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.     

Effects of interactions among genotypically diverse nestmates on task specialization by foraging honey bees (Apis mellifera)

Summary Recent studies have shown that differences in patterns of task specialization among nestmate honeybee workers (Apis mellifera) can be explained, in part, as a consequence of genotypic variability. Here, we present evidence supporting the hypothesis that an individual's pattern of task specialization is affected not only by her own genotype, but, indirectly, by the genotypes of her nestmates. Workers from two strains of honey bees, one selected for high pollen hoarding, the other for low pollen hoarding, were observed in colonies of their respective parent strains and in colonies of the other strain. Worker genotype and host-colony type affected foraging activity. Workers from the high strain fostered in low-strain colonies returned with pollen on 75.6% of total foraging trips, while workers from the high strain fostered in high-strain colonies returned with pollen on 53.5% of total trips. Workers from the low strain fostered in low-strain colonies returned with pollen on 34.8% of total foraging trips while workers from the low strain fostered in high-strain colonies returned with pollen on 2.6% of total trips. Similar results were obtained in a second experiment. We suggest that workers influence the behavior of their nestmates indirectly through their effects on the shared colony environment. The asymmetry seen in the response of workers from these strains to the two types of colony environments also suggests that these genotypes exhibit different norms of reaction. Offprint requests to: N.W. Calderone     

Complex pleiotropy characterizes the pollen hoarding syndrome in honey bees (Apis mellifera L.)

The pollen hoarding syndrome consists of a large suite of correlated traits in honey bees that may have played an important role in colony organization and consequently the social evolution of honey bees. The syndrome was first discovered in two strains that have been artificially selected for high and low pollen hoarding. These selected strains are used here to further investigate the phenotypic and genetic links between two central aspects of the pollen hoarding syndrome: sucrose responsiveness and pollen hoarding. Sons of hybrid queen offspring of these two strains were tested for sucrose responsiveness and used to produce colonies with either a highly responsive or an unresponsive father. These two colony groups differed significantly in the amount of pollen stored on brood combs and with regard to their relationship between brood and pollen amounts. Additionally, four quantitative trait loci (QTL) for pollen hoarding behavior were assessed for their effect on sucrose responsiveness. Drone offspring of two hybrid queens were phenotyped for responsiveness and genotyped at marker loci for these QTL, identifying some pleiotropic effects of the QTL with significant QTL interactions. Both experiments thus provided corroborating evidence that the distinct traits of the pollen hoarding syndrome are mechanistically and genetically linked and that these links are complex and dependent on background genotype. The study demonstrates genetic worker–drone correlations within the context of the pollen hoarding syndrome and establishes that an indirect selection response connects pollen hoarding and sucrose responsiveness, regardless of which trait is directly selected.     

Effects of protein-constrained brood food on honey bee (<Emphasis Type="Italic">Apis mellifera</Emphasis> L.) pollen foraging and colony growth

Pollen is the sole source of protein for honey bees, most importantly used to rear young. Honey bees are adept at regulating pollen stores in the colonies based on the needs of the colony. Mechanisms for regulation of pollen foraging in honey bee are complex and remain controversial. In this study, we used a novel approach to test the two competing hypothesis of pollen foraging regulation. We manipulated nurse bee biosynthesis of brood food using a protease inhibitor that interferes with midgut protein digestion, significantly decreasing the amount of protein extractable from hypopharyngeal glands. Experimental colonies were given equal amounts of protease inhibitor-treated and untreated pollen. Colonies receiving protease inhibitor treatment had significantly lower hypopharyngeal gland protein content than controls. There was no significant difference in the ratio of pollen to nonpollen foragers between the treatments. Pollen load weights were also not significantly different between treatments. Our results supported the pollen foraging effort predictions generated from the direct independent effects of pollen on the regulation of pollen foraging and did not support the prediction that nurse bees regulate pollen foraging through amount of hypopharyngeal gland protein biosynthesis.     

Regulation of honey bee age polyethism by juvenile hormone

Summary Previous studies suggested that juvenile hormone (JH) is involved in the regulation of physiological processes that are associated with division of labor in honey bees but the effects of JH on behavior were not clear. The hypothesis that JH affects worker age polyethism was tested by observing individually marked bees topically treated with different doses of the JH analog methoprene. Methoprene caused dose-dependent changes in the timing and frequency of occurrence of four important age-dependent tasks: brood and queen care, food storage, nest maintenance, and foraging. Weak or no effects were observed for social interactions, self-grooming, and other non-task behaviors that were not performed in an age-dependent manner. These results support the hypothesis that JH is involved in the control of age polyethism. A model is presented that explains the role of JH in regulating division of labor. JH may regulate the colony's allocation of labor by altering the probabilities of response to tasks. According to this model, hormone titers increase with age according to a genetically determined pattern of development, but this rise may be modulated by environmental and colony factors such as food availability and population structure. Extrinsic regulation of JH may be a mechanism underlying the ability of workers to respond to changing colony needs.     

Effects of colony food shortage on behavioral development in honey bees

Three experiments were conducted to explore the effects of severe food shortage on the control of two important and interrelated aspects of temporal division of labor in colonies of the honey bee (Apis mellifera): the size and age distribution of a colony's foraging force. The experiments were conducted with single-cohort colonies, composed entirely of young bees, allowing us to quickly distinguish the development of new (precocious) foragers from increases in activity of bees already competent to forage. In experiment 1, colony food shortage caused an acceleration of behavioral development; a significantly greater proportion of bees from starved colonies than from fed colonies became precocious foragers, and at significantly younger ages. Temporal aspects of this starvation effect were further explored in experiment 2 by feeding colonies that we initially starved, and starving colonies that we initially fed. There was a significant decrease in the number of new foragers in starved colonies that were fed, detected 1 day after feeding. There also was a significant increase in the number of new foragers in fed colonies that were starved, but only after a 2-day lag. These results suggest that colony nutritional status does affect long-term behavioral development, rather than only modulate the activity of bees already competent to forage. In experiment 3, we uncoupled the nutritional status of a colony from that of the individual colony members. The behavior of fed individuals in starved colonies was indistinguishable from that of bees in fed colonies, but significantly different from that of bees in starved colonies, in terms of both the number and age distribution of foragers. These results demonstrate that effects of starvation on temporal polyethism are not mediated by the most obvious possible worker-nest interaction: a direct interaction with colony food stores. This is consistent with previous findings suggesting the importance of worker-worker interactions in the regulation of temporal polyethism in honey bees as well as other social insects. Received: 17 April 1997 / Accepted after revision: 26 December 1997     

Timekeeping in the honey bee colony: integration of circadian rhythms and division of labor

The daily patterns of task performance in honey bee colonies during behavioral development were studied to determine the role of circadian rhythmicity in age-related division of labor. Although it is well known that foragers exhibit robust circadian patterns of activity in both field and laboratory settings, we report that many in-hive tasks are not allocated according to a daily rhythm but rather are performed 24 h per day. Around-the-clock activity at the colony level is accomplished through the performance of some tasks by individual workers randomly with respect to time of day. Bees are initially arrhythmic with respect to task performance but develop diel rhythmicity, by increasing the occurrence of inactivity at night, prior to becoming foragers. There are genotypic differences for age at onset of rhythmicity and our results suggest that these differences are correlated with genotypic variation in rate of behavioral development: genotypes of bees that progressed through the age polyethism schedule faster also acquired behavioral rhythmicity at an earlier age. The ontogeny of circadian rhythmicity in honey bee workers ensures that essential in-hive behaviors are performed around the clock but also allows the circadian clock to be engaged before the onset of foraging. Received: 6 October 1997 / Accepted after revision: 28 March 1998     

Division of labor between undertaker specialists and other middle-aged workers in honey bee colonies

A primary determinant of colony organization in temporally polyethic insect societies is inter-individual variation in behavior that is independent of worker age. We examined behavioral repertoires, behavioral correlates of adult development, and spatial distributions within the hive to explore the mechanisms that produce behavioral variation among middle-age honey bees (Apis mellifera). Individually labeled undertakers, guards, food storers, and wax workers exhibited a broad range of task-related behavior, but bees tagged as undertakers were more likely to subsequently remove a corpse from the hive and handle a corpse compared to other middle-aged bees. The activity level of undertakers was similar to other task groups, suggesting that undertaking specialists were neither hyper-active “elites” nor quiescent “reserves” that become active only when a dead bee stimulus is present. Undertakers also were more likely to remove debris and to remain in the lower region of the hive or near the entrance, even when not engaged in corpse removal; both preferences may promote colony efficiency by reducing inter-task travel times. Guards and undertakers were less likely to perform behavior normally associated with young bees compared to food storers and wax workers. Undertakers and guards also initiated foraging at earlier ages than the other task groups. These results suggest that undertakers and guards may be slightly developmentally advanced compared to food storers and wax workers. There also was evidence for lifetime differences in behavioral preferences which could not be explained by differences in adult development. Bees tagged as undertakers were more likely to subsequently remove a dead bee during their entire pre-foraging career compared to other task groups or members of their general age cohort. Differences in both the rate of adult development and individual behavioral preferences, both of which may be subject to genetic and environmental influences, are important determinants of inter-individual variation among honey bees of middle age. Received: 5 February 1997 / Accepted after revision: 27 May 1997     

Genotypic variability in age polyethism and task specialization in the honey bee,Apis mellifera (Hymenoptera: Apidae)

Summary The currently accepted model for division of labor in honey bees, Apis mellifera, explains variation in the frequency at which workers perform specific tasks as the result of differences in age and environment. Although well documented, the model is incomplete because it fails to take genotypic variability among workers into account. We show that workers from two genetically distinct strains of honey bees differed in the age at which they began foraging and in the relative frequency at which they foraged for pollen. Workers from the two strains also exhibited significant spatial heterogeneity within the nest, suggesting that they differed in the frequency at which they performed within-nest tasks as well. A heuristic model of division of labor that incorporates genotypic effects is presented.     

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.     

The communal crop: modulation of sucrose response thresholds of pre-foraging honey bees with incoming nectar quality

We examined whether the quality (concentration) of incoming sucrose solutions returned by foraging honey bees affected the response thresholds of pre-foraging members of the colony. Six pairs of colonies were given ad libitum access to sucrose solution feeders. A colony from each pair was switched from 20–50% sugar concentration feeders while the other continued to have access to 20% sucrose feeders. Proboscis extension response (PER) scores to an increasing series of sucrose concentrations were significantly higher in pre-foragers of colonies foraging on 20% sucrose throughout compared to pre-foragers in colonies where foraging was switched to 50% sucrose. Although all colonies had honey stores, the concentration of sugar solution in non-foraging bees crops were significantly lower in bees from colonies foraging on 20% sucrose compared to those from colonies foraging on 50% sucrose. Because response thresholds to sugar of young bees were modulated by the concentration of sucrose solution returned to colonies, we repeated the 2000 study of Pankiw and Page that potentially confounded baseline response thresholds with modulated scores due to experience in the colony. Here, we examined PER scores to sucrose in bees within 6 h of emergence, prior to feeding experience, and their forage choice 2 to 3 weeks later. Pollen foragers had higher PER scores as newly emerged bees compared to bees that eventually became nectar foragers. These results confirm those of the 2000 study by Pankiw and Page. Combined, these experiments demonstrate that variation in pre-forager sucrose response thresholds are established prior to emerging as adults but may be modulated by incoming resources later on. Whether this modulation has long-term effects on foraging behavior is unknown but modulation has short-term effects and the potential to act as a means of communication among all bees in the colony.Communicated by M. Giurfa     

Colony state and regulation of pollen foraging in the honey bee,Apis mellifera L.

Summary To place social insect foraging behavior within an evolutionary context, it is necessary to establish relationships between individual foraging decisions and parameters influencing colony fitness. To address this problem, we examined interactions between individual foraging behavior and pollen storage levels in the honey bee, Apis mellifera L. Colonies responded to low pollen storage conditions by increasing pollen intake rates 54% relative to high pollen storage conditions, demonstrating a direct relationship between pollen storage levels and foraging effort. Approximately 80% of the difference in pollen intake rates was accounted for by variation in individual foraging effort, via changes in foraging activity and individual pollen load size. An additional 20% resulted from changes in the proportion of the foraging population collecting pollen. Under both high and low pollen storage treatments, colonies returned pollen storage levels to pre-experimental levels within 16 days, suggesting that honey bees regulate pollen storage levels around a homeostatic set point. We also found a direct relationship between pollen storage levels and colony brood production, demonstrating the potential for cumulative changes in individual foraging decisions to affect colony fitness. Offprint requests to: J.H. Fewell at the current address     

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     

Genotype and colony environment affect honeybee (Apis mellifera L.) development and foraging behavior

We examined the interaction of genotype and environment on foraging-behavior development and forage choice in honeybees. High- and low-pollen-hoarding strains and unselected wild-type bees were co-fostered in pairs of colonies manipulated to differentially stimulate high and low pollen foraging. The high-pollen-foraging stimulus consisted of high amounts of larvae, a known stimulus for pollen foraging, plus low amounts of pollen, known to induce pollen foraging. The low-pollen-foraging stimulus consisted of low amounts of larvae plus high amounts of pollen. We estimated the median age at which bees initiated foraging, determined forage choice, and the quality and quantity of resources collected. High-strain bees consistently foraged at younger ages than workers from the other sources. High-strain bees appeared to be more sensitive to the pollen-foraging-stimulus treatments, showing greater differences in foraging age and behavior. Three-way interactions of genotype, pollen foraging stimulus, and colony pair (replicate) were statistically significant for most foraging variables measured suggesting that additional, unknown environmental factors also affect foraging behavior. Our results suggest there is a functional relationship between age of first foraging and forage choice with a strong genetic component that is modulated by colony environment.     

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     

Brood temperature, task division and colony survival in honeybees: A model

One of the mechanisms by which honeybees regulate division of labour among their colony members is age polyethism. Here the younger bees perform in-hive tasks such as heating and the older ones carry out tasks outside the hive such as foraging. Recently it has been shown that the higher developmental temperatures of the brood, which occur in the centre of the brood nest, reduce the age at which individuals start to forage once they are adult. It is unknown whether this effect has an impact on the survival of the colony. The aim of this paper is to study the consequences of the temperature gradient on the colony survival in a model on the basis of empirical data.We created a deterministic simulation of a honeybee colony (Apis mellifera) which we tuned to our empirical data. In the model in-hive bees regulate the temperature of the brood nest by their heating activities. These temperatures determine the age of first foraging in the newly emerging bees and thus the number of in-hive bees present in the colony. The results of the model show that variation in the onset of foraging due to the different developmental temperatures has little impact on the population dynamics and on the absolute number of bees heating the nest unless we increase this effect by several times to unrealistic values, where individuals start foraging up to 10 days earlier or later. Rather than on variation in the onset of foraging due to the temperature gradient it appears that the survival of the colony depends on a minimal number of bees available for heating at the beginning of the simulation.     

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     

Brood pheromone modulates honeybee (Apis mellifera L.) sucrose response thresholds

Foraging behavior and the mechanisms that regulate foraging activity are important components of social organization. Here we test the hypothesis that brood pheromone modulates the sucrose response threshold of bees. Recently the honeybee proboscis extension response to sucrose has been identified as a ”window” into a bee’s perception of sugar. The sucrose response threshold measured in the first week of adult life, prior to foraging age, predicts forage choice. Bees with low response thresholds are more likely to be pollen foragers and bees with high response thresholds are more likely to forage for nectar. There is an associated genetic component to sucrose response thresholds and forage choice such that bees selected to hoard high quantities of pollen have low response thresholds and bees selected to hoard low quantities of pollen have higher response thresholds. The number of larvae in colonies affects the number of bees foraging for pollen. Hexane-extractable compounds from the surface of larvae (brood pheromone) significantly increase the number of pollen foragers. We tested the hypothesis that brood pheromone decreases the sucrose response threshold of bees, to suggest a pheromone- modulated sensory-physiological mechanism for regulating foraging division of labor. Brood pheromone significantly decreased response thresholds as measured in the proboscis extension response assay, a response associated with pollen foraging. A synthetic blend of honeybee brood pheromone stimulated and released pollen foraging in foraging bioassays. Synthetic brood pheromone had dose-dependent effects on the modulation of sucrose response thresholds. We discuss how brood pheromone may act as a releaser of pollen foraging in older bees and a primer pheromone on the development of response thresholds and foraging ontogeny of young bees. Received: 24 May 2000 / Revised: 26 September 2000 / Accepted: 15 October 2000     

The regulation of pollen foraging by honey bees: how foragers assess the colony's need for pollen

Summary The honey bee colony presents a challenging paradox. Like an organism, it functions as a coherent unit, carefully regulating its internal milieu. But the colony consists of thousands of loosely assembled individuals each functioning rather autonomously. How, then, does the colony acquire the necessary information to organize its work force? And how do individuals acquire information about specific colony needs, and thus know what tasks need be performed? I address these questions through experiments that analyze how honey bees acquire information about the colony's need for pollen and how they regulate its collection. The results demonstrate features of the colony's system for regulating pollen foraging: (1) Pollen foragers quickly acquire new information about the colony's need for pollen. (2) When colony pollen stores are supplemented, many pollen foragers respond by switching to nectar foraging or by remaining in the hive and ceasing to forage at all. (3) Pollen foragers do not need direct contact with pollen to sense the colony's change of state, nor do they use the odor of pollen as a cue to assess the colony's need for pollen. (4) Pollen foragers appear to obtain their information about colony pollen need indirectly from other bees in the hive. (5) The information takes the form of an inhibitory cue. The proposed mechanism for the regulation of pollen foraging involves a hierarchical system of information acquisition and a negative feedback loop. By taking advantage of the vast processing capacity of large numbers of individuals working in parallel, such a system of information acquisition and dissemination may be ideally suited to promote efficient regulation of labor within the colony. Although each individual relies on only limited, local information, the colony as a whole achieves a finely-tuned response to the changing conditions it experiences.     

Individual-level patterns of division of labor in honeybees highlight flexibility in colony-level developmental mechanisms

Honeybee division of labor (DOL) has become a model system for exploring the genetic basis of complex traits and phenotypic plasticity. Although many highly informative behavioral studies have been conducted on this topic (both at the cohort and individual levels), most studies have focused on a few behavioral acts, such as the age of first foraging. Few studies have recorded large numbers of relatively complete individual-level patterns of DOL. Such fine-scale patterns would lay the foundation for rigorous molecular analyses of this phenomenon and allow us to differentiate between competing mechanistic models of DOL. Here, we record over 100 individual-level DOL patterns of bees living under natural conditions. We found that the transitions between castes (polyphenism states) are often gradual, with bees being in multiple castes at once. This is contrary to the traditional view that changes are abrupt. We also found that bees often skip castes, a key prediction of a recent model of DOL. We further confirm variation in the rate at which bees pass through castes and the age of first foraging. Taken together, these results greatly improve our understanding of this model system and allow for a strong revision of current models of honeybee DOL.