Cyprinodon nevadensis mionectes from Ash Meadows: Photo credit: Frank van Breukelen.

Cyprinodon nevadensis mionectes from Ash Meadows: Photo credit: Frank van Breukelen.

Deep in a warm pool in a limestone cavern in the Mojave Desert lives one of the rarest species on earth: the Devils Hole pupfish (Cyprinodon diabolis). With a current population of just 131 adults, the race is on to secure the fish's future. ‘One possible cause for the small population size of C. diabolis is limited food availability’, says Frank van Breukelen from the University of Nevada Las Vegas, USA. Realising that the dark conditions dramatically limit the amount of food that grows in the cavern to support the fish, van Breukelen and his colleague, Stanley Hillyard, were curious to know how many pupfish the restricted ecosystem could sustain. However, before they could do the calculation, the duo needed to measure the scarce fish's metabolic rate. As the native Devils Hole pupfish population is too endangered to study directly, van Breukelen and Hillyard measured the metabolic rate of a refuge population of the fish that had been established as an insurance policy should the population ever be wiped out. But when they performed the measurement, the duo stumbled across an unexpected paradox.

Recording the fish's oxygen consumption at temperatures ranging from 25 to 38°C, Matt Heuton found that they consumed oxygen at a stable rate of around 300 μl h−1 when they came from a population that had been raised at 28°C. However, when Heuton measured the oxygen consumption rate of fish raised at 33°C – the temperature in the Devils Hole spring – something went wrong. The fish appeared to stop consuming oxygen. ‘My initial reaction was that there was a malfunction of the electrode’, laughs van Breukelen. However, after testing 295 animals, van Breukelen and Hillyard had to concede that the phenomenon was real. The fish were somehow switching from aerobic metabolism to anaerobic metabolism, which was perplexing as anaerobic metabolism is nowhere near as effective as aerobic metabolism – only yielding 1/15 the amount of ATP per glucose molecule generated by aerobic metabolism. Why were the fish indulging in such a profligate practice?

Intrigued, the team tested whether the phenomenon was the result of the refuge C. diabolis population breeding with another closely related species, Cyprinodon nevadensis mionectes. van Breukelen explains that it has been suggested that interbreeding with other pupfish could have compromised the function of the mitochondria that generate ATP. However, when the team measured the oxygen consumption patterns of the two species, they both performed paradoxical anaerobism, so there was no mitochondrial disruption. And when the team tested whether C. diabolis were switching to paradoxical anaerobism because they had depressed metabolism, they found that the fish were still wafting their gill covers to take in oxygen, so they weren't depressing their metabolism. Finally, the team checked whether C. diabolis were switching to paradoxical anaerobism because there simply was not enough oxygen to sustain aerobic metabolism in the warm conditions. However, even that theory did not hold water.

‘We were going nuts trying to figure out what triggers paradoxical anaerobism’, admits van Breukelen, until he and Heuton embarked on an animated brain-storming session one night. It occurred to them that the fish may be switching to paradoxical anaerobism to avoid the toxic side-effects of aerobic metabolism, producing ethanol instead. They knew that the 33°C-acclimated fish naturally produced high levels of ethanol – 7.3 times more than the fish from cooler water: could the ethanol be switching off aerobic energy production and stalling oxygen consumption? ‘I said, “Let's get the fish drunk”’, recalls van Breukelen. And when the team added ethanol to the fish's water, even the fish that were adapted to cooler water switched to paradoxical anaerobism. So Devils Hole pupfish switch off aerobic metabolism to avoid the toxic side-effect of an aerobic lifestyle, despite the expense.

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