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     

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.     

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     

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     

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.     

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 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     

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.     

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     

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 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.     

Manuscript in preparation for <Emphasis Type="Italic">Behavioral Ecology and Sociobiology</Emphasis> Bumble bee pollen foraging regulation: role of pollen quality,storage levels,and odor

The regulation of protein collection through pollen foraging plays an important role in pollination and in the life of bee colonies that adjust their foraging to natural variation in pollen protein quality and temporal availability. Bumble bees occupy a wide range of habitats from the Nearctic to the Tropics in which they play an important role as pollinators. However, little is known about how a bumble bee colony regulates pollen collection. We manipulated protein quality and colony pollen stores in lab-reared colonies of the native North American bumble bee, Bombus impatiens. We debut evidence that bumble bee colony foraging levels and pollen storage behavior are tuned to the protein quality (range tested: 17–30% protein by dry mass) of pollen collected by foragers and to the amount of stored pollen inside the colony. Pollen foraging levels (number of bees exiting the nest) significantly increased by 55%, and the frequency with which foragers stored pollen in pots significantly increased by 233% for pollen with higher compared to lower protein quality. The number of foragers exiting the nest significantly decreased (by 28%) when we added one pollen load equivalent each 5 min to already high intranidal pollen stores. In addition, pollen odor pumped into the nest is sufficient to increase the number of exiting foragers by 27%. Foragers directly inspected pollen pots at a constant rate over 24 h, presumably to assess pollen levels. Thus, pollen stores can act as an information center regulating colony-level foraging according to pollen protein quality and colony need. An erratum to this article can be found at     

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.     

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     

Genetic determination of nectar foraging,pollen foraging,and nest-site scouting in honey bee colonies

Summary Allozyme analyses of honey bee workers revealed significant differences in the intracolonial subfamily composition of groups of nectar foragers, pollen foragers, and nest-site scouts. These differences demonstrate that colony genetic structure influences the division of labor among older foraging-age bees just as it does for younger workers. The maintenance of genetic variability for the behavior of individual workers and its possible effects on the organization of colonies are discussed.     

Regulation of honey bee division of labor by colony age demography

The age at which worker honey bees begin foraging varies under different colony conditions. Previous studies have shown that juvenile hormone (JH) mediates this behavioral plasticity, and that worker-worker interactions influence both JH titers and age at first foraging. These results also indicated that the age at first foraging is delayed in the presence of foragers, suggesting that colony age demography directly influences temporal division of labor. We tested this hypothesis by determining whether behavioral or physiological development can be accelerated, delayed, or reversed by altering colony age structure. In three out of three trials, earlier onset of foraging was induced in colonies depleted of foragers compared to colonies depleted of an equal number of bees across all age classes. In two out of three trials, delayed onset of foraging was induced in colonies in which foragers were confined compared to colonies with free-flying foragers. Finally, in three out of three trials, both endocrine and exocrine changes associated with reversion from foraging to brood care were induced in colonies composed of all old bees and devoid of brood; JH titers decreased and hypopharyngeal glands regenerated. These results demonstrate that plasticity in age-related division of labor in honey bee colonies is at least partially controlled by social factors. The implications of these results are discussed for the recently developed ‘‘activator-inhibitor” model for honey bee behavioral development. Received: 8 November 1995/Accepted after revision: 10 May 1996     

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.     

Heritable variation in learning performance affects foraging preferences in the honey bee (Apis mellifera)

There has now been an abundance of research conducted to explore genetic bases that underlie learning performance in the honey bee (Apis mellifera). This work has progressed to the point where studies now seek to relate genetic traits that underlie learning ability to learning in field-based foraging problems faced by workers. Accordingly, the focus of our research is to explore the correlation between laboratory-based performance using an established learning paradigm and field-based foraging behavior. To evaluate learning ability, selected lines were established by evaluating queens and drones in a proboscis extension reflex (PER) conditioning procedure to measure learning in a laboratory paradigm—latent inhibition (LI). Hybrid queens were then produced from our lines selected for high and low levels of LI and inseminated with semen from many drones chosen at random. The genetically diverse worker progeny were then evaluated for expression of LI and for preference of pollen and/or nectar during foraging. Foragers from several different queens, and which had resulted from fertilization by any of several different drone fathers, were collected as they returned from foraging flights and analyzed for pollen and nectar contents. They were subsequently evaluated for expression of LI. Our research revealed that pollen foragers exhibited stronger learning, both in the presence (excitatory conditioning) and absence (LI) of reinforcement. The heightened overall learning ability demonstrated by pollen foragers suggests that pollen foragers are in general more sensitive to a large number of environmental stimuli. This mechanism could contribute toward explanations of colony-level regulation of foraging patterns among workers.Communicated by R. Page     

Condition-dependent response to changes in pollen stores by honey bee (Apis mellifera) colonies with different parasitic loads

The impact of a parasitic infestation may be influenced by nutritional state, in both individuals and colonies. This study examined the interaction between pollen storage and the effects of an infestation by the mite, Varroa jacobsoni Oudemans, in colonies of the honey bee, Apis mellifera L. We manipulated the pollen storage and mite infestation levels of colonies, and measured pollen foraging and brood rearing. Increased pollen stores decreased both the number of pollen foragers and pollen load size, while initially at least foragers from colonies with moderate infestations carried smaller pollen loads than those from lightly infested colonies. Over the course of the experiment, all colonies significantly increased pollen-foraging rates and pollen consumption, which was presumably a seasonal effect. Lightly infested colonies exhibited a larger increase in pollen forager number than moderately infested colonies, suggesting that more intense mite infestations compromised forager recruitment. Brood production was not affected by the addition of pollen, but moderately infested colonies were rearing significantly less brood by the end of the experiment than lightly infested colonies. Furthermore, the efficiency with which colonies converted pollen to brood decreased as the pollen storage level decreased and the infestation level increased. The results of this study may indicate that honey bee colonies adaptively alter brood-production efficiency in response to parasitic infestations and seasonal changes. Received: 3 May 1999 / Received in revised form: 14 September 1999 / Accepted: 25 September 1999