Abstract
Marsupials are born with immature lungs when compared to eutherian mammals and rely, to various extents, on cutaneous gas exchange in order to meet metabolic requirements. Indeed, the fat-tailed dunnart is born with lungs in the canalicular stage of development and relies almost entirely on the skin for gas exchange at birth; consequently undergoing the majority of lung development in air. Plane radiographs and computed tomography data sets were acquired using phase contrast imaging with a synchrotron radiation source for two marsupial species, the fat-tailed dunnart and the larger tammar wallaby, during the first weeks of postnatal life. Phase contrast imaging revealed that only two lung sacs contain air after the first hour of life in the fat-tailed dunnart. While the lung of the tammar wallaby was comparatively more developed, both species demonstrated massive increases in air sac number and architectural complexity during the postnatal period. In addition, both the tammar wallaby and fat-tailed dunnart had lower lung volumes and parenchymal surface areas than were expected from morphometrically determined allometric equations relating these variables to body mass during the neonatal period. However, lung volume is predicted to scale with mass as expected after the neonatal marsupial reaches a body mass of ∼1 g and no longer relies on the skin for gas exchange. Decreased lung volume in the marsupial neonate further supports the maxim that cutaneous gas exchange occurs in the marsupial neonate because the respiratory apparatus is not yet capable of meeting the gas exchange requirements of the newborn.
Highlights
Marsupials are born with structurally immature lungs by eutherian standards
This study aimed to explore lung development in the tammar wallaby and fat-tailed dunnart during the first weeks of life using phase contrast imaging with a synchrotron radiation source
The air sacs were no longer large circular sacs, and lung volume and surface area were improved through extensive increases in air sac number, as well as architectural complexity
Summary
Marsupials are born with structurally immature lungs by eutherian standards. The fat-tailed dunnart (Sminthopsis crassicaudata) [1] and quokka wallaby (Setonix brachyurus) [2] are born with lungs at the canalicular stage of development, though more commonly marsupials, including the tammar wallaby (Macropus eugenii), are born with lungs at the saccular stage [3]. The lung of the newborn tammar wallaby contains abundant surfactant [4,5] and is largely functional as a gas exchanger, contributing 60–70% of the gas exchange required to meet the total metabolic demands of the newborn [6]. The remaining 30– 40% of gas exchange is cutaneous, with the skin continuing to play a role in meeting metabolic demands until four days postpartum (P4) in the tammar wallaby [6]. In the fat-tailed dunnart the skin contributes to gaseous exchange until P40 [1], enabled in part by the large surface area to volume ratio associated with a very small body size, low metabolic rate, possible neural and/or mechanical constraints to pulmonary ventilation and the presence of cardiac shunts in these immature newborns [7]
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