Mechanisms of what-where-when memory in black-capped chickadees (Poecile atricapillus): do chickadees remember "when"?

Integrated what-where-when memory, sometimes called 'episodic-like' memory, has been shown to occur in a number of animals, including food-storing birds and rodents. It is not always clear in these studies, however, what aspect of "when" is remembered. We examined memory for what, where, and when in black-capped chickadees Poecile atricapillus in a procedure designed to dissociate memory for elapsed time (how long ago) from memory for a point in time, the sense of "when" implied in most discussions of episodic or episodic-like memory. Chickadees searched for food in multiple trials that each involved a two-phase procedure. In Phase 1, birds found preferred mealworms in half the sites on one side of an aviary and less preferred sunflower seeds in half the sites on the other side of the aviary. In Phase 2, following a retention interval, birds searched in the aviary with fresh sunflower seeds placed in the sites that held seeds in Phase 1 but either fresh or degraded mealworms in the sites that held mealworms in Phase 1. Whether a site held fresh or degraded worms depended on either when during the day Phase 1 had occurred (Group When), how long ago Phase 1 had occurred (Group HLA), or both (Group When + HLA). Chickadees in all three groups were able to discriminate where and when palatable worms were to be found, but there were temporal limitations on the use of HLA and When + HLA cues that were not found for the use of When cues.