Classical experiments on honey bee time-memory showed that foragers trained to collect food at a fixed time of day return the following day with remarkable time-accuracy. Previous field experiments revealed that not all foragers return to a food source on unrewarded test days. Rather, there exist 2 subgroups: “persistent” foragers reconnoiter the source; “reticent” foragers wait in the hive for confirmation of source availability. To examine how these foragers contribute to a colony’s ability to reallocate foragers across sources with rapidly changing availabilities, foragers were trained to collect sucrose during a restricted window for several days and observed over 3 days throughout which the feeder was empty. In 2 separate trials, activity monitoring revealed a high level of activity apparently directed at other food sources. This “extracurricular” activity showed extensive temporal overlap with visits to the feeder, indicating that honey bees can manage at least 2 different overlapping time memories.

Honey bee foragers form time memories that enable them to match their foraging activity to the time of day when a particular food source is most productive. Persistent foragers show food-anticipatory activity by making reconnaissance flights to the previously productive food source and may continue to inspect it for several days. In contrast, reticent foragers do not investigate the source but wait for confirmation from returning persistent foragers. To determine how persistent and reticent foragers might contribute to the colony's ability to rapidly reallocate foragers among sources, we trained foragers to collect sucrose from a feeder at a restricted time of day for several days and then observed their behavior for three consecutive days during which the feeder was empty. In two separate trials, video monitoring of the hive entrance during unrewarded test days in parallel with observing reconnaissance visits to the feeder revealed a high level of activity, in both persistent and reticent foragers, thought to be directed at other food sources. This 'extracurricular' activity showed a high degree of temporal overlap with reconnaissance visits to the feeder. In some cases, inspection flights to the unrewarded feeder were made within the same trip to an extracurricular source, indicating that honey bees have the ability to manage at least two different time memories despite coincidence with respect to time of day. The results have major implications for understanding flower fidelity throughout the day, flower constancy within individual foraging excursions, and the sophisticated cognitive management of spatiotemporal memories in honey bees.

Honey bee foragers form time memories that enable them to match their foraging activity to the time of day when a particular food source is most productive. Persistent foragers show food-anticipatory activity by making reconnaissance flights to the previously productive food source and may continue to inspect it for several days. In contrast, reticent foragers do not investigate the source but wait for confirmation from returning persistent foragers. To determine how persistent and reticent foragers might contribute to the colony's ability to rapidly reallocate foragers among sources, we trained foragers to collect sucrose from a feeder at a restricted time of day for several days and then observed their behavior for three consecutive days during which the feeder was empty. In two separate trials, video monitoring of the hive entrance during unrewarded test days in parallel with observing reconnaissance visits to the feeder revealed a high level of activity, in both persistent and reticent foragers, thought to be directed at other food sources. This 'extracurricular' activity showed a high degree of temporal overlap with reconnaissance visits to the feeder. In some cases, inspection flights to the unrewarded feeder were made within the same trip to an extracurricular source, indicating that honey bees have the ability to manage at least two different time memories despite coincidence with respect to time of day. The results have major implications for understanding flower fidelity throughout the day, flower constancy within individual foraging excursions, and the sophisticated cognitive management of spatiotemporal memories in honey bees.

Abstract: The honey bee time memory enables foragers to return to a profitable food source in anticipation of the time of day at which they previously collected food from that source. The time memory thus allows foragers to quickly resume exploiting a source after interruption, at the appropriate time of day, without the costs associated with having to rediscover it. A portion of a foraging group (the persistent foragers) will reconnoiter a previously profitable source and may do so for several days. The remaining bees (the reticent foragers) await confirmation of availability before revisiting the source. Recent work has shown that both persistent and reticent bees make extracurricular flights to alternative sources when one food source ceases being productive. Little else, however, is known about reticent foragers. In the present study, we determined that reticent bees congregate near the hive entrance in anticipation of the learned foraging time as do persistent foragers. We then confirmed that the food-anticipatory clustering takes place on the waggle dance floor, as suspected, but also found differences in the number of days that persistent and reticent foragers continue clustering. Finally, we found that persistent foragers had significantly more rewards per day at the source than did reticent foragers, supporting the hypothesis that experience at a food source influences a forager’s decision to become either persistent or reticent. Our findings demonstrate that persistence and reticence are not immutable characteristics of foragers themselves but rather strategies they employ toward different food sources. Significance statement: Much has been learned in recent years about the honey bee time memory and foraging behavior. Receiving scant attention, however, is the phenomenon of forager bees gathering near the hive entrance, anticipating the time of day when previously productive food sources become available. We show that both persistent and reticent bees (foragers that do and do not investigate the source, respectively) congregate on the waggle dance floor at the appropriate time of day, but, in the absence of food at the source, persistent bees continue to show this behavior a day or two longer than reticent bees do. We also show that experience with the source influences the decision to become persistent or reticent. Our results reveal how foraging experience influences the individual bee’s decision making, thereby providing insights into how foragers are reallocated efficiently among different resources in the environment.

Forager honey bees exhibit a robust time memory, based on an endogenous circadian clock, enabling them to schedule their flights to coincide with the nectar presentation of known food sources. They retain this time memory for several consecutive days even in the absence of nectar rewards. Recent work has identified 2 classes of forager: "persistent" foragers that reconnoiter a known food source to ascertain its status and "reticent" foragers that apparently wait in the hive for a waggle dance confirming source availability. Surprisingly, a foraging group contains 40-90% persistent foragers, depending on experience at the source. What is the benefit in sending so many foragers to investigate a source when only a few foragers are required to reactivate the entire group? We used an agent-based software model to test the energetics underlying several different ratios of persistent and reticent individuals in the foraging group while varying 6 ecological factors: forager group size, source distance, source sucrose concentration, source availability in hours, number of days the source is known to the colony, and the rate at which new unemployed foragers appear on the dance floor. Our model demonstrates 2 primary explanations. First, a large number of persistent foragers are needed to ensure that at least some foragers will reconnoiter their source early in its availability, thus enabling the group to effectively exploit the source. Second, the cost of a reconnaissance flight is negligible compared with even a single successful foraging trip.

Classical experiments demonstrated that honey bee foragers trained to collect food at virtually any time of day will return to that food source on subsequent days with a remarkable degree of temporal accuracy. This versatile time-memory, based on an endogenous circadian clock, presumably enables foragers to schedule their reconnaissance flights to best take advantage of the daily rhythms of nectar and pollen availability in different species of flowers. It is commonly believed that the time-memory rapidly extinguishes if not reinforced daily, thus enabling foragers to switch quickly from relatively poor sources to more productive ones. On the other hand, it is also commonly thought that extinction of the time-memory is slow enough to permit foragers to 'remember' the food source over a day or two of bad weather. What exactly is the time-course of time-memory extinction? In a series of field experiments, we determined that the level of food-anticipatory activity (FAA) directed at a food source is not rapidly extinguished and, furthermore, the time-course of extinction is dependent upon the amount of experience accumulated by the forager at that source. We also found that FAA is prolonged in response to inclement weather, indicating that time-memory extinction is not a simple decay function but is responsive to environmental changes. These results provide insights into the adaptability of FAA under natural conditions.

Forager honey bees can associate the time of day with the presence of food at locations outside the hive. It is thought that this time-memory enables the bee to make a spatio-temporal match between its behavior and floral nectar secretion rhythms. Despite a long tradition of research, the mechanisms by which the time-memory becomes established are unknown. We investigated the influences of two experiential factors on the acquisition of time-memory: (1) the number of collecting visits made by the forager within a feeding bout during a restricted time of day and (2) the number of days of exposure to the restricted feeding time. Our results indicate that these two factors control different processes. The number of days of experience influences the temporal accuracy of reconnaissance behavior to the food source. The cumulative number of collecting visits within the feeding bouts has no apparent effect on time-accuracy but, instead, determines the probability of exhibiting food-anticipatory behavior and, if that overt behavior is performed, the intensity of its expression.

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.

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Made available in DSpace on 2014-12-17T15:36:59Z (GMT). No. of bitstreams: 1 BrenoTSC_DISSERT.pdf: 3046533 bytes, checksum: 8a10fc9b8e091299347bfd22993003fe (MD5) Previous issue date: 2010-08-10 / Conselho Nacional de Desenvolvimento Cient?fico e Tecnol?gico / Food is essential for the survival of all animals. Its temporal availability is an important enviromental cue for the behavioral and physiological organization throughout the 24 hours of day in different species. Rats and mice, for example, show increased locomotion in the hours before food availability when it is presented in a recurrent manner, a behavior named foodanticipatory activity. Several lines of evidence indicate that this anticipation is mediated by a circadian oscillator. In this work, based on the hypothesis that pre- or post-ingestive humoral signals are involved in the entrainment process, we tested whether the daily intake of glucose is sufficient to induce anticipatory activity in rats. The rhythms of motor activity and central temperature were recorded in animals undergoing 10 days of temporal glucose (solution at 50%) or chow restriction in light-dark (LD) and constant darkness (DD). Animals under temporal glucose restriction increase motor activity and and central temperature in the hours preceding glucose availability and such aticipation is extremely similar to that observed in animals under temporal chow restriction. Glucose ingestion is, therefore, a sufficient temporal cue to induce anticipation in rats. It is possible that the increase in plasma glucose after food ingestion constitutes one of the signals involved in the behavioral entrainment process to food availability / O alimento ? essencial para a sobreviv?ncia de todos os animais. Sua disponibilidade temporal ? uma pista ambiental importante para a organiza??o comportamental e fisiol?gica ao longo das 24 horas do dia em diferentes esp?cies. Ratos e camundongos, por exemplo, mostram aumento da locomo??o nas horas que antecedem a disponibilidade de alimento quando este ? apresentado de forma recorrente, um comportamento denominado de atividade antecipat?ria ao alimento. V?rias evid?ncias indicam que esta antecipa??o ? mediada por um oscilador circadiano. Neste trabalho, com base na hip?tese de que sinais humorais pr?- ou p?s-ingestivos est?o envolvidos no processo de sincroniza??o, testamos se a ingest?o di?ria de glicose ? suficiente para induzir atividade antecipat?ria em ratos. Os ritmos de atividade motora e temperatura central foram registrados em animais submetidos a 10 dias de restri??o de glicose (solu??o a 50 %) ou ra??o em claro-escuro (CE) 12h:12h e escuro constante (EE). Animais submetidos ? restri??o temporal de glicose mostram aumento da atividade motora e da temperatura central nas horas que antecedem a disponibilidade de glicose e tal antecipa??o ? extremamente semelhante ?quela observada em animais sob restri??o temporal de ra??o. A ingest?o de glicose ?, portanto, uma pista temporal suficiente para induzir antecipa??o em ratos. ? poss?vel que o aumento na concentra??o plasm?tica de glicose ap?s a ingest?o de alimento constitua um dos sinais envolvidos no processo de sincroniza??o comportamental ? disponibilidade de alimento