Fish gills are truly remarkable; breathing, salt balance regulation and waste disposal are all in a day's work for this versatile organ. These competing demands present some interesting challenges, says Steve Perry of the University of Ottawa, Canada. Large gills are good for breathing and flushing out toxins like ammonia, but not so good for retaining useful things like salt – a big problem for freshwater fish. ‘In cold water, crucian carp and goldfish reduce salt loss by physically covering their gills with a structure called an interlamellar cell mass,’ says Perry. But how can ‘cold’ fish continue to pump out toxins when their gills are covered up (p. 3656)?

To find out, Perry and his team first had to show that ‘cold’ fish with covered gills find it harder to expel ammonia than ‘warm’ fish. But when they measured ammonia levels in the tanks of goldfish housed at 7°C and 25°C, instead of pumping out ammonia at a slower rate, the team were surprised to find that the ‘cold’ fish pumped out ammonia at a similar rate to the ‘warm’ fish. However, knowing that acclimation temperature can affect ammonia production, Perry decided to standardise the amount of ammonia that the fish had in their bodies. Sure enough, when the team injected goldfish with large quantities of ammonia, ‘cold’ fish only managed to pump out 40% of the injected load within 3 hours, while ‘warm’ fish expelled 90%.

‘This was consistent with our idea that fish with covered gills find it harder to expel ammonia than fish with uncovered gills,’ says Perry, ‘but the better performance of the “warm” fish could also be explained by their faster breathing and higher blood flow compared with fish in cold water.’ To test this, the team chased ‘cold’ fish around the tank with a net until they were breathing as fast as ‘warm’ fish, and then measured ammonia levels in the tanks of exercised and non-exercised fish. ‘Lo and behold, we were able to turn a 7°C fish into a 25°C fish!’ says Perry. So ‘cold’ fish can avoid becoming poisoned just by breathing faster – but was this the complete story?

The team were still troubled by the fact that they were comparing fish at different temperatures, as ‘warm’ fish eat more, breathe faster and have higher blood flow, all of which can affect ammonia excretion. So the team devised a way to take temperature out of the equation; they compared ‘cold’ fish with covered and uncovered gills. Starving some fish of oxygen so that they uncovered their gills, the team were delighted to discover that these fish pumped out ammonia much more quickly than fish with covered gills. ‘This showed clearly that the interlamellar cell mass does impede ammonia excretion,’ says Perry. ‘We had now come full circle. When “cold” fish have covered gills, how do they manage to excrete ammonia as well as “warm” fish?’

The team knew that ammonia moves through channels called Rhesus proteins, so they decided to take a closer look at Rhesus protein expression and distribution in ‘cold’ and ‘warm’ fish. While Rhesus protein expression didn't change with temperature, the team found that Rhesus proteins were redistributed to gill edges in ‘cold’ fish, allowing them to shuttle out ammonia even when their gills are covered. Perry concludes that, when the temperature drops, fish can remodel their gills to cut salt loss and still manage to avoid poisoning simply by relocating their ammonia transporting proteins.

S. F.
M. H.
The consequences of reversible gill remodelling on ammonia excretion in goldfish (Carassius auratus)
J. Exp. Biol.