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It seems to be a bug that appears when collections have large numbers of books.
I reported it long ago (2 years ago or more) and -- like any number of other bugs -- it hasn't been fixed. I don't bother with collections now. As a work-around, Calibre has a feature called 'catalog' which creates a mobi file listing all books on the device by various categories like author, genre, etc. It's not a complete solution but it serves my needs. (btw, if you choose this solution, use mobi output format instead of azw3).
FWIW, Kobo doesn't have this problem.
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