The functional organization of resin work in honeybee colonies

Resin is an important building material in the nests of honeybees, but little is known about how it is handled within the nest and how its collection is controlled. We studied the functional organization of resin work to better understand how a colony adaptively controls its intake of resin. Two hypotheses have been proposed for how resin collectors stay informed of the need for additional resin: (1) the unloading difficulty hypothesis (resin need is sensed indirectly by the unloading delay) and (2) the caulking activity hypothesis (resin need is sensed directly while engaged in using resin). A falsifiable prediction of the latter hypothesis, but not of the former, is that resin collectors not only gather resin outside the hive but also regularly handle resin inside the hive (taking it from other bees and using it to caulk crevices). Consistent with this prediction are our findings that in the resin sector of a colony’s economy, unlike in the pollen, nectar, and water sectors, there is no strict division of labor between the collectors and the users of a material. Over the course of a day, bees seen collecting resin were also commonly seen using resin. Moreover, we found that the unloading locations of resin collectors are unlike those of water and nectar collectors, being deep inside the hive (at the sites of resin use) rather than at the hive entrance. This arrangement facilitates the engagement in resin use by resin collectors. We conclude that the caulking activity hypothesis is well-supported, but that the unloading difficulty hypothesis also remains viable, for we found that resin collectors experience variable delays in getting rid of their loads, from less than 15 min to more than an hour, consistent with this hypothesis. The stage is now set for experimental tests of these two hypotheses. Both may be correct, which if true will imply that social insect workers, despite their small brains, can acquire and integrate information from multiple sources to improve their knowledge of conditions within the colony.     

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.     

Influence of age polyethism on longevity of workers in social insects

Age polyethism is widespread among social insects and, as a rule, safe tasks are performed by workers earlier in life than are risky ones. Mathematical models were used to compare expected longevity of workers in colonies with and without age polyethism. The results of the models suggest that if aging does not depend on activity then age polyethism is profitable when safer tasks are performed earlier in life. If, however, aging depends on activity, age polyethism is profitable when safer tasks are performed earlier in life and if they are associated with higher aging-related mortality. On the other hand, age polyethism is not profitable if safer tasks are performed later in life, and if they are associated with lower aging-related mortality. Furthermore, if there is no aging, then age polyethism does not bring any benefits. Electronic supplementary material to this paper can be obtained by using the Springer Link server located at http://dx.doi.org/10.1007/s00265-001-0429-z     

The role of age in temporal polyethism in a primitively eusocial wasp

The relation of age to division of labor was assessed in a primitively eusocial wasp, Ropalidia marginata. The performance of four functionally significant tasks was analyzed. It was found that age has a definite correlation with division of labor, since wasps performed tasks in a distinct sequence in their life with successive tasks being initiated at significantly older ages. Age of a wasp was measured in absolute terms and also relative to other individuals in the colony. Probability of performance of a given task relative to other tasks (PTP) and absolute rates at which tasks were performed per unit time (FTP) both showed clear age-dependent patterns, confirming the association of age with division of labor. The proportion of variance explained for both PTP and FTP was significantly higher with relative age than with absolute age. Interindividual interactions were found to be a potential mechanism through which wasps can determine their relative age. The advantages of work organization depending on relative age and the constraints imposed by absolute age are discussed. Received: 2 April 1997 / Accepted after revision: 20 July 1997     

An equilibrium theory of queen production in honeybee colonies preparing to swarm

Summary An equilibrium model is developed which seeks to explain the regulation of queen rearing in honeybee colonies preparing to swarm. The model postulates that there is a balance between nurse bees becoming inhibited from queen rearing and nurses losing their inhibition, and that whether a colony does or does not rear queens reflects the equilibrium percentage of inhibited nurses. This model leads to a quantitative prediction about the size of a conoly's nurse population at which queen rearing should start. Comparing the model's predictions with empirical observations pinpoints data needed for a more complete explanation of control of queen rearing. In particular, the model suggests a central regulatory role for density-dependent changes in the behaviors involved in queen substance dispersal.     

Role of esters in egg removal behaviour in honeybee (Apis mellifera) colonies

In queen-right honeybee colonies workers detect and eat the vast majority of worker-laid eggs, a behaviour known as worker policing. However, if a colony becomes permanently queen-less then up to 25% of the worker population develops their ovaries and lay eggs, which are normally reared into a final batch of males. Ovary development in workers is accompanied by changes in the chemical secretion of the Dufour's gland with the production of queen-like esters. We show that ester production increases with the period that the colony is queen-less. The increased ester production also corresponds to an increase in persistence of worker-laid eggs in queen-right colonies, since the esters somehow mask the eggs true identity. However, in a rare queen-less colony phenotype, workers always eat eggs indiscriminately. We found that the egg-laying workers in these colonies were unusual in that they were unable to produce esters. This apparently maladaptive egg eating behaviour is also seen in queen-less colonies prior to the appearance of egg-laying workers, a period when esters are also absent. However, the indiscriminate egg eating behaviour stops with the appearance of ester-producing egg-laying workers. These observations suggest that esters are providing some contextual information, which affects the egg eating behaviour of the workers.     

Within-nest temporal polyethism in the honey bee

A well-regulated division of labor has been one of the core adaptations leading to the success of the social insects. Honeybee division of labor has been classically viewed as a sequence of age-related changes in task performance. Kolmes questioned this view arguing that his studies did not support the existence of any age-related within-nest specialization. To resolve this controversy, Kolmes and Seeley conducted a joint study with mixed results. They found support for a cell cleaning caste, but diverged on whether their results supported distinct nursing and middle age castes. In this paper, I follow up on their work to resolve the question of caste number in within-nest honey bees. To determine whether nurses (typically aged 4–12 days) and middle-aged bees (aged 12–20 days) have distinct task repertoires, I conducted focal animal observations on a large number of workers in both age groups working within the same nests at the same time. The results support their being two castes of within-nest bees. Young bees specialized on brood care tasks, while middle-aged bees specialized on nectar processing and nest maintenance. Middle-aged bees were observed caring for brood in less than 1% of the observations. Moreover, both castes exhibited movement patterns that correspond to the traditional view that nurses stay within the broodnest, while middle-aged bees move around a great deal in search of work throughout the nest. A review of studies conducted since the debate of Seeley and Kolmes supports the reliability of these results. This work has relevance for proximate models of temporal polyethism, as it is often assumed by such models that there is only one within-nest caste in the honeybee.     

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.     

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.     

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     

Effect of queen quality on interactions between workers and dueling queens in honeybee (Apis mellifera L.) colonies

The fitness of a social insect colony depends greatly on the quality (i.e., mating ability, fecundity, and offspring viability) of its queen(s). In honeybees, there is marked variation in the quality of young queens that compete in a series of lethal duels to replace a colonys previous queen. Workers interact with queens during these duels and could increase their inclusive fitness by biasing the outcomes of the duels in favor of high-quality queens. We predicted that workers will have more antagonistic interactions (chasing, grabbing, clamping) and fewer beneficent interactions (feeding, grooming) with low-quality than high-quality queens. To test this prediction, we reared queens from 0-day-old, 2-day-old, and 3-day-old worker larvae in observation colonies undergoing queen replacement, thus producing high-quality, low-quality, and very low-quality queens, respectively. Immediately after each queen emerged, we observed her for 1 h to record her interactions with the workers. Subsequent morphological measurement of the queens confirmed that initial larval age had a significant effect on queen quality. However, there was no consistent effect of queen quality on the rates of worker–queen interactions, thus falsifying our hypothesis. The mean power of our tests was high (0.599), therefore the probability of a type II error (a false negative) is low. We conclude that if workers actively select high-quality queens, then they do so prior to queen duels, during queen development. We suggest that each worker–queen interaction has a distinct adaptive significance rather than forming a suite of behavior that favors particular queens (e.g., chasing repels any queen that approaches a queen cell, thus protecting all queen cells from destruction).Communicated by M. Giurfa     

Ovariole number—a predictor of differential reproductive success among worker subfamilies in queenless honeybee (Apis mellifera L.) colonies

A honeybee queen normally mates with 10–20 drones, and reproductive conflicts may arise among a colony’s different worker patrilines, especially after a colony has lost its single queen and the workers commence egg laying. In this study, we employed microsatellite markers to study aspects of worker reproductive competition in two queenless Africanized honeybee colonies. First, we determined whether there was a bias among worker patrilines in their maternity of drones and, second, we asked whether this bias could be attributed to differences in the degree of ovary activation of workers. Third, we relate these behavioral and physiological factors to ontogenetic differences between workers with respect to ovariole number. Workers from each of three (colony A) and one (colony B) patrilineal genotypes represented less than 6% of the worker population, yet each produced at least 13% of the drones in a colony, and collectively they produced 73% of the drones. Workers representing these genotypes also had more developed follicles and a greater number of ovarioles per ovary. Across all workers, ovariole development and number were closely correlated. This suggests a strong effect of worker genotype on the development of the ovary already in the postembryonic stages and sets a precedent to adult fertility, so that “workers are not born equal”. We hypothesize a frequency-dependent or “rare patriline” advantage to queenless workers over the parentage of males and discuss the maintenance of genetic variance in the reproductive capacity of workers.Electronic supplementary material Supplementary material is available for this article at and is accessible for authorized users.     

Optimal timing of comb construction by honeybee (Apis mellifera) colonies: a dynamic programming model and experimental tests

Honeybee colonies, like organisms, should exhibit optimal design in their temporal pattern of resource allocation to somatic structures. A vital colony structure is the comb which stores honey for overwinter survival. However, the timing of comb construction poses a dilemma to a colony attempting to maximize its honey reserves. On the one hand, plenty of empty comb is needed for efficient exploitation of temporally unpredictable flower blooms. On the other hand, because comb is made from energetically expensive wax, its construction too early or in excessive amounts will reduce the amount of honey available for winter thermoregulation and brood-rearing. A dynamic optimization model concludes that colonies should add new comb only when they have filled their old comb with food and brood above a threshold level. The threshold increases with time until, at the end of the season, building is never an optimal behavior. The temporal pattern of construction predicted by the model – pulses of building coincident with periods of nectar intake and comb fullness – matches that seen in an actual colony observed over the course of an entire foraging season. When nectar sources are rich but temporally clumped, the model also predicts that bees should be sensitive to nectar intake, employing much higher thresholds on days when nectar is not available than on days when it is. Even under poorer and more dispersed nectar regimes, little fitness cost is paid by colonies replacing the optimal strategy with a simpler rule of thumb calling for new construction only when two conditions are met: (1) a fullness threshold has been exceeded, and (2) nectar is currently being collected. Experiments demonstrate that colonies do in fact use such a rule of thumb to control the onset of construction. However, once they have begun building, the bees continue as long as nectar collection persists, regardless of changes in comb fullness. Thus the onset and duration of comb-building bouts appear to be under partially independent control. Received: 30 October 1998 / Received in revised form: 14 December 1998 / Accepted: 16 January 1999     

Adaptive significance of phytoplankton stickiness with emphasis on the diatom Skeletonema costatum

Diatom aggregate formation was analyzed using coagulation theory. Population dynamics models show that coagulation has an important impact on species succession during diatom blooms. When different species collide and form mixed aggregates this process causes interspecific interference competition within the diatom community. The outcome can be predicted by a set of simple differential equations. For a twospecies system the equations reduce to the Lotka-Volterra two-species competition model. The outcome of this interference competition depends on species-specific growth rates, cell sizes, stickiness and on the species composition of the seeding populations of a bloom. Due to mutual flocculation some species may disappear from the environment. Small and fast growing diatoms are favoured by high stickiness coefficients. The impact of stickiness on species succession was found to be most pronounced in eutrophic and hydrographically isolated environments. The sticking properties of the diatom Skeletonema costatum are discussed in an evolutionary context; we suggest that mutual coagulation increases the abundance of S. costatum relative to other diatom species in coastal areas. The model was tested on field data, and the predicted dynamics of a spring bloom was very similar to that observed.     

Dominance and polyethism in the eusocial wasp Mischocyttarus mastigophorus (Hymenoptera: Vespidae)

Dominance interactions affected patterns of non-reproductive division of labor (polyethism) in the eusocial wasp Mischocyttarus mastigophorus. Socially dominant individuals foraged for food (nectar and insect prey) at lower rates than subordinate individuals. In contrast, dominant wasps performed most of the foraging for the wood pulp used in nest construction. Social dominance also affected partitioning of materials collected by foragers when they returned to the nest. Wood pulp loads were never shared with nest mates, while food loads, especially insect prey, were often partitioned with other wasps. Dominant individuals on the nest were more likely to take food from arriving foragers than subordinate individuals. The role of dominance interactions in regulating polyethism has evolved in the eusocial paper wasps (Polistinae). Both specialization by foragers and task partitioning have increased from basal genera (independent-founding wasps, including Mischo-cyttarus spp.) to more derived genera (swarm-founding Epiponini). Dominance interactions do not regulate forager specialization or task partitioning in epiponines. I hypothesize that these changes in polyethism were enabled by the evolution of increased colony size in the Epiponini. Received: 8 December 1997 / Accepted after revision: 28 March 1998     

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.     

Pathogen-associated self-medication behavior in the honeybee Apis mellifera

Honeybees, Apis mellifera, have several prophylactic disease defense strategies, including the foraging of antibiotic, antifungal, and antiviral compounds of plant products. Hence, honey and pollen contain many compounds that prevent fungal and bacterial growth and inhibit viral replication. Since these compounds are also fed to the larvae by nurse bees, they play a central role for colony health inside the hive. Here, we show that honeybee nurse bees, infected with the microsporidian gut parasite Nosema ceranae, show different preferences for various types of honeys in a simultaneous choice test. Infected workers preferred honeys with a higher antibiotic activity that reduced the microsporidian infection after the consumption of the honey. Since nurse bees feed not only the larvae but also other colony members, this behavior might be a highly adaptive form of therapeutic medication at both the individual and the colony level.