An integrated look at decision-making in bees as they abandon a depleted food source

While there has been considerable research on the behavioral processes that underlie animals’ ability respond to shifting rewards, it remains unclear how animals coordinate multiple processes over time. To investigate this, we compared the behavior of honeybees (Apis mellifera) and bumblebees (Bombus impatiens), in an open-ended search task. Bees were given brief access to a high-quality food source, which then became non-rewarding. Then, over an extended period, we examined (1) bees’ tendency to persist at the depleted site, (2) their tendency to return to a different low-quality food source where they had been foraging previously, (3) their tendency to return to the hive, and (4) how previous reward history influenced their tendency to shift among these options. Compared to bumblebees, honeybees were much slower to abandon the depleted site and were much more likely to make trips to the hive while bumblebees were much more likely to return to the familiar low-quality site. These observed species differences are interpreted in terms of evolved individual and social differences between these species. We show evidence of well-studied behavioral processes such as extinction, negative contrast effects, and reliance on a social group, and provide, for the first time, a picture of how these processes interact with one another as part of a common sequential decision-making process.     

Self-organization in collective honeybee foraging: emergence of symmetry breaking,cross inhibition and equal harvest-rate distribution

De Vries and Biesmeijer described in 1998 an individual-oriented model that simulates the collective foraging behaviour of a colony of honeybees. Here we report how this model has been expanded and show how, through self-organization, three colony-level phenomena can emerge: symmetry breaking, cross inhibition and the equal harvest-rate distribution. Symmetry breaking is the phenomenon that the numbers of foragers visiting two equally profitable food sources will diverge after some time. Cross inhibition is the phenomenon that, by increasing the profitability of one of two equal food sources, the number of foragers visiting the other source will decrease. In some circumstances, the bees foraging on two sources of different profitabilities will be distributed between these sources such that the two average energy harvest rates are equal. We will refer to this phenomenon as the equal harvest-rate distribution. For each of these three phenomena, we show what the necessary behavioural rules to be followed by the individual forager bees are, and what the necessary circumstances are (that is, what values the model parameters should take) in order for these phenomena to arise. It seems that patch size and forager group size largely determine when each of these phenomena will arise. Experimenting with two types of currency, net gain rate and net gain efficiency, revealed that only gain rate may result in an equal harvest-rate distribution of foragers visiting different food sources.     

Nectar-receiver behavior in relation to the reward rate experienced by foraging honeybees

Since forager honeybees change their food-unloading behavior according to nectar-source profitability, an experiment was performed in order to analyze whether food-receivers modify their within-hive tasks related to different reward conditions. We offered individual foragers two reward conditions at a rate feeder while an additional feeder offered a constant reward and was of free access to the rest of the hive. Both feeders were the only food sources exploited by the colony during the assays since a flight chamber was used. After receiving nectar, hive bees performed processing cycles that involved several behaviors and concluded when they returned to the delivery area to receive a new food sample. During these cycles, receivers mainly performed oral contacts offering food, or inspected cells, and often both. In the latter case, both behaviors occurred simultaneously and at the same distance from the hive entrance. When they performed a single task, either the occurrence of cell inspections increased or contact offerings decreased for the highest reward rate offered to the donor-forager. Receivers also begged for food more often after interacting with low-profit foragers. Thus, the profitability of the food source exploited by nectar-forager honeybees could affect receiver behaviors within the hives based on individual-to-individual interactions.Communicated by R.F.A. Moritz     

Honeybee foragers adjust crop contents before leaving the hive

Upon leaving the hive, foragers carry a small amount of honey, which they subsequently consume to generate energy for flight. We investigated the relationship between waggle-phase duration and crop volume in foragers (both dancers and dance followers) leaving the hive. Our findings indicate that these variables were positively correlated in the two types of bee, suggesting that they were able to adjust the amount of food that they carry depending on the distance to a food source. We also found that dance followers left the hive with a larger amount of honey than dancers. We suggest two possible explanations: (1) dance followers have less information about the location of the food source than dancers, who have a better knowledge of the surrounding area; or (2) honeybees lack a precise calibration method for estimating energy needs from waggle-run duration. The effect of foraging experience was confirmed: bees decreased their honey load at departure with repeated trips to a sugar-syrup feeder. Honeybees showed a different pattern of change when the feeder provided soybean flour as a pollen substitute, possibly because honeybees use honey not only as an energy source but also as “glue” to form “balls” of pollen on their hind legs. Based on our observations that followers of sugar-syrup foragers carry a different amount of honey in their crop than followers of soybean-followers, we suggest that waggle dancers also convey information concerning food type.     

Paying for information: partial loads in central place foragers

Information about food sources can be crucial to the success of a foraging animal. We predict that this will influence foraging decisions by group-living foragers, which may sacrifice short-term foraging efficiency to collect information more frequently. This result emerges from a model of a central-place forager that can potentially receive information on newly available superior food sources at the central place. Such foragers are expected to return early from food sources, even with just partial loads, if information about the presence of sufficiently valuable food sources is likely to become available. Returning with an incomplete load implies that the forager is at that point not achieving the maximum possible food delivery rate. However, such partial loading can be more than compensated for by an earlier exploitation of a superior food source. Our model does not assume cooperative foraging and could thus be used to investigate this effect for any social central-place forager. We illustrate the approach using numerical calculations for honeybees and leafcutter ants, which do forage cooperatively. For these examples, however, our results indicate that reducing load confers minimal benefits in terms of receiving information. Moreover, the hypothesis that foragers reduce load to give information more quickly (rather than to receive it) fits empirical data from social insects better. Thus, we can conclude that in these two cases of social-insect foraging, efficient distribution of information by successful foragers may be more important than efficient collection of information by unsuccessful ones.     

Division of labor between scouts and recruits: genetic influence and mechanisms

Every recruitment system in social insects requires some individuals that serve as scouts, foragers that search independently for food sources. It is not well understood which factors influence whether an individual becomes a scout or a recruit, nor how the division of labor between the two forager groups is regulated. It is shown here for honeybees (Apis mellifera), using two different molecular techniques, that there is a genetically based difference in the probability that individuals will scout independently for food. In contrast to earlier suggestions, experimental tests showed that the age of a bee does not seem to influence its probability of becoming a scout or a recruit. Furthermore, scout bees do not search opportunistically for either pollen or nectar but, rather, individuals have preferences that are genetically based. These findings are discussed in the framework of foraging regulation by specialization in honeybees and the adaptive significance of polyandry. Received: 23 October 1997 / Accepted after revision: 10 April 1998     

Effect of food location and quality on recruitment sounds and success in two stingless bees,<Emphasis Type="Italic"> Melipona mandacaia</Emphasis> and<Emphasis Type="Italic"> Melipona bicolor</Emphasis>

It is unclear whether stingless bees in the genus Melipona (Hymenoptera, Apidae, Meliponini) can reliably encode the distance to a food source through recruitment sounds produced inside the nest, in part because the sound features correlated with distance also vary with food quality. We therefore trained marked foragers of two species, Melipona mandacaia and M. bicolor, to feeders at different distances and to different sucrose concentrations at the same distance. In both species, foragers successfully recruited to a rich 2.5-m food source and produced pulsed recruitment sounds in which pulse duration was significantly and positively correlated with distance to the rich food source. When returning from poorer food sources (0.6–1.5 m), foragers of both species decreased sound production, producing shorter sound pulses and longer sound interpulses than they did for 2.5 m food located at the same distance. Thus the temporal structure of M. mandacaia and M. bicolor recruitment sounds varies with distance and food quality. However, nestmates were not recruited by performances for poorer food sources (0.6–1.5 m), whose sucrose concentration was sufficiently low to affect recruitment sounds. Surprisingly, the interphase (the time between behavioral phases that communicate location) also increases with decreasing food quality in the closely related honeybees (Apis), suggesting a potential homology in the effect of food quality on the recruitment systems of Apis and Melipona. We explore the evolutionary implications of these similarities.Communicated by M. Giurfa     

The importance of experience in the interpretation of conspecific chemical signals

Foraging bumblebees scent mark flowers with hydrocarbon secretions. Several studies have found these scent marks act as a repellent to bee foragers. This was thought to minimize the risk of visiting recently depleted flowers. Some studies, however, have found a reverse, attractive effect of scent marks left on flowers. Do bees mark flowers with different scents, or could the same scent be interpreted differently depending on the bees’ previous experience with reward levels in flowers? We use a simple experimental design to investigate if the scent marks can become attractive when bees forage on artificial flowers that remain rewarding upon the bees’ return after having depleted them. We contrast this with bees trained in the more natural scenario where revisits to recently emptied flowers are unrewarding. The bees’ association between scent mark and reward value was tested with flowers scent marked from the same source. We find that the bees’ experience with the level of reward determines how the scent mark is interpreted: the same scent can act as both an attractant and a repellent. How experience and learning influence the interpretation of the meaning of chemical signals deposited by animals for communication has rarely been investigated.     

Tactile learning in resin foraging honeybees

Honeybees harvest and use plant resins in a mixture called propolis to seal cracks and smooth surfaces in the nest architecture. Resins in the nest may be important in maintaining a healthy colony due to their antimicrobial properties. This study had two main objectives: (1) Provide initial insight on the learning capabilities of resin foraging honeybees; (2) analyze the sensitivity of resin foraging honeybees to tactile stimuli to elucidate its possible role as a mechanism behind resin foraging. The first objective provides insight into the phenotype of these bees as compared to other forager types, while the second creates a starting point for further work on behavioral mechanisms of resin foraging. Using tactile proboscis extension response conditioning, we found that resin foragers learned to associate two different tactile stimuli, the presence of a gap between two plates and a rough sandpaper surface, with a sucrose reward significantly better than pollen foragers. The results of differential tactile conditioning exhibited no significant difference in the ability of resin foragers to discriminate between smooth and rough surfaces as compared to pollen foragers. We also determined that the sucrose response thresholds (SRTs) of returning resin foragers were lower compared to returning pollen foragers, but both resin foragers and pollen foragers learned a floral odor equally well. This is the first study to examine SRTs and conditioning to tactile and olfactory stimuli with resin foraging honeybees. The results provide new information and identify areas for future research on resin collectors, an understudied foraging phenotype.     

Assessing the benefits of cooperation in honeybee foraging: search costs,forage quality,and competitive ability

Summary The foragers in honeybee colonies cooperate by sharing information about rich sources of food. This study examines three hypotheses about the benefits of this cooperation: (H1) it decreases foragers' costs in finding new food sources, (H2) it increases the quality of the food sources located by foragers, and (H3) it increases the ability of a colony's foragers to compete for high-quality food sources. To test each hypothesis, we identified a critical pattern in the foraging process which, if observed, would cast doubt on that hypothesis, and then gathered data to check for these patterns. Our observations do not support the first hypothesis, but do support the second and third. These results, in addition to helping us understand the functional significance of the honeybee's dance language, provide insights into the colonial organization of foraging by honeybees.     

Decision making in ant foragers (<Emphasis Type="Italic">Lasius niger</Emphasis>) facing conflicting private and social information

Foragers of many ant species use pheromone trails to guide nestmates to food sources. During foraging, individual workers can also learn the route to a food source. Foragers of the mass-recruiting ant Lasius niger use both pheromone trails and memory to locate a food source. As a result, an experienced forager can have a conflict between social information (trail pheromones) and private information (route memory) at trail bifurcations. We tested decision making in L. niger foragers facing such an informational conflict in situations where both the strength of the pheromone trail and the number of previous visits to the food source varied. Foragers quickly learned the branch at a T bifurcation that leads to a food source, with 74.6% choosing correctly after one previous visit and 95.3% after three visits. Pheromone trails had a weaker effect on choice behaviour of naïve ants, with only 61.6% and 70.2% choosing the branch that had been marked by one or 20 foragers versus an unmarked branch. When there was a conflict between private and social information, memory overrides pheromone after just one previous visit to a food source. Most ants, 82–100%, chose the branch where they had collected food during previous foraging trips, with the proportion depending on the number of previous trips (1 v. 3) but not on the strength of the pheromone trail (1 v. 20). In addition, the presence of a pheromone trail at one branch in a bifurcation had no effect on the time it took an experienced ant to choose the correct branch (the branch without pheromone). These results suggest that private information (navigational memory) dominates over social information (chemical tail) in orientation decisions during foraging activities in experienced L. niger foragers.     

Sensory allometry, foraging task specialization and resource exploitation in honeybees

Insect societies are important models for evolutionary biology and sociobiology. The complexity of some eusocial insect societies appears to arise from self-organized task allocation and group cohesion. One of the best-supported models explaining self-organized task allocation in social insects is the response threshold model, which predicts specialization due to inter-individual variability in sensitivity to task-associated stimuli. The model explains foraging task specialization among honeybee workers, but the factors underlying the differences in individual sensitivity remain elusive. Here, we propose that in honeybees, sensory sensitivity correlates with individual differences in the number of sensory structures, as it does in solitary species. Examining European and Africanized honeybees, we introduce and test the hypothesis that body size and/or sensory allometry is associated with foraging task preferences and resource exploitation. We focus on common morphological measures and on the size and number of structures associated with olfactory sensitivity. We show that the number of olfactory sensilla is greater in pollen and water foragers, which are known to exhibit higher sensory sensitivity, compared to nectar foragers. These differences are independent of the distribution of size within a colony. Our data also suggest that body mass and number of olfactory sensilla correlate with the concentration of nectar gathered by workers, and with the size of pollen loads they carry. We conclude that sensory allometry, but not necessarily body size, is associated with resource exploitation in honeybees and that the differences in number of sensilla may underlie the observed differences in sensitivity between bees specialized on water, pollen and nectar collection.     

Tactics of dance choice in honey bees: do foragers compare dances?

Summary (1) When a honey bee follows recruitment dances to locate a new food source, does she sample multiple dances representing different food sources and selectively respond to the strongest dance? (2) Several initial findings suggested that foragers might indeed compare dances. First, dance information is arrayed in the hive in a way that facilitates comparison-making: dances for different flower patches are performed close together in time and space. Second, food-source quality is coded in the dances, in terms of dance length (number of circuits per dance). Third, dances to natural food sources vary in length by more than 2 orders of magnitude, indicating that the quality of natural food sources varies greatly. Fourth, foragers seeking a new food source follow several dances before exiting the hive (though only one dance is followed closely). (3) Nevertheless, a critical test for comparison-making revealed that foragers evidently do not compare dances. A colony was given two feeders that were equidistant from the hive but different in profitability. If foragers do not compare dances, then the proportion of recruits arriving at the richer feeder should match the proportion of dance circuits for the richer feeder. This is the pattern that we found in all 11 trials of the experiment. (4) We suggest that the reason foragers do not compare dances is that a colony's foraging success is greater if its foragers distribute themselves among the various food sources being advertised in the hive than if they crowd themselves on the one, best source. (5) Food-source selection by honey bee colonies is a democratic decision-making process. This study reveals that this selection process is organized to function effectively even though each member of the democracy possesses incomplete information about the available choices. Offprint requests to: T.D. Seeley     

The role of internal and external information in foraging decisions of Melipona workers (Hymenoptera: Meliponinae)

Social insect foragers have to make foraging decisions based on information that may come from two different sources: information learned and memorised through their own experience (“internal” information) and information communicated by nest mates or directly obtained from their environment (“external” information). The role of these sources of information in decision-making by foragers was studied observationally and experimentally in stingless bees of the genus Melipona. Once a Melipona forager had started its food-collecting career, its decisions to initiate, continue or stop its daily collecting activity were mainly based upon previous experience (activity on previous days, the time at which foraging was initiated the day(s) before, and, during the day, the success of the last foraging flights) and mediated through direct interaction with the food source (load size harvested and time to collect a load). External information provided by returning foragers advanced the start of foraging of experienced bees. Most inexperienced bees initiated their foraging day after successful foragers had returned to the hive. The start of foraging by other inexperienced bees was stimulated by high waste-removal activity of nest mates. By experimentally controlling the entries of foragers (hence external information input) it was shown that very low levels of external information input had large effect on the departure of experienced foragers. After the return of a single successful forager, or five foragers together, the rate of forager exits increased dramatically for 15 min. Only the first and second entry events had large effect; later entries influenced forager exit patterns only slightly. The results show that Melipona foragers make decisions based upon their own experience and that communication stimulates these foragers if it concerns the previously visited source. We discuss the organisation of individual foraging in Melipona and Apis mellifera and are led to the conclusion that these species behave very similarly and that an information-integration model (derived from Fig. 1) could be a starting point for future research on social insect foraging. Received: 16 April 1997 / Accepted after revision: 30 August 1997     

Recruitment to food by the German yellowjacket, Vespula germanica

The hypothesis that Vespula germanica foragers can recruit nestmates to food resources was tested using a protocol that controlled for the biasing effects of social factors at the resource, including local enhancement and food-site marking substances. Foragers from an observation colony in the field were trained to visit a dish of scented corn syrup solution 15?m east of the nest. A second feeding station, 22?m northeast of the nest, offered incoming foragers a choice between food with the training scent and food with a control scent. Significantly more naive foragers arriving at that station chose the food with the training scent. We conclude that the German yellowjacket is able to recruit nestmates to carbohydrate food sources, and that recruits use food odor to locate the source of food being brought into the nest.     

Intracolonial genetic diversity in honeybee (<Emphasis Type="Italic">Apis mellifera</Emphasis>) colonies increases pollen foraging efficiency

Multiple mating by honeybee queens results in colonies of genotypically diverse workers. Recent studies have demonstrated that increased genetic diversity within a honeybee colony increases the variation in the frequency of tasks performed by workers. We show that genotypically diverse colonies, each composed of 20 subfamilies, collect more pollen than do genotypically similar colonies, each composed of a single subfamily. However, genotypically similar colonies collect greater varieties of pollen than do genotypically diverse colonies. Further, the composition of collected pollen types is less similar among genotypically similar colonies than among genotypically diverse colonies. The response threshold model predicts that genotypic subsets of workers vary in their response to task stimuli. Consistent with this model, our findings suggest that genotypically diverse colonies likely send out fewer numbers of foragers that independently search for pollen sources (scouts) in response to protein demand by the colony, resulting in a lower variety of collected pollen types. The cooperative foraging strategy of honeybees involves a limited number of scouts monitoring the environment that then guide the majority of foragers to high quality food sources. The genetic composition of the colony appears to play an important role in the efficiency of this behavior.     

Honeybees modify gustatory responsiveness after receiving nectar from foragers within the hive

Food quality is a relevant characteristic to be transferred within eusocial insect colonies because its evaluation improves the collective foraging efficiency. In honeybees, colony mates could directly acquire this resource characteristic during trophallactic encounters with nectar foragers. In the present study, we focused on the gustatory responsiveness of bees that have unloaded food from incoming foragers. The sugar sensitivity of receiver bees was assessed in the laboratory by using the proboscis extension response paradigm. After unloading, hive bees were captured either from a colony that foraged freely in the environmental surroundings or from a colony that foraged at an artificial feeder with a known sucrose solution. In the first situation, the sugar sensitivity of the hive bees negatively correlated with the sugar concentration of the nectar crops brought back by forager mates. Similarly, in the controlled situation, the highest sucrose concentration the receivers accepted during trophallaxis corresponded to the highest thresholds to sucrose. The results indicate that first-order receivers modify their sugar sensitivity according to the quality of the food previously transferred through trophallaxis by the incoming foragers. In addition, trophallaxis is a mechanism capable of transferring gustatory information in honeybees. Its implications at a social scale might involve changes in the social information as well as in nectar distribution within the colony.     

How ants determine the number of potential recruits

In this paper we present a model that determines the number of potential recruits of Lasius niger, when feeding on a liquid sugar source. The core of the model are two rules: (i) there is a number of workers (facultative foragers) that become potential recruits if starved and (ii) facultative foragers are more likely to become starved than nonforagers because they are more likely to donate food in a trophallaxis (sugar-exchange) event. We develop and explore an analytical model based on these rules, deriving the number of potential recruits after an arbitrary period of starvation. We develop a simplified recruitment model and observe that the predictions of the model are in rough agreement with the empirical data.     

Social foraging by honeybees: how colonies allocate foragers among patches of flowers

Summary To understand how a colony of honeybees keeps its forager force focussed on rich sources of food, and analysis was made of how the individual foragers within a colony decide to abandon or continue working (and perhaps even recruit to) patches of flowers. A nectar forager grades her behavior toward a patch in response to both the nectar intake rate of her colony and the quality of her patch. This results in the threshold in patch quality for acceptance of a patch being higher when the colonial intake rate of nectar is high than when it is low. Thus colonies can adjust their patch selectivity so that they focus on rich sources when forage is abundant, but spread their workers among a wider range of sources when forage is scarce. Foragers assess their colony's rate of nectar intake while in the nest, unloading nectar to receiver bees. The ease of unloading varies inversely with the colonial intake rate of nectar. Foragers assess patch quality while in the field, collecting nectar. By grading their behavior steeply in relation to such patch variables as distance from the nest and nectar sweetness, foragers give their colony high sensitivity to differences in profitability among patches. When a patch's quality declines, its foragers reduce their rate of visits to the patch. This diminishes the flow of nectar from the poor patch which in turn stimulates recruitment to rich patches. Thus a colony can swiftly redistribute its forager force following changes in the spatial distribution of rich food sources. The fundamental currency of nectar patch quality is not net rate of energy intake, (Gain-Cost)/Time, but may be net energy efficiency, (Gain-Cost)/Cost.     

Colony-level selection effects on individual and colony foraging task performance in honeybees, Apis mellifera L.

In honeybees, as in other highly eusocial species, tasks are performed by individual workers, but selection for worker task phenotypes occurs at the colony level. We investigated the effect of colony-level selection for pollen storage levels on the foraging behavior of individual honeybee foragers to determine (1) the relationship between genotype and phenotypic expression of foraging traits at the individual level and (2) how genetically based variation in worker task phenotype is integrated into colony task organization. We placed workers from lines selected at the colony level for high or low pollen stores together with hybrid workers into a common hive environment with controlled access to resources. Workers from the selected lines showed reciprocal variation in pollen and nectar collection. High-pollen-line foragers collected pollen preferentially, and low- pollen-line workers collected nectar, indicating that the two tasks covary genetically. Hybrid workers were not intermediate in phenotype, but instead showed directional dominance for nectar collection. We monitored the responses of workers from the selected strains to changes in internal (colony) and external (resource) stimulus levels for pollen foraging to measure the interaction between genotypic variation in foraging behavior and stimulus environment. Under low-stimulus conditions, the foraging group was over-represented by high-pollen-line workers. However, the evenness in distribution of the focal genetic groups increased as foraging stimuli increased. These data are consistent with a model where task choice is a consequence of genetically based response thresholds, and where genotypic diversity allows colony flexibility by providing a range of stimulus thresholds. Received: 3 May 1999 / Received in revised form: 22 December 1999 / Accepted: 23 January 2000