The effect of foraging specialization on various learning tasks in the honey bee (<Emphasis Type="Italic">Apis mellifera</Emphasis>)

Honey bee foragers may collect nectar, pollen, water, or propolis, and their foraging specialization has been associated with several behavioral traits. By conditioning of the proboscis extension response (PER), we compared the performance of foragers that collected nectar, pollen, both nectar and pollen, or water in several learning and choice assays. Foragers were first tested in a three-trial olfactory associative learning assay. For further tests, we selected only good learners that responded in two out of three conditioning trials. One group was tested in an additional olfactory associative learning assay involving different reward volumes and concentrations. Another group was tested for risk sensitivity in a two-alternative forced-choice PER procedure and then in a latent inhibition (LI) assay. Levels of acquisition in olfactory associative learning were highest in pollen and water foragers, and better acquisition was associated with collection of heavier pollen loads and smaller and lighter nectar loads of lower sugar concentration. Among the good learners, pollen foragers still showed better acquisition than nectar foragers when rewarded with several volumes and concentrations of sucrose solution. Pollen and nectar foragers were equally risk averse, preferring a constant reward to a variable one, and choice was not affected by pollen load weight. Contrary to a previous study, pollen and nectar foragers were similarly affected by LI. We discuss possible explanations for the discrepancy between the two studies. Overall, our results suggest that differences between foraging groups in sensitivity to various stimuli may not correspond to differences in choice behavior.     

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.     

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     

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.     

Limited flexibility in the temporal caste system of the honey bee

Caste theory predicts that social insect colonies are organized into stable groups of workers specialized on particular task sets. Alternative concepts of organization of work suggest that colonies are composed of extremely flexible workers able to perform any task as demand necessitates. I explored the flexibility of workers in temporal castes of the honey bee Apis mellifera by determining the ability of colonies to reorganize labor after a major demographic disturbance. I evaluated the flexibility of temporal castes by comparing the foraging rates of colonies having just lost their foragers with colonies having also lost their foragers but having been given a week to reorganize. The population sizes and contents of the colonies in each group were equalized and foraging rates were recorded for one week. Colonies given a weeks initial recovery time after the loss of their foragers were found to forage at significantly higher rates than those colonies given no initial recovery time. This result was consistent for nectar and pollen foraging. These results suggest that honeybee workers lack sufficient flexibility to reorganize labor without compromising foraging. This finding is consistent with the caste concept model of organization of work in insect societies.     

Division of foraging labor in ants can mediate demands for food and safety

Solitary foragers can balance demands for food and safety by varying their relative use of foraging patches and their level of vigilance. Here, we investigate whether colonies of the ant, Formica perpilosa, can balance these demands by dividing labor among workers. We show that foragers collecting nectar in vegetation near their nest are smaller than are those collecting nectar at sites away from the nest. We then use performance tests to show that smaller workers are more likely to succumb to attack from conspecifics but feed on nectar more efficiently than larger workers, suggesting a size-related trade-off between risk susceptibility and harvesting ability. Because foragers that travel away from the nest are probably more likely to encounter ants from neighboring colonies, this trade-off could explain the benefits of dividing foraging labor among workers. In a laboratory experiment, we show that contact with aggressive workers results in an increase in the mean size of recruits to a foraging site: this increase was not the result of more large recruits, but rather because fewer smaller ants traveled to the site. These results suggest that workers particularly susceptible to risk avoid dangerous sites, and suggest that variation in worker size can allow colonies to exploit profitably both hazardous and resource-poor patches.Communicated by L. Sundström     

The effects of young brood on the foraging behavior of two strains of honey bees (<Emphasis Type="Italic">Apis mellifera</Emphasis>)

Honey bee foragers specialize on collecting pollen and nectar. Pollen foraging behavior is modulated by at least two stimuli within the nest: the presence of brood pheromone and young larvae and the quantity of stored pollen. Genetic variation in pollen foraging behavior has been demonstrated repeatedly. We used selected high and low pollen-hoarding strains of bees that differ dramatically in the quantity of pollen collected to determine if the observed differences in foraging could be explained by differential responses to brood stimuli. Workers from the high and low pollen-hoarding strains and wild-type bees were co-fostered in colonies with either brood or no brood. As expected based on previous studies, returning high pollen-hoarding foragers collected heavier pollen loads and lighter nectar loads than low pollen-hoarding bees. Effects of brood treatment were also observed; bees exposed to brood collected heavier pollen loads and initiated foraging earlier than those from broodless colonies. More specifically, brood treatment resulted in increased pollen foraging in high pollen-hoarding bees but did not affect pollen foraging in low pollen-hoarding bees, suggesting that high pollen-hoarding bees are more sensitive to the presence of brood. However, response to brood stimuli does not sufficiently explain the differences in foraging behavior between the strains since these differences persisted even in the absence of brood.     

Regulation of pollen foraging in honeybee colonies: effects of young brood, stored pollen, and empty space

Pollen storage in a colony of Apis mellifera is actively regulated by increasing and decreasing pollen foraging according to the “colony's needs.” It has been shown that nectar foragers indirectly gather information about the nectar supply of the colony from nestmates without estimating the amount of honey actually stored in the combs. Very little is known about how the actual colony need is perceived with respect to pollen foraging. Two factors influence the need for pollen: the quantity of pollen stored in cells and the amount of brood. To elucidate the mechanisms of perception, we changed the environment within normal-sized colonies by adding pollen or young brood and measured the pollen-foraging activity, while foragers had either direct access to them or not. Our results show that the amount of stored pollen, young brood, and empty space directly provide important stimuli that affect foraging behavior. Different mechanisms for forager perception of the change in the environment are discussed. Received: 13 June 1998 / Accepted after revision: 25 October 1998     

Response thresholds to sucrose predict foraging division of labor in honeybees

Division of labor, where thousands of individuals perform specific behavioral acts repeatedly and non-randomly, is the hallmark of insect societies. Virtually nothing is known about the underlying neurophysiological processes that direct individuals into specific behavioral roles. We demonstrate that sensory-physiological variation in the perception of sucrose in honeybees measured when they are 1 week old correlates with their foraging behavior 2–3 weeks later. Workers with the lowest response thresholds became water foragers, followed with increasing response thresholds by pollen foragers, nectar foragers, bees collecting both pollen and nectar, and finally those returning to the colony empty (water<pollen<nectar<both<empty). Sucrose concentrations of nectar loads were positively correlated with response thresholds measured on 1-week-old bees. These results demonstrated how the variable response thresholds of a sensory-physiological process, the perception of sucrose, is causally linked to the division of labor of foraging. Received. 28 June 1999 / Received in revised form: 2 November 1999 / Accepted: 20 November 1999     

Effects of experience and weather on foraging rate and pollen versus nectar collection in the bumblebee, Bombus terrestris

This study examines factors that affect foraging rate of free-flying bumblebees, Bombus terrestris, when collecting nectar, and also what factors determine whether they collect pollen or nectar. We show that nectar foraging rate (mass gathered per unit time) is positively correlated with worker size, in accordance with previous studies. It has been suggested that the greater foraging rate of large bees is due to their higher thermoregulatory capacity in cool conditions, but our data suggest that this is not so. Workers differing in size were not differentially affected by the weather. Regardless of size, naïve bees were poor foragers, often using more resources than they gathered. Foraging rate was not maximised until at least 30 trips had been made from the nest. Foraging rates were positively correlated with humidity, perhaps because nectar secretion rates were higher or evaporation of nectar lower at high humidity. Temperature, wind speed and cloud cover did not significantly influence foraging rate, within the summertime range that occurred during the study. Weather greatly influenced whether bees collected pollen or nectar. Pollen was preferably collected when it was warm, windy, and particularly when humidity was low; and preferably during the middle of the day. We suggest that bees collect pollen in dry conditions, and avoid collecting pollen when there is dew or rain-water droplets on the vegetation, which would make grooming pollen into the corbiculae difficult. Availability of sufficient dry days for pollen collection may be an important factor determining the success of bumblebee colonies.Communicated by M. Giurfa     

Worker piping in honey bees (<Emphasis Type="Italic">Apis mellifera</Emphasis>): the behavior of piping nectar foragers

This study investigates the brief piping signals ("stop signals") of honey bee workers by exploring the context in which worker piping occurs and the identity and behavior of piping workers. Piping was stimulated reliably by promoting a colony's nectar foraging activity, demonstrating a causal connection between worker piping and nectar foraging. Comparison of the behavior of piping versus non-piping nectar foragers revealed many differences, e.g., piping nectar foragers spent more time in the hive, started to dance earlier, spent more time dancing, and spent less time on the dance floor. Most piping signals (approximately 99%) were produced by tremble dancers, yet not all (approximately 48%) tremble dancers piped, suggesting that the short piping signal and the tremble dance have related, but not identical, functions in the nectar foraging communication system. Our observations of the location and behavior of piping tremble dancers suggest that the brief piping signal may (1) retard recruitment to a low-quality food source, and (2) help to enhance the recruitment success of the tremble dance.     

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.     

Intra-colonial foraging specialism by honey bees (Apis mellifera) (Hymenoptera:Apidae)

Summary Colonies of honey bees with two identifiable subfamilies were established. Returning foragers were captured and killed at two different sampling times. The mean volume and per cent soluble solids of crop contents were determined for each subfamily, as was the mean weight of the pollen pellets. No significant differences in nectar volume or concentration were detected between subfamilies within colonies. However, in a few colonies, significant subfamily by sampling-time interactions were present, suggesting that in these colonies subfamilies differed in their nectar and pollen collecting behavior at different times of day. The plant genera worked by pollen foragers were also determined. In four of six colonies, bees of different subfamilies were found to be majoring on different plant species (Fig. 1). Implications of this intra-colonial variance in foraging behavior for colony fitness are discussed. Offprint requests to: B.P. Oldroyd     

Promiscuous honeybee queens generate colonies with a critical minority of waggle-dancing foragers

Honeybees present a paradox that is unusual among the social Hymenoptera: extremely promiscuous queens generate colonies of nonreproducing workers who cooperate to rear reproductives with whom they share limited kinship. Extreme polyandry, which lowers relatedness but creates within-colony genetic diversity, produces substantial fitness benefits for honeybee queens and their colonies because of increased disease resistance and workforce productivity. However, the way that these increases are generated by individuals in genetically diverse colonies remains a mystery. We assayed the foraging and dancing performances of workers in multiple-patriline and single-patriline colonies to discover how within-colony genetic diversity, conferred to colonies by polyandrous queens, gives rise to a more productive foraging effort. We also determined whether the initiation by foragers of waggle-dance signaling in response to an increasing sucrose stimulus (their dance response thresholds) was linked to patriline membership. Per capita, foragers in multiple-patriline colonies visited a food source more often and advertised it with more waggle-dance signals than foragers from single-patriline colonies, although there was variability among multiple-patriline colonies in the strength of this difference. High-participation patrilines emerged within multiple-patriline colonies, but their more numerous foragers and dancers were neither more active per capita nor lower-threshold dancers than their counterparts from low-participation patrilines. Our results demonstrate that extreme polyandry does not enhance recruitment effort through the introduction of low-dance-threshold, high-activity workers into a colony’s population. Rather, genetic diversity is critical for injecting into a colony’s workforce social facilitators who are more likely to become engaged in foraging-related activities, so boosting the production of dance signals and a colony’s responsiveness to profitable food sources.     

The influence of pollen quality on foraging behavior in honeybees (Apis mellifera L.)

Individual and colony-level foraging behaviors were evaluated in response to changes in the quantity or nutritional quality of pollen stored within honeybee (Apis mellifera L.) colonies. Colonies were housed in vertical, three-frame observation hives situated inside a building, with entrances leading to the exterior. Before receiving treatments, all colonies were deprived of pollen for 5 days and pollen foragers were marked. In one treatment group, colony pollen reserves were quantitatively manipulated to a low or high level, either by starving colonies of pollen or by providing them with a fully provisioned frame of pollen composed of mixed species. In another treatment group, pollen reserves were qualitatively manipulated by removing pollen stores from colonies and replacing them with low- or high-protein pollen supplements. After applying treatments, foraging rates were measured four times per day and pollen pellets were collected from experienced and inexperienced foragers to determine their weight, species composition, and protein content. Honeybee colonies responded to decreases in the quantity or quality of pollen reserves by increasing the proportion of pollen foragers in their foraging populations, without increasing the overall foraging rate. Manipulation of pollen stores had no effect on the breadth of floral species collected by colonies, or their preferences for the size or protein content of pollen grains. In addition, treatments had no effect on the weight of pollen loads collected by individual foragers or the number of floral species collected per foraging trip. However, significant changes in foraging behavior were detected in relation to the experience level of foragers. Irrespective of treatment group, inexperienced foragers exerted greater effort by collecting heavier pollen loads and also sampled their floral environment more extensively than experienced foragers. Overall, our results indicate that honeybees respond to deficiencies in the quantity or quality of their pollen reserves by increasing the gross amount of pollen returned to the colony, rather than by specializing in collecting pollen with a greater protein content. Individual pollen foragers appear to be insensitive to the quality of pollen they collect, indicating that colony-level feedback is necessary to regulate the flow of protein to and within the colony. Colonies may respond to changes in the quality of their pollen stores by adjusting the numbers of inexperienced to experienced foragers within their foraging populations.     

The effects of colony-level selection on the social organization of honey bee (Apis mellifera L.) colonies: colony-level components of pollen hoarding

Two-way selection for quantities of stored pollen resulted in the production of high and low pollen hoarding strains of honey bees (Apis mellifera L.). Strains differed in areas of stored pollen after a single generation of selection and, by the third generation, the high strain colonies stored an average 6 times more pollen than low strain colonies. Colony-level organizational components that potentially affect pollen stores were identified that varied genetically within and between these strains. Changes occurred in several of these components, in addition to changes in the selected trait. High strain colonies had a significantly higher proportion of foragers returning with loads of pollen, however, high and low strain colonies had equal total numbers of foragers Colony rates of intake of pollen and nectar were not independent. Selection resulted in an increase in the number of pollen collectors and a decrease in the number of nectar collectors in high strain colonies, while the reciprocal relationship occurred in the low strain. High and low strain colonies also demonstrated different diurnal foraging patterns as measured by the changing proportions of returning pollen foragers. High strain colonies of generation 3 contained significantly less brood than did low strain colonies, a consequence of a constraint on colony growth resulting from a fixed nest volume and large quantities of stored pollen. These components represent selectable colony-level traits on which natural selection can act and shape the social organization of honey bee coloniesCommunicated by R.F.A. Moritz     

Directional change in a suite of foraging behaviors in tropical and temperate evolved honey bees (<Emphasis Type="Italic">Apis mellifera</Emphasis> L.)

The concept of a suite of foraging behaviors was introduced as a set of traits showing associative directional change as a characterization of adaptive evolution. I report how naturally selected differential sucrose response thresholds directionally affected a suite of honey bee foraging behaviors. Africanized and European honey bees were tested for their proboscis extension response thresholds to ascending sucrose concentrations, reared in common European colonies and, captured returning from their earliest observed foraging flight. Race constrained sucrose response threshold such that Africanized bees had significantly lower sucrose response thresholds. A Cox proportional hazards regression model of honey bee race and sucrose response threshold indicated that Africanized bees were 29% (P<0.01) more at risk to forage over the 30-day experimental period. Sucrose response threshold organized age of first foraging such that each unit decrease in sucrose response threshold increased risk to forage by 14.3% (P<0.0001). Africanized bees were more likely to return as pollen and water foragers than European foragers. Africanized foragers returned with nectar that was significantly less concentrated than European foragers. A comparative analysis of artificial and naturally selected populations with differential sucrose response thresholds and the common suite of directional change in foraging behaviors is discussed. A suite of foraging behaviors changed with a change in sucrose response threshold that appeared as a product of functional ecological adaptation.Communicated by R.F.A. Moritz     

Patch departure rules in Bumblebees: evidence of a decremental motivational mechanism

The patch living rules of a pollinator, the bumblebee Bombus terrestris L., are studied here in the framework of motivational models widely used for parasitoids: The rewarding events found during the foraging process are supposed to increase or decrease suddenly the tendency of the insect to stay in the current patch and therefore to adjust the patch residence time to the patch profitability. The foraging behaviour of these pollinators was observed in two environment types to determine their patch-leaving decisions. The rich environment was composed of male-fertile flowers, offering pollen and nectar, and the poor one of male-sterile flowers, offering little nectar and no pollen. The experimental design consisted of a patch system in which inflorescences were evenly arranged in two rows (1 m distance). Residence times of foragers inside inflorescences and rows were analysed by a Cox proportional hazards model, taking into account recent and past experience acquired during the foraging bout. Most of the results showed a decremental motivational mechanism, that is, a reduction in the residence time on the inflorescence or in the row related to exploitation of flowers within inflorescences and inflorescences within rows These results indicate that bumblebees tend to leave the patch using departure rules similar to those found in parasitoids. The results also provide information on the memory, learning and evaluating capabilities of bumblebees especially when rich and poor environments were compared. The patch-leaving mechanism suggested by this study is consistent with the central place foraging theory.     

Behavioral and life-history components of division of labor in honey bees (Apis mellifera L.)

Variability exists among worker honey bees for components of division of labor. These components are of two types, those that affect foraging behavior and those that affect life-history characteristics of workers. Variable foraging behavior components are: the probability that foraging workers collect (1) pollen only; (2) nectar only; and (3) pollen and nectar on the same trip. Life history components are: (1) the age the workers initiate foraging behavior; (2) the length of the foraging life of a worker; and (3) worker length of life. We show how these components may interact to change the social organization of honey bee colonies and the lifetime foraging productivity of individual workers. Selection acting on foraging behavior components may result in changes in the proportion of workers collecting pollen and nectar. Selection acting on life-history components may affect the size of the foraging population and the distribution of workers between within nest and foraging activities. We suggest that these components define possible sociogenic pathways through which colony-level natural selection can change social organization. These pathways may be analogous to developmental pathways in the morphogenesis of individual organisms because small changes in behavioral or life history components of individual workers may lead to major changes in the organizational structure of colonies. Correspondence to: R.E. Page, Jr.     

Brood pheromone stimulates pollen foraging in honey bees (Apis mellifera)

Foraging and the mechanisms that regulate the quantity of food collected are important evolutionary and ecological attributes for all organisms. The decision to collect pollen by honey bee foragers depends on the number of larvae (brood), amount of stored pollen in the colony, as well as forager genotype and available resources in the environment. Here we describe how brood pheromone (whole hexane extracts of larvae) influenced honey bee pollen foraging and test the predictions of two foraging-regulation hypotheses: the indirect or brood-food mechanism and the direct mechanism of pollen-foraging regulation. Hexane extracts of larvae containing brood pheromone stimulated pollen foraging. Colonies were provided with extracts of 1000 larvae (brood pheromone), 1000 larvae (brood), or no brood or pheromone. Colonies with brood pheromone and brood had similar numbers of pollen foragers, while those colonies without brood or pheromone had significantly fewer pollen foragers. The number of pollen foragers increased more than 2.5-fold when colonies were provided with extracts of 2000 larvae as a supplement to the 1000 larvae they already had. Within 1 h of presenting colonies with brood pheromone, pollen foragers responded to the stimulus. The results from this study demonstrate some important aspects of pollen foraging in honey bee colonies: (1) pollen foragers appear to be directly affected by brood pheromone, (2) pollen foraging can be stimulated with brood pheromone in colonies provided with pollen but no larvae, and (3) pollen forager numbers increase with brood pheromone as a supplement to brood without increasing the number of larvae in the colony. These results support the direct-stimulus hypothesis for pollen foraging and do not support the indirect-inhibitor, brood-food hypothesis for pollen-foraging regulation. Received: 5 March 1998 / Accepted after revision: 29 August 1998