It just didn't make sense, going to the page everything would work as expected but refreshing the very same page caused it to fail - it didn't matter if it was the start up page of the visual studio project or not. In one of the many attempts to isolate / identify the problem I cleared out the browser cache. Amusingly this now broke the entire site - the error occurred every time the page was viewed.
............It was at this point that I noticed I'd accidently moved the projects localised copy of jQuery. The requests to the page that had worked originally had been using a browser cached copy of the file - it was the refresh of the page that was acting correctly.