Development of the skin in the eastern quoll (Dasyurus viverrinus) with focus on cutaneous gas exchange in the early postnatal period.

A morphological and morphometric study of the skin development in the eastern quoll (Dasyurus viverrinus) was conducted to follow the transition from cutaneous to pulmonary gas exchange in this extremely immature marsupial species. Additionally, the development of the cardiac and respiratory system was followed, to evaluate the systemic prerequisites allowing for cutaneous respiration. The skin in the newborn D. viverrinus was very thin (36 ± 3 µm) and undifferentiated (no hair follicles, no sebaceous and perspiratory glands). Numerous superficial cutaneous capillaries were encountered, closely associated with the epidermis, allowing for gaseous exchange. The capillary volume density was highest in the neonate (0.33 ± 0.04) and decreased markedly during the first 4 days (0.06 ± 0.01). In the same time period, the skin diffusion barrier increased from 9 ± 1 µm to 44 ± 6 µm. From this age on the skin development was characterized by thickening of the different cutaneous layers, formation of hair follicles (day 55) and the occurrence of subcutaneous fat (day 19). The heart of the neonate D. viverrinus had incomplete interatrial, inter-ventricular, and aortico-pulmonary septa, allowing for the possibility that oxygenated blood from the skin mixes with that of the systemic circulation. The fast-structural changes in the systemic circulations (closing all shunts) in the early postnatal period (3 days) necessitate the transition from cutaneous to pulmonary respiration despite the immaturity of the lungs. At this time, the lung was still at the canalicular stage of lung development, but had to be mature enough to meet the respiratory needs of the growing organism. The morphometric results for the skin development of D. viverrinus suggest that cutaneous respiration is most pronounced in neonates and decreases rapidly during the first 3 days of postnatal life. After this time a functional transition of the skin from cutaneous respiration to insulation and protection of the body takes place.

Skin structure in newborn marsupials with focus on cutaneous gas exchange.

A morphological and morphometric study of the skin of a variety of newborn marsupials (Dasyurus viverrinus, Monodelphis domestica, Trichosurus vulpecula, Isoodon obesulus, Perameles nasuta, Phascolarctos cinereus, Potorous tridactylus, Petrogale penicillata, Thylogale thetidi, Macropus dorsalis) and of a monotreme hatchling (Ornithorhynchus anatinus) was undertaken to assess the possibility of cutaneous gas exchange. Additionally, the lungs of some of these species were investigated to assess its structural degree at birth. The skin in the different newborn marsupials and the monotreme hatchling had a similar structure (no hair follicles and no sebaceous or perspiratory glands) and was in all cases less developed than the skin of altricial eutherians. The thickness of the entire skin (36-186 µm) and its different layers, epidermis (6-29 µm) and dermis (29-171 µm) varied among the marsupial species and reflected the differences in size and developmental degree of the neonates. In the skin of all marsupial neonates and the monotreme hatchling, numerous superficial cutaneous capillaries were encountered, some closely associated with the epidermis, indicating the possibility that the skin participated in gaseous exchange. The skin of the newborn D. viverrinus had the highest capillary volume density and shortest skin diffusion barrier of all marsupial neonates, suggesting that skin gas exchange in the dasyurid neonate might be the most pronounced. A graduation of the skin capillary density among the marsupial neonates inversely followed the respective lung structure and general developmental degree of the neonates.

Evolution and development of gas exchange structures in Mammalia: the placenta and the lung.

Appropriate oxygen supply is crucial for organisms. Here we examine the evolution of structures associated with the delivery of oxygen in the pre- and postnatal phases in mammals. There is an enormous structural and functional variability in the placenta that has facilitated the evolution of specialized reproductive strategies, such as precociality. In particular the cell layers separating fetal and maternal blood differ markedly: a non-invasive epitheliochorial placenta, which increases the diffusion distance, represents a derived state in ungulates. Rodents and their relatives have an invasive haemochorial placental type as optimum for the diffusion distance. In contrast, lung development is highly conserved and differences in the lungs of neonates can be explained by different developmental rates. Monotremes and marsupials have altricial stages with lungs at the early saccular phase, whereas newborn eutherians have lungs at the late saccular or alveolar phase. In conclusion, the evolution of exchange structures in the pre- and postnatal periods does not follow similar principles.