Breathing through skin in a newborn mammal

Abstract

The exchange of oxygen and carbon dioxide through the skin does not occur in most mammals because they have high metabolic rates and diffusion through the skin is poor. But we have found that in the Julia Creek dunnart (Sminthopsis douglasi), a marsupial mouse with one of the smallest newborns of any mammal, gas exchange through the skin is the predominant form of O₂ and CO₂ transfer in the first days after birth.

Main

These small newborns have lower O₂ consumption than non-marsupial species¹, and thermoregulation is not a problem because they develop in the thermoneutral environment of the maternal pouch. Further, because they are delivered at a very early stage of development², the skin, which is hairless and rich in blood, provides a much smaller barrier to gas diffusion than in most newborn mammals.

A 70-kg human athlete can reach a level of maximal oxygen consumption ($V_{{\text{O}}_{\text{2}}}$) of up to 65 ml kg^-1 min^-1 (4,550 ml min^-1). Such high values are possible because of a very large surface area for gas exchange in the lungs, estimated at about 70 m² (ref. 3). In an adult human, the body surface could therefore never replace the lungs as a site of gas exchange because its total area is only about 2% of the minimal surface required. If the lungs were designed optimally⁴, the ratio between the pulmonary gas-exchange surface and O₂ flux would be the minimum necessary for gas exchange. In humans, this value would be 70 m² per 4,550 ml min^-1, or about 150 cm² per ml O₂ min^-1.

The Julia Creek dunnart is a small dasyurid marsupial from Australia⁵. After a gestation lasting about 13 days, the newborn is about 4 mm long and weighs around 17 mg, so it is one of the smallest newborn mammals known². At birth, the skeleton is entirely cartilaginous and the internal organs are visible through the transparent skin. The lungs are represented by a small number of approximately spherical air sacs ( Fig. 1). In the newborn dunnart and in individuals up to 21 days old, $V_{{\text{O}}_{\text{2}}}$ averaged 18 ml kg^-1 min^-1, and the body surface area is estimated at about 7 mm². The ratio between body surface area and $V_{{\text{O}}_{\text{2}}}$ is therefore about 220 cm² per ml O₂min^-1, above the minimum value necessary for the skin to be an important site of gas exchange.

Figure 1: Pouch young of Sminthopsis douglasi at one day old.

The lungs are visible as air sacs on each side of the heart. Despite the presence of ribs, no respiratory thoracic movements can be detected. Scale bar, 1 mm.

We measured separately, but simultaneously, the gaseous metabolism of lungs and skin in 22 pouch young from five litters during the first three weeks after birth. We sealed a mask made from a short length of polyethylene tube to the face of the animal, covering both mouth and nostrils, using a removable dental polyether material. The low mobility of the newborns ensured that the seal was maintained. The tube passed through a thin rubber stopper placed in the centre of a moist cylindrical chamber of volume 0.5-2 ml, completely separating the chamber into two compartments, one containing the animal and the other communicating with the airways.

A small quantity of air was injected into one compartment, and the absence of pressure transmission to the other indicated complete separation. The chamber was maintained at pouch temperature (36 °C) by a water bath. After temperature and humidity equilibration, the compartments were sealed for 5-15 min, depending on the animal's age. The compartments were then flushed with a constant airflow of 20 ml min^-1 and the gas was forced through a drying column before O₂ and CO₂ concentration were determined.

$V_{{\text{O}}_{\text{2}}}$and $V_{{\text{CO}}_{\text{2}}}$(CO₂ production) were calculated from the time integral of the gas concentration curves⁶, multiplied by the flow and the time the chamber was sealed. At all ages, the skin's contribution to gas exchange was very marked. In the youngest animals, with body weight below 100 mg, gas exchange through the skin exceeded that through the lungs (Fig. 2). In the oldest individuals studied, which were 20 to 21 days of age with a body weight of about 290 mg, skin exchange was about one-third that of the lungs.

Figure 2: Ratio between skin and pulmonary gas exchange in the pouch young of S. douglasi.

Values refer to oxygen consumption ($V_{{\text{O}}_{\text{2}}}$, filled symbols) and carbon dioxide production ($V_{{\text{CO}}_{\text{2}}}$, open symbols), measured at an ambient temperature of 36 °C. The broken line indicates equal contributions of lungs and skin to total gas exchange.

In animals two to three days old, spontaneous body movements did not appreciably expand the air sacs, and resulted in minimal changes in lung volume. These were calculated from the displacement of a drop of soapy solution in a microtube directly connected to the polyethylene tube sealed to the face of the animal, magnified by a microscope and displayed on a television screen by a video camera. These observations suggest that, in the Julia Creek dunnart during the early postnatal phases, pulmonary convection is highly inefficient. Sustaining oxygen demands through the skin allows these very small animals to be born before the respiratory apparatus is fully functional.