The solutions aquatic insects have evolved for underwater air breathing range from simple siphons or snorkels to tracheal gills and plastrons. An in-between solution adopted mostly by beetles and bugs is to collect and hold an air bubble over their spiracles while diving. At depth the increased hydrostatic pressure will increase the bubble's oxygen and nitrogen partial pressures (PO2 and PN2) and O2 and N2 will diffuse into the water. Simultaneously, insect O2 consumption (
) causes the bubble PO2 to drop below that of the water. Now O2 diffuses from the water back into the bubble. At this point the bubble becomes a gill. However, bubble PN2 will remain high and N2 dissolves continually into the water, reducing the bubble's volume. This system is called a compressible gas gill. The gas gill continues to shrink and eventually must be ‘refilled’ at the water surface.
Two competing models aimed to theoretically describe compressible gas gill function. First, the ‘shrinking area’ gas gill model states that decreasing volume would also cause gill surface area to decrease. The shrinking area reduces the ratio of gill O2 uptake to insect oxygen consumption until increased hypoxia in the gill ends the dive.
The ‘constant area’ gas gill model states that while gas gill volume decreases, the gill surface area remains constant. When a bug collects a bubble, which forms the compressible gill, the air adheres to the entire lower surface of the bug, from below the head to the outer edges and tip of the abdomen. The bubble forms a thin layer over the entire surface of the insect's underside, and as the bubble's volume decreases the air layer becomes thinner, but the surface area remains essentially unchanged. This sustains constant O2 diffusion into the gill, stabilizing internal gill oxygen partial pressure until the declining gill height reaches a minimal limit and the insects must return to the surface for more air. This results in a theoretical oxygen gain of 8: that is, 7 times the original bubble's O2 content diffused inward, extending dive time 8-fold.
Both models are mathematically consistent but which holds true? An empirical test was required to resolve the stalemate.
Philip Matthews and Roger Seymour from the University of Adelaide did just that. Using the water boatman, Agraptacorixa eurynome, in a series of elegantly conceived experiments, they checked that the bubble adhered to the underside of the bug and measured the PO2, volume and area of the bug's gas gill, the bug's oxygen consumption and critical PO2, and gill ventilation through leg movements.
Seeing that the bubble did adhere to the bug's underside, the team found that the initial gill PO2 dropped rapidly from 21 kPa (atmospheric PO2). However, the interaction between bug oxygen consumption and O2 diffusion into the gill allowed gill PO2 to stabilize at ∼3.23 kPa as long as gill ventilation was maintained. With minimal leg movement gill PO2 reached ∼1 kPa, while it stabilized at 5 kPa during swimming. The bug's critical PO2 (the PO2 required to maintain resting oxygen consumption against tracheal resistance) was 2.1 kPa. Finally, the authors calculated that the gill factor (gill oxygen gain) is 7.5, allowing a dive time of 42–78 min before the flattened gill needs ‘refilling’.
The authors' empirical test results very closely approximated the ‘constant area’ gas gill model. An interesting aside to the understanding of the functioning of compressible gas gills is that the bugs can regulate gill PO2 through increased or decreased leg gill ventilation, thus manipulating gill PO2 to supply oxygen at physiologically useful rates.
