Labor In Honey Bees Research Articles

Learning, aging and division of labour in honey bees

Learning, aging and division of labour in honey bees

Meta-analysis of genome-wide expression patterns associated with behavioral maturation in honey bees

BackgroundThe information from multiple microarray experiments can be integrated in an objective manner via meta-analysis. However, multiple meta-analysis approaches are available and their relative strengths have not been directly compared using experimental data in the context of different gene expression scenarios and studies with different degrees of relationship. This study investigates the complementary advantages of meta-analysis approaches to integrate information across studies, and further mine the transcriptome for genes that are associated with complex processes such as behavioral maturation in honey bees. Behavioral maturation and division of labor in honey bees are related to changes in the expression of hundreds of genes in the brain. The information from various microarray studies comparing the expression of genes at different maturation stages in honey bee brains was integrated using complementary meta-analysis approaches.ResultsComparison of lists of genes with significant differential expression across studies failed to identify genes with consistent patterns of expression that were below the selected significance threshold, or identified genes with significant yet inconsistent patterns. The meta-analytical framework supported the identification of genes with consistent overall expression patterns and eliminated genes that exhibited contradictory expression patterns across studies. Sample-level meta-analysis of normalized gene-expression can detect more differentially expressed genes than the study-level meta-analysis of estimates for genes that were well described by similar model parameter estimates across studies and had small variation across studies. Furthermore, study-level meta-analysis was well suited for genes that exhibit consistent patterns across studies, genes that had substantial variation across studies, and genes that did not conform to the assumptions of the sample-level meta-analysis. Meta-analyses confirmed previously reported genes and helped identify genes (e.g. Tomosyn, Chitinase 5, Adar, Innexin 2, Transferrin 1, Sick, Oatp26F) and Gene Ontology categories (e.g. purine nucleotide binding) not previously associated with maturation in honey bees.ConclusionThis study demonstrated that a combination of meta-analytical approaches best addresses the highly dimensional nature of genome-wide microarray studies. As expected, the integration of gene expression information from microarray studies using meta-analysis enhanced the characterization of the transcriptome of complex biological processes.

TaskSelSim: a model of the self-organization of the division of labour in honeybees

We here describe a novel multi-agent model of the decentralized task selection process in honeybee colonies. The model is based on individual behavioural programs represented as hierarchical finite state automatons. We successfully simulated empirical experiments (with real honeybees) using the model. We shed more light on task specialization and polyethism in honeybees by modelling the heterogeneous environment that emerges over time inside the colony and by considering the changing differences in stimuli strength in each small area of the hive. Our simulation experiments presented here investigate the model's reaction to changing values in crucial model parameters and investigate the stability of the predicted colony behaviours.

The influence of the vibration signal on worker interactions with the nest and nest mates in established and newly founded colonies of the honey bee, Apis mellifera

Honey bees adjust cooperative activities to colony needs, based in part on information acquired through interactions with the nest and nest mates. We examined the role of the vibration signal in these interactions by investigating the influence of the signal on the movement rates, cell inspection activity, and trophallaxis behavior of workers in established and newly founded colonies of the honey bee, Apis mellifera. Compared to non-vibrated control bees, vibrated recipients in both colony types exhibited increased movement through the nest and greater cell inspection activity, which potentially increased contact with stimuli that enhanced task performance. Also, compared to controls, recipients in both colony types showed increased rates of trophallactic interactions and spent more time engaged in trophallaxis, which potentially further increased the acquisition of information about colony needs. The vibration signal may therefore help to organize labor in honey bees in part by increasing the rate at which workers obtain information about their colony. Vibrated recipients in the established and newly founded colonies did not differ in any aspect of behavior examined, suggesting that colony developmental state did not influence the degree to which individual workers responded to the signal. However, previous work has demonstrated that newly founded colonies have increased levels of vibration signal behavior. Thus, the vibration signal may help to adjust worker activity to colony conditions partly by stimulating greater numbers of bees to acquire information about colony needs, rather than by altering the level at which individual recipients react to the signal.

Phototactic behaviour correlates with gustatory responsiveness in honey bees ( Apis mellifera L.)

The response threshold hypothesis of division of labour in honey bees assumes that individuals differ in their responsiveness to different stimulus modalities. However, previous experiments have shown that responsiveness to gustatory stimuli correlates with responsiveness to odours, pollen and tactile stimuli. Evaluation of these stimuli involves sensory receptors on the antenna. We tested whether responsiveness to gustatory stimuli correlates with responsiveness to visual stimuli in a phototaxis experiment, which is independent of antennal input. Gustatory responsiveness was measured using the proboscis extension response to antennal stimulation with water and different sucrose concentrations. Phototaxis was quantified by measuring the walking times a bee needed to reach light sources of different intensities. Walking behaviour in the darkness was measured to test for differences in locomotor behaviour. The walking time towards a light stimulus, the path length, and the walking speed depended on the intensity of the light stimulus. Responsiveness to visual stimuli correlated significantly with gustatory responsiveness. Bees displaying a high gustatory responsiveness were also very sensitive to light. Locomotor activity did not correlate with gustatory responsiveness. This shows that gustatory responsiveness is a good indicator of sensitivity for visual stimuli, which are not perceived by the antenna.

Worker nutrition and division of labour in honeybees

We determined whether there is an association between nutritional state (as indicated by stored abdominal lipid amounts) and division of labour in the honeybee, Apis mellifera. We found that foragers (typically older bees) had lower lipid amounts than did nurses (typically young bees). Results from experimental colonies that contained nurses and foragers of the same age showed that the lipid decline in foragers was not attributable to age. Analysis of bees with different amounts of foraging experience revealed little effect of the act of foraging on lipid stores. Lipid levels were low even on the first day of foraging, suggesting that the decline in stored lipid precedes the onset of foraging. We also found that bees that revert from foraging to nursing did not regain their lipid stores, indicating that high lipid stores are not required to sustain brood care behaviour. This demonstration of a robust association between reduced lipid stores and the transition to foraging suggests that worker nutritional state may be involved in the regulation of division of labour in honeybee colonies.

The vibration signal, modulatory communication and the organization of labor in honey bees, Apis mellifera

Cooperative activities in honey bee colonies involve the coordinated interactions of multiple workers that perform different, but interrelated tasks. A central objective in the study of honey bee sociality therefore is to understand the communication signals used to integrate behavior within and among worker groups. This paper focuses on the role of the in organizing labor in honey bee colonies. The vibration signal functions as a type of communication signal. It is directed toward diverse recipients, causes a non-specific increase in activity that may alter responsiveness to a wide array of stimuli, and thus may influence the performance of many different tasks simultaneously. We review the empirical evidence that the signal is involved in coordinating at least three colony-level activities: food collection and foraging-dependent tasks, queen behavior during swarming and queen replacement, and house hunting by honey bee swarms. Signals that function like the vibration signal may be widespread in highly social insects and social animals in general, and may help to fine-tune the collective decision-making processes that underlie cooperative actions in a wide array of species. vibration signal / modulatory communication / collective decision making / Apis mellifera / multimodal signals

Juvenile hormone and circadian locomotor activity in the honey bee Apis mellifera

Age-related division of labor in honeybees is associated with plasticity in circadian rhythms. Young nest bees care for brood around the clock with no circadian rhythms while older foragers have strong circadian rhythms that are used for sun compass navigation and for timing visits to flowers. Since juvenile hormone (JH) is involved in the coordination of physiological and behavioral processes underlying age-related division of labor in honey bees, we tested the hypothesis that JH influences the ontogeny of circadian rhythms and other clock parameters in young worker bees. Treatments with the JH analog methoprene or allatectomy did not influence the onset of rhythmicity, overall locomotor activity, or the free-running period of rhythmic locomotor behavior. There were, however, significant differences in the onset of rhythmicity, overall locomotor activity, and longevity between bees from different source colonies, suggesting that there is significant genetic variation for these traits. Our results suggest that JH does not coordinate all aspects of division of labor in bees and that coordination of task performance with circadian rhythms is probably mediated by other regulatory systems.

Changes in period mRNA levels in the brain and division of labor in honey bee colonies.

Previous research showed that age-related division of labor in honey bees is associated with changes in activity rhythms; young adult bees perform hive tasks with no daily rhythms, whereas older bees forage with strong daily rhythms. We report that this division of labor is also associated with differences in both circadian rhythms and mRNA levels of period, a gene well known for its role in circadian rhythms. The level of period mRNA in the brain oscillated in bees of all ages, but was significantly higher at all times in foragers. Elevated period mRNA levels cannot be attributed exclusively to aging, because bees induced to forage precociously because of a change in social environment had levels similar to normal age foragers. These results extend the regulation of a "clock gene" to a social context and suggest that there are connections at the molecular level between division of labor and chronobiology in social insects.

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.

Biogenic amines and division of labor in honey bee colonies

Brain levels of dopamine, serotonin, and octopamine were measured in relation to both age-related division of labor and inter-individual differences in task specialization independent of age in honey bee colonies. The only differences among similarly aged bees performing different tasks were significantly lower levels of dopamine in food storers than comb builders and significantly lower levels of octopamine in soldiers than foragers, but soldiers also were slightly younger than foragers. Differences associated with age-related division of labor were stronger. Older bees, notably foragers, had significantly higher levels of all three amines than did younger bees working in the hive. Using social manipulations to unlink chronological age and behavioral status, octopamine was found to exhibit the most robust association between behavior and amine level, independent of age. Octopamine levels were significantly lower in normal-age nurses versus precocious foragers and overage nurses versus normal-age foragers, but not different in reverted nurses versus reversion colony foragers. Dopamine levels were significantly lower in normal-age nurses versus precocious foragers, but higher in reverted nurses versus reversion colony foragers. Serotonin levels did not differ in any of these comparisons. These correlative results suggest that octopamine is involved in the regulation of age-related division of labor in honey bees.

Biogenic amines and division of labor in honey bee colonies: behaviorally related changes in the antennal lobes and age-related changes in the mushroom bodies.

Levels of the biogenic amines dopamine, serotonin, and octopamine were measured in different brain regions of adult worker honey bees as a function of age-related division of labor, using social manipulations to unlink age and behavioral state. In the antennal lobes, foragers had higher levels of all three amines than nurses, regardless of age. Differences were larger for octopamine than serotonin or dopamine. In the mushroom bodies, older bees had higher levels of all three amines than younger bees, regardless of behavioral state. These correlative results suggest that increases in octopamine in the antennal lobes may be particularly important in the control of age-related division of labor in honey bees.

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

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

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.

Selective neuroanatomical plasticity and division of labour in the honeybee.

The mushroom bodies in the protocerebrum are believed to be the structures of the insect brain most closely associated with higher-order sensory integration and learning. Drosophila melanogaster mutants with olfactory learning deficits have anatomically abnormal mushroom bodies or altered patterns of gene expression in mushroom body neurons. In addition, anatomical reorganization of the mushroom bodies occurs in adult flies, and possibly in adult honeybees; disturbance of electrical activity in this region disrupts memory formation in honeybees. Little is known, however, about the relationship of naturally occurring anatomical changes in the mushroom bodies to naturally occurring behavioural plasticity. We now report that age-based division of labour in adult worker honeybees (Apis mellifera) is associated with substantial changes in certain brain regions, notably the mushroom bodies. Moreover, these striking changes in brain structure are dependent, not on the age of the bee, but on its foraging experience, thus demonstrating a robust anatomical plasticity associated with complex behaviour in an adult insect.

Individual involvement in queen-attending of worker honeybees

Studies on the division of labour in honeybees have mainly been focused on behaviour that is performed by workers of different ages or genetic background. However, little is yet known about behavioural differenceswithin groups of honeybee workers. The aim of this paper is to establish whether queen attendance in honeybee colonies is a function of “specialists” among the workers within one age cohort in colonies with a natural number of partilines. Furthermore, I want to assess whether the duration of contact of individual workers with the queen is correlated with their involvement in other behaviour and, in the long term, with their differentiation into laying and non-laying workers after the colony becomes queenless.

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

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.

Defensive behaviour and the division of labour in the African honeybee (Apis mellifera scutettata)

1. Venom protein release and alarm pheromone production by African worker honey-bees (Apis mellifera scutellata) were documented with respect to adult age. Behavioural assays were used to explore relationships among venom protein release, the alarm pheromone bouquets and the recruitability of bees to colony defence as a function of age. 2. The concentration of venom protein released by young worker honeybees is low (10–30 μg/bee), gradually increasing with age, reaching a plateau of 60 μg/bee at 17 days and remaining at this value in older bees. 3. Nine alarm pheromones from the sting were identified and analysed gas chromatographically. Of these, only isopentyl acetate, isopentyl alcohol, benzyl alcohol and n-hexyl acetate showed concentration profiles that clearly differed with age. The mandibular gland alarm pheromone 2-heptanone, had a reasonably well-defined concentration profile as related to age. 4. Behavioural assays showed: (1) more bees of all ages responded to an isolated sting (sting alarm pheromones) than to (2) an isolated pair of mandibular glands (2-heptanone). A response equivalent to (1) occurred when both a sting and a pair of mandibular glands were presented together. Older bees (15–25 days old) responded more readily to the donor stings, mandibular glands and stings and mandibular glands together of 15–25 day old bees than did younger bees. The responses of older bees (25 days old) were more rapid and of longer duration than of younger bees. 5. Our combined data on the production of venom protein, alarm signals and their efficacy in recruitment; and the latency and duration of worker responses can be correlated with age. The defensive capacity of African worker bees is one which develops in relation to age and is consistent with defence being yet another element associated with the division of labour in honeybees.

Regulation of honey bee age polyethism by juvenile hormone

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.

Factors determining temporal division of labor in honeybees

Honeybee workers perform tasks in an age-related sequence during their lifetimes, with young workers generally performing hive duties and older workers guarding the entrance. The relationship between the timing of brood care and foraging and the colony characteristics of worker population, age distribution, and brood care were examined in order to determine the influence of colony growth on the ontogeny of worker activities. Foraging age was strongly correlated with colony population but not with age distribution or brood area. The age when workers cared for brood was weakly correlated with colony population and not correlated with age distribution or brood area. The results suggest that the ages when tasks are performed depend in part on colony population and less on age distribution and brood area.