Crucian carp. Photo credit: Goran Nilsson.

Crucian carp. Photo credit: Goran Nilsson.

At first glance, elegant crucian carp and freshwater turtles may appear to be strange bedfellows, but they share a remarkable superpower. Both animals are capable of surviving for months without oxygen, emerging apparently unscathed from icy lakes and puddles at the end of winter when the sun returns. But Sjannie Lefevre and colleagues from the University of Oslo, Norway, and the University of West Scotland, UK, weren't so sure; could the remarkably robust fish be suffering brain damage as a result of oxygen deprivation and the subsequent return of oxygen?

Intrigued by the possibility, Lefevre and colleagues went fishing in a small lake near Oslo to collect carp before exposing them to a mini-winter followed by spring in the lab by supplying them with deoxygenated water for 1 week before turning the air back on for a day. Checking for signs of cell death in the fish's brains, the team was impressed to see that the cell death rate was unaffected while no oxygen was available. However, as soon as the oxygen returned, the brain cell death rate more than doubled. And when the team checked to find out how the cells were dying, there was no evidence of the programmed form of cell death (known as apoptosis) that naturally tidies away defunct cells, suggesting that the brain cells might be dying through other, more destructive or unconventional processes. However, when the team tested for signs of cell growth 1 day after the oxygen returned, neither the fish in the oxygen-rich water nor those in the oxygen-poor water seemed to be rebuilding their brains, although Lefevre points out that recovery may occur later.

As the oxygen levels in lakes vary naturally over the seasons, the team collected fish when the lake oxygen levels were highest in summer and early autumn, and at their lowest in late autumn and winter, and checked for signs of brain cell death. Interestingly, the winter fish showed relatively low levels of brain cell death by apoptosis; however, the summer and early autumn fish were disposing of brain cells at a higher rate.

Having discovered that the fish experience serious levels of brain damage through cell death when the oxygen returns in spring, the team tested how the damage affected the fish's memory. After training small groups of the fish to navigate a maze in return for a food reward, the team plunged the fish into a brief simulated winter followed by a day of spring. Despite experiencing brain damage following the return of oxygen, the fish were able to reach the food reward at the end of the maze as fast as they had before the simulated winter; however, their memories were poor and they took more wrong turns. But when the scientists tested the ability of the brain-damaged fish to learn how to navigate the maze, they found that the animals picked up the task quickly: ‘They were able to repair any brain damage caused by anoxia/re-oxygenation’, says Lefevre.

So, crucian carp suffer brain damage when oxygen floods back into their systems at the start of spring, and memories formed before the winter suffer, but they seem to regain the ability to learn after repairing the damage. However, Lefevre points out that the same may not be true for turtles. ‘They utilise markedly different strategies to survive without oxygen’, she says, pointing out that the turtles are virtually comatose and inactive when their oxygen supply is cut off, while the carp remain active, probably leaving the fish more vulnerable to damage when the oxygen returns.

Lefevre
,
S.
,
Stecyk
,
J. A. W.
,
Torp
,
M.-K.
,
Løvold
,
L. Y.
,
Sørensen
,
C.
,
Johansen
,
I. B.
,
Stensløkken
,
K.-O.
,
Couturier
,
C. S.
,
Sloman
,
K. A.
and
Nilsson
,
G. E.
(
2017
).
Re-oxygenation after anoxia induces brain cell death and memory loss in the anoxia-tolerant crucian carp
.
J. Exp. Biol.
220
,
3883-3895
.