High Experience Levels Delay Recruitment but Promote Simultaneous Time-Memories in Honey Bee Foragers

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Honey bee (Apis mellifera) foragers can remember both the location and time of day food is collected and, even in the absence of a reward, reconnoiter the food source at the appropriate time on subsequent days. This spatiotemporal memory (time-memory) is linked to the circadian clock and enables foragers to synchronize their behavior with floral nectar secretion rhythms, thus eliminating the need to rediscover productive food sources each day. Here, we asked whether the establishment of one time-memory influences the formation of another time-memory at the same time of day. In other words, can two time-place memories with the same ‘time-stamp’ coexist? We simultaneously trained two groups of foragers from a single hive to two separate feeders at the same restricted time of day. After 5 days of training, one feeder was shut off. The second feeder continued being productive 4 more days. Our results showed that (1) foragers with high experience levels at the first source were significantly more likely than low-experience foragers to maintain fidelity to their original source and resist recruitment to the alternative source, (2) nearly one-third of foragers demonstrated multiple, overlapping time-memories by visiting both feeders at the correct time and (3) significantly more high-experience than low-experience foragers exhibited this multitasking behavior. The ability to maintain and act upon two different, yet contemporaneous, time-memories gives the forager bee a previously unknown level of versatility in attending to multiple food sources. These findings have major implications for understanding the formation and management of circadian spatiotemporal memories.