Many fish hatch with stubby gills that have little surface area for oxygen uptake. Instead, most oxygen comes and goes across the skin over the first few weeks of development. Regardless of whether this process of gas exchange happens via the gills or the skin, it all comes down the boundary layer, a thin coat of stagnant water that envelops the larvae as water flows around it. A thick boundary layer makes it more difficult for gases to move into (or out of) the larvae.
Fully formed gills have a boundary layer too, but the rhythmic opening and closing of the fish's mouth keeps it from getting too thick. The notion that larvae may also ventilate their skin, by swimming or fanning their pectoral fins, has intrigued physiologists for decades. However, no direct evidence linked fin movement with managing the oxygen boundary layer, oxygen uptake or metabolism in larvae. In a new paper, Alex Zimmer, Milica Mandic and colleagues from the University of Ottawa, Canada, tested the idea that pectoral fin movement plays a role in oxygen uptake in larval zebrafish and rainbow trout.
First, the researchers measured how quickly zebrafish larvae flapped their gills and fins as the oxygen availability was reduced to produce hypoxic conditions. Just like adult fish, the larvae of all ages (4–21 days post-hatching, dph) ventilated their gills faster during hypoxia. As the larvae developed, their fin-beating behaviour changed: young (4 dph) larvae furiously fanned their fins when the oxygen levels were low, whereas older (15 dph) larvae waved their fins less urgently. The oldest larvae (21 dph) barely beat their fins at all. Most intriguingly, the larvae ceased beating their fins frantically just as the gills took over as the main site of gas exchange.
Intrigued, the team measured oxygen levels along the skin surface of trout larvae with a precise oxygen sensor. They found that regions near the pectoral fins, like the front of the yolk sac, were more oxygen rich than areas towards the tail. And when the scientists anaesthetised the larvae to briefly halt fin and gill ventilation, the oxygen concentration in the water near the fins decreased by as much as 50%, demonstrating that fin beating was responsible for the high oxygen levels in these body regions. What's interesting is that surgically removing the pectoral fins, but leaving the gills intact, had comparable effects on the distribution of oxygen along the bodies of the larvae to complete anaesthesia. Pectoral fins have a significant role in stirring up the oxygen boundary layer and maintaining high oxygen levels at the skin surface.
To definitively link fin beating with oxygen uptake and metabolism, the team compared whole-animal oxygen consumption rates in intact and fin-clipped larvae exposed to hypoxia. The oxygen consumption rates were markedly lower in the fin-clipped trout larvae, supporting the notion that fanning supports oxygen uptake in hypoxia. Interestingly, fin-clipped zebrafish larvae maintained their oxygen consumption rates despite low water oxygen levels, hinting that the higher activity levels or greater hypoxia tolerance of zebrafish larvae may mitigate the effects of pectoral fin removal on oxygen uptake.
Just like adult gills, the skin of larval fish is only as good as its (lack of) boundary layer. These observations are the first direct evidence for the respiratory role of pectoral fins, which facilitate oxygen uptake by dissipating the boundary layer in at least one species. For young larvae, oxygen uptake is more than skin deep.
