I have found at least one possible cause for this.
The way the image displayed is loaded was not properly closing old images.
After some time, and on a machine with plenty memory, this could cause over 10000 images to be in an open state, and at that point Windows will refuse to open more.
I am not sure what causes the frequent image reloads, but I have fixed the issue by keeping the same images open instead of re-opening them. This fix is included in canary 2.1.0.112