I recall in the updates notes of a release a few releases back mentioned a new ~400 item-per-collection limit. I bet this is related.
You are correct.
"Limit for number of items in a collection
In order to optimize performance, a new limit of 450 items (articles, banners, and collections) per collection is now in place."
From: New features in 2015.8 (December 18, 2015)