures have been established in previous work (Lawson et al, 2021; Schachner et al, 2021), and were based upon hypothesized homologous structures in other crocodilians (Farmer, 2015b; Sanders & Farmer, 2012; Schachner et al, 2013, 2021), as well as developmental work on reptiles and birds (Broman, 1939; Locy & Larsell, 1916a, 1916b). All measures were completed in the 3D MPR viewer of OsiriX.…”

“…Comparatively, the functional morphology of other crocodilian taxa has received considerably less attention with much of the research focusing instead on behavior, ecology, and systematics (Bittencourt et al, 2019; Campos et al, 2010; Campos et al, 2012). In terms of the respiratory morphology, to the best of our knowledge, only A. mississippiensis (Farmer & Sanders, 2010; Sanders & Farmer, 2012; Schachner et al, 2021) and C. niloticus (Perry, 1988; Schachner et al, 2013) have been reconstructed and described in detail in three dimensions making it difficult to understand which morphological characters relate to group wide trends within Crocodylia, and which are specific to a given crocodilian taxon. With respect to the respiratory system of caimans, Gans and Clark (Gans & Clark, 1976) conducted a seminal and thorough investigation of the ventilatory mechanics of C. crocodilus .…”

“…Through a series of descriptive models of lung architecture and pulmonary measurements, we present the detailed gross anatomy of the lungs of three hatchlings and two adults. We additionally provide a comparison between P. palpebrosus and A. mississippiensis across a limited growth series (Schachner et al, 2021) which demonstrates which aspects of the bronchial tree are constrained as the lungs increase in size. Given the related respiratory biology of both P. palpebrosus and A. mississippiensis , we predict gross lung architecture and airway size and shape to be similar across both species due to functional constraints associated with unidirectional airflow patterns and the hepatic–piston ventilation system.…”