Octopamine influences division of labor in honey bee colonies

Forager honey bees have higher brain levels of octopamine than do bees tending larvae in the hive. To test the hypothesis that octopamine influences honey bee division of labor we treated bees orally with octopamine or its immediate precursor tyramine and determined whether these treatments increased the probability of initiating foraging. Octopamine treatment significantly elevated levels of octopamine in the brain and caused a significant dose-dependent increase in the number of new foragers. This effect was seen for precocious foragers in single-cohort colonies and foragers in larger colonies with more typical age demographies. Tyramine treatment did not increase the number of new foragers, suggesting that octopamine was exerting a specific effect. Octopamine treatment was effective only when given to bees old enough to forage, i.e., older than 4 days of age. Treatment when bees were 1-3 days of age did not cause a significant increase in the number of new foragers when the bees reached the minimal foraging age. These results demonstrate that octopamine influences division of labor in honey bee colonies. We speculate that octopamine is acting in this context as a neuromodulator.     

Octopamine modulates responsiveness to foraging-related stimuli in honey bees (Apis mellifera)

The biogenic amine neurochemical octopamine is involved in the onset of foraging behaviour in honey bees. We tested the hypothesis that octopamine influences honey bee behavioural development by modulating responsiveness to task-related stimuli. We examined the effect of octopamine treatment on responsiveness to brood pheromone (an activator of foraging) and to the presence of older bees in the colony (an inhibitor of foraging in young bees). Octopamine treatment increased responsiveness to brood pheromone and decreased responsiveness to social inhibition. These results identify octopamine both as an important source of variation in response thresholds and as a modulator of pheromonal communication in insect societies. We speculate that octopamine plays more than one role in the organisation of behavioural development indicating a very high level of integration between the neurochemical system and the generation of complex behaviour.     

Biogenic amines in the antennal lobes and the initiation and maintenance of foraging behavior in honey bees

Previous findings showed that high levels of octopamine and serotonin in the antennal lobes of adult worker honey bees are associated with foraging behavior, and octopamine treatment induces precocious foraging. To better characterize the relationship between amines and foraging behavior in honey bees, we performed a detailed correlative analysis of amine levels in the antennal lobes as a function of various aspects of foraging behavior. Flight activity was measured under controlled conditions in a large outdoor flight cage. Levels of octopamine in the antennal lobes were found to be elevated immediately subsequent to the onset of foraging, but they did not change as a consequence of preforaging orientation flight activity, diurnal pauses in foraging, or different amounts of foraging experience, suggesting that octopamine helps to trigger and maintain the foraging behavioral state. In contrast, levels of serotonin and dopamine did not show changes that would implicate them as either causal agents of foraging, or as neurochemical systems affected by the act of foraging. Serotonin treatment had no effect on the likelihood of foraging. These results provide further support for the hypothesis that an increase in octopamine levels in the antennal lobes plays a causal role in the initiation and maintenance of the behavioral state of foraging, and thus is involved in the regulation of division of labor in honey bees.     

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. Accepted: 10 February 1999     

Sucrose response thresholds of honey bee (Apis mellifera) foragers are not modulated by brood ester pheromone

Division of labor is a hallmark of eusocial insects and their ecological success can be attributed to it. Honey bee division of labor proceeds along a stereotypical ontogenetic path based on age, modulated by various internal and external stimuli. Brood pheromone is a major social pheromone of the honey bee that has been shown to affect honey bee division of labor. It elicits several physiological and behavioral responses; notably, regulating the timing of the switch from performing in-hive tasks to the initiation of foraging. Additionally, brood pheromone affects future foraging choice. In honey bees, sucrose response threshold is a physiological correlate of age of first foraging and foraging choice. Brood pheromone has been shown to modulate sucrose response threshold in young bees, but its effects on sucrose response thresholds of bees in advanced behavioral states (foragers) are not known. In this study we examined the sucrose response thresholds of two different task groups, foragers (pollen and non-pollen) and non-foraging bees, in response to honey bee brood pheromone. Sucrose response thresholds were not significantly different between brood pheromone treatment and controls among both non-pollen and pollen foragers. However, the sucrose response threshold of non-foraging bees was significantly higher in the brood pheromone treatment group than in the control group. The switch to foraging task is considered a terminal one, with honey bee lifespan being determined at least partially by risks and stress accompanying foraging. Our results indicate that foragers are physiologically resistant to brood pheromone priming of sucrose response thresholds.     

Division of Labor Associated with Brood Rearing in the Honey Bee: How Does It Translate to Colony Fitness?

Division of labor is a striking feature observed in honey bees and many other social insects. Division of labor has been claimed to benefit fitness. In honey bees, the adult work force may be viewed as divided between non-foraging hive bees that rear brood and maintain the nest, and foragers that collect food outside the nest. Honey bee brood pheromone is a larval pheromone that serves as an excellent empirical tool to manipulate foraging behaviors and thus division of labor in the honey bee. Here we use two different doses of brood pheromone to alter the foraging stimulus environment, thus changing demographics of colony division of labor, to demonstrate how division of labor associated with brood rearing affects colony growth rate. We examine the effects of these different doses of brood pheromone on individual foraging ontogeny and specialization, colony level foraging behavior, and individual glandular protein synthesis. Low brood pheromone treatment colonies exhibited significantly higher foraging population, decreased age of first foraging and greater foraging effort, resulting in greater colony growth compared to other treatments. This study demonstrates how division of labor associated with brood rearing affects honey bee colony growth rate, a token of fitness.     

Inter‐individual variation in honey bee dance intensity correlates with expression of the foraging gene

Individual behavioural differences in responding to the same stimuli is an integral part of division of labour in eusocial insect colonies. Amongst honey bee nectar foragers, individuals strongly differ in their sucrose responsiveness, which correlates with strong differences in behavioural decisions. In this study, we explored whether the mechanisms underlying the regulation of foraging are linked to inter‐individual differences in the waggle dance activity of honey bee foragers. We first quantified the variation in dance activity amongst groups of foragers visiting an artificial feeder filled consecutively with different sucrose concentrations. We then determined, for these foragers, the sucrose responsiveness and the brain expression levels of three genes associated with food search and foraging; the foraging gene Amfor, octopamine receptor gene AmoctαR1 and insulin receptor AmInR‐2. As expected, foragers showed large inter‐individual differences in their dance activity, irrespective of the reward offered at the feeder. The sucrose responsiveness correlated positively with the intensity of the dance activity at the higher reward condition, with the more responsive foragers having a higher intensity of dancing. Out of the three genes tested, Amfor expression significantly correlated with dance activity, with more active dancers having lower expression levels. Our results show that dance and foraging behaviour in honey bees have similar mechanistic underpinnings and supports the hypothesis that the social communication behaviour of honey bees might have evolved by co‐opting behavioural modules involved in food search and foraging in solitary insects.     

Managing honey bees (Hymenoptera: Apidae) for greenhouse tomato pollination

Although commercially reared colonies of bumble bees (Bombus sp.) are the primary pollinator world-wide for greenhouse tomatoes (Lycopersicon esculentum Mill.) previous research indicates that honey bees (Apis mellifera L.) might be a feasible alternative or supplement to bumble bee pollination. However, management methods for honey bee greenhouse tomato pollination scarcely have been explored. We 1) tested the effect of initial amounts of brood on colony population size and flight activity in screened greenhouses during the winter, and 2) compared foraging from colonies with brood used within screened and unscreened greenhouses during the summer. Brood rearing was maintained at low levels in both brood and no-brood colonies after 21 d during the winter, and emerging honey bees from both treatments had significantly lower weights than bees from outdoor colonies. Honey bee flight activity throughout the day and over the 21 d in the greenhouse was not influenced by initial brood level. In our summer experiment, brood production in screened greenhouses neared zero after 21 d but higher levels of brood were reared in unscreened greenhouses with access to outside forage. Flower visitation measured throughout the day and over the 21 d the colonies were in the greenhouse was not influenced by screening treatment. An economic analysis indicated that managing honey bees for greenhouse tomato pollination would be financially viable for both beekeepers and growers. We conclude that honey bees can be successfully managed for greenhouse tomato pollination in both screened and unscreened greenhouses if the foraging force is maintained by replacing colonies every 3 wk.     

Primer effects of a brood pheromone on honeybee behavioural development

Primer pheromones are thought to act in a variety of vertebrates and invertebrates but only a few have been chemically identified. We report that a blend of ten fatty-acid esters found on the cuticles of honeybee larvae, already known as a kairomone, releaser pheromone and primer pheromone, also act as a primer pheromone in the regulation of division of labour among adult workers. Bees in colonies receiving brood pheromone initiated foraging at significantly older ages than did bees in control colonies in five out of five trials. Laboratory and additional field tests also showed that exposure to brood pheromone significantly depressed blood titres of juvenile hormone. Brood pheromone exerted more consistent effects on age at first foraging than on juvenile hormone, suggesting that the primer effects of this pheromone may occur via other, unknown, mechanisms besides juvenile hormone. These results bring the number of social factors known to influence honeybee division of labour to three: worker-worker interactions, queen mandibular pheromone and brood pheromone.     

Nutrition and division of labor: Effects on foraging and brain gene expression in the paper wasp Polistes metricus

Deeply conserved molecular mechanisms regulate food-searching behaviour in response to nutritional cues in a wide variety of vertebrates and invertebrates. Studies of the highly eusocial honey bee have shown that nutritional physiology and some conserved nutrient signalling pathways, especially the insulin pathway, also regulate the division of labour between foraging and non-foraging individuals. Typically, lean workers leave the nest to forage for food, and well-nourished workers perform tasks inside the nest. Here we provide the first direct test of whether similar mechanisms operate in a primitively eusocial insect in an independently evolved social lineage, the paper wasp Polistes metricus. We found that food deprivation caused reduced lipid stores and higher levels of colony and individual foraging. Individuals with greatly reduced lipid stores foraged at extremely elevated levels. In addition, brain expression of several foraging-related genes was influenced by food deprivation, including insulin-like peptide 2 (ilp2). Together with previous findings, our results demonstrate that nutrition regulates foraging division of labour in two independently evolved social insect lineages (bees and wasps), despite large differences in social organization. Our results also provide additional support for the idea that nutritional asymmetries among individuals, based on differences in nutritional physiology and expression of conserved nutrient signalling genes in the brain, are important in the division of labour in eusocial societies.     

Hygienic behavior of the honey bee (Apis mellifera) is independent of sucrose responsiveness and foraging ontogeny

Hygienic behavior in honey bees is a behavioral mechanism of disease resistance. Bees bred for hygienic behavior exhibit an increased olfactory sensitivity to odors of diseased brood, which is most likely differentially enhanced in the hygienic line by the modulatory effects of octopamine (OA), a noradrenaline-like neuromodulator. Here, we addressed whether the hygienic behavioral state is linked to other behavioral activities known to be modulated by OA. We specifically asked if, during learning trials, bees from hygienic colonies discriminate better between odors of diseased and healthy brood because of differences in sucrose (reward) response thresholds. This determination had to be tested because sucrose response thresholds are susceptible to OA modulation and may have influenced the honey bee's association of the conditioned stimulus (odor) with the unconditioned stimulus (i.e., the sucrose reward). Because the onset of first foraging is also modulated by OA, we also examined whether bees from hygienic colonies differentially forage at an earlier age compared to bees from non-hygienic colonies. Our study revealed that 1-day- and 15- to 20-day-old bees from the hygienic line do not have lower sucrose response thresholds compared to bees from the non-hygienic lines. In addition, hygienic bees did not forage at an earlier age or forage preferentially for pollen as compared to non-hygienic bees. These results support the idea that OA does not function in honey bees simply to enhance the detection of all chemical cues non-selectively or control related behaviors regardless of their environmental milieu. Our results indicate that the behavioral profile of the hygienic bee is sculpted by multiple factors including genetic, neural, social and environmental systems.     

Brood Pheromone Modulation of Pollen Forager Turnaround Time in the Honey Bee (<Emphasis Type="Italic">Apis mellifera</Emphasis> L.)

Foraging for pollen is an important behavior of the honey bee because pollen is their sole source of protein. Through nurse bees, larvae are the principal consumers of pollen. Fatty acid esters extractable from the surface of larvae, called brood pheromone, release multiple colony-level and individual foraging behaviors increasing pollen intake. In this study pollen forager turnaround time was measured in observation hives supplemented with brood pheromone versus a blank control treatment. Treatment with brood pheromone significantly decreased pollen forager turnaround time in the hive between foraging bouts by approximately 72%. Concurrently, brood pheromone increased the ratio of pollen to non-pollen foragers entering colonies. Brood pheromone has been shown to release most of the mechanisms known to increase pollen intake by colonies acting as an important regulator of colony foraging decisions and growth.     

Interaction between Sleep and Metabolism in Drosophila with Altered Octopamine Signaling

Sleep length and metabolic dysfunction are correlated, but the causal relationship between these processes is unclear. Octopamine promotes wakefulness in the fly by acting through the insulin-producing cells (IPCs) in the fly brain. To determine if insulin signaling mediates the effects of octopamine on sleep:wake behavior, we assayed flies in which insulin signaling activity was genetically altered. We found that increasing insulin signaling does not promote wake, nor does insulin appear to mediate the wake-promoting effects of octopamine. Octopamine also affects metabolism in invertebrate species, including, as we show here, Drosophila melanogaster. Triglycerides are decreased in mutants with compromised octopamine signaling and elevated in flies with increased activity of octopaminergic neurons. Interestingly, this effect is mediated at least partially by insulin, suggesting that effects of octopamine on metabolism are independent of its effects on sleep. We further investigated the relative contribution of metabolic and sleep phenotypes to the starvation response of flies with altered octopamine signaling. Hyperactivity (indicative of foraging) induced by starvation was elevated in octopamine receptor mutants, despite their high propensity for sleep, indicating that their metabolic state dictates their behavioral response under these conditions. Moreover, flies with increased octopamine signaling do not suppress sleep in response to starvation, even though they are normally hyper-aroused, most likely because of their high triglyceride levels. Together, these data suggest that observed correlations between sleep and metabolic phenotypes can result from shared molecular pathways rather than causality, and environmental conditions can lead to the dominance of one phenotype over the other.     

Reproductive physiology, dominance interactions, and division of labour among bumble bee workers

Abstract. Bumble bee workers (Bombus bifarius, Hymenoptera: Apidae) exhibit aggression toward one another after the colony begins producing female reproductive offspring (the competition phase). Workers in competition phase colonies must continue to perform in‐nest tasks, such as nest thermoregulation, and to forage for food, to rear the reproductives to maturity. Therefore, competition phase workers are faced with potentially conflicting pressures to work for their colonies, or to compete for direct reproduction. The effects of reproductive competition on worker task performance were quantified by measuring relationships of worker body size, reproductive physiology, and aggression with their rates of task performance. If worker division of labour was strongly affected by competition, it was predicted that fecund workers would avoid performing nest maintenance and foraging tasks, focusing instead on reproductive behaviour. Furthermore, it was predicted that fecund workers would dominate their nest mates, and that subordinate workers would perform nonreproductive tasks at higher rates. Worker aggression was associated closely with direct reproductive competition. Both aggression and brood interaction rates were related positively with ooctye development. Furthermore, foraging was associated negatively with ovarian development. However, in‐nest and foraging task performance rates were not associated with social aggression. The results support a partial role for reproductive competition in worker polyethism. Although worker aggression did not directly affect polyethism, reproductively competent workers avoided foraging tasks that would remove them from egg‐laying opportunities. Reproductively competent workers did perform in‐nest tasks, suggesting that these tasks entail little cost in terms of reproductive competition.     

Juvenile hormone and octopamine in the regulation of division of labor in honey bee colonies

Forager honey bees have high circulating levels of juvenile hormone (JH) and high brain levels of octopamine, especially in the antennal lobes, and treatment with either of these compounds induces foraging. Experiments were performed to determine whether octopamine acts more proximally than JH to affect the initiation of foraging behavior. Bees treated with octopamine became foragers more rapidly than bees treated with the JH analog methoprene. Bees treated with methoprene showed an increase in antennal lobe levels of octopamine, especially after 12 days. Bees with no circulating JH (corpora allata glands removed) treated with octopamine became foragers in similar numbers to bees with intact corpora allata. These results suggest that JH affects the initiation of foraging at least in part by increasing brain levels of octopamine, but octopamine can act independently of JH. Effects of JH that are not related to octopamine also are possible, as bees treated with both octopamine and methoprene were more likely to become foragers than bees treated with only octopamine or methoprene.     

Influence of brood, vent screening, and time of year on honey bee (Hymenoptera: Apidae) pollination and fruit quality of greenhouse tomatoes

Greenhouse tomatoes, Lycopersicon esculentum Miller (Solanaceae), are autogamous, but facilitated pollination results in increased fruit size and set. Previous research examining honey bee pollination in greenhouse tomato crops established that fruit quality resulting from honey bee visitation is often comparable to bumble bees (Bombus spp.) and significantly better than in flowers that receive no facilitated pollination. However, management alternatives have not been studied to improve tomato fruit quality when honey bees are the only pollination option available for the high-value greenhouse industry. We investigated whether the quantity of brood (eggs, larvae, and pupae) in a honey bee colony in the winter and screening on greenhouse vents in the summer would encourage honey bee foraging on tomato flowers. We also established the influence of time of year on the potential for honey bees to be effective pollinating agents. We constructed small honey bee colonies full of naive forager bees with either two frames of brood ("brood colonies") or two empty frames ("no-brood") and compared total fruit set and the number of tomato seeds resulting from fruit potentially visited by honey bees in each of these treatments to bagged flowers that received no facilitated pollination. There was no significant difference in the quality of fruit resulting from honey bees from "brood" and "no-brood" colonies. However, these fruits produced significantly more seeds than bagged flowers restricted from facilitated pollination. Honey bees from brood and no-brood colonies also resulted in 98% fruit set compared with 80% fruit set in bagged flowers that received no facilitated pollination. During the summer, the number of seeds per fruit did not differ significantly between unbagged flowers potentially visited by honey bees in screened greenhouses and unscreened greenhouses and bagged flowers that received no facilitated pollination. However, time of year did have a significant influence on the quality of fruit produced by honey bees compared with flowers that received no facilitated pollination, because no difference in seed number was observed between the treatments after mid-April. The results from this study demonstrate that the management of brood levels and vent screening cannot be used to improve the quality of fruit resulting from honey bee pollination and that honey bees can be a feasible greenhouse pollination alternative only during the winter.     

Effects of brood pheromone (SuperBoost) on consumption of protein supplement and growth of honey bee (Hymenoptera: Apidae) colonies during fall in a northern temperate climate

Honey bee, Apis mellifera L. (Hymenoptera: Apidae), nutrition is vital for colony growth and maintenance of a robust immune system. Brood rearing in honey bee colonies is highly dependent on protein availability. Beekeepers in general provide protein supplement to colonies during periods of pollen dearth. Honey bee brood pheromone is a blend of methyl and ethyl fatty acid esters extractable from cuticle of honey bee larvae that communicates the presence of larvae in a colony. Honey bee brood pheromone has been shown to increase protein supplement consumption and growth of honey bee colonies in a subtropical winter climate. Here, we tested the hypothesis that synthetic brood pheromone (SuperBoost) has the potential to increase protein supplement consumption during fall in a temperate climate and thus increase colony growth. The experiments were conducted in two locations in Oregon during September and October 2009. In both the experiments, colonies receiving brood pheromone treatment consumed significantly higher protein supplement and had greater brood area and adult bees than controls. Results from this study suggest that synthetic brood pheromone may be used to stimulate honey bee colony growth by stimulating protein supplement consumption during fall in a northern temperate climate, when majority of the beekeepers feed protein supplement to their colonies.     

The efficacy of small cell foundation as a varroa mite (<Emphasis Type="Italic">Varroa destructor</Emphasis>) control

Due to a continuing shift toward reducing/minimizing the use of chemicals in honey bee colonies, we explored the possibility of using small cell foundation as a varroa control. Based on the number of anecdotal reports supporting small cell as an efficacious varroa control tool, we hypothesized that bee colonies housed on combs constructed on small cell foundation would have lower varroa populations and higher adult bee populations and more cm² brood. To summarize our results, we found that the use of small cell foundation did not significantly affect cm² total brood, total mites per colony, mites per brood cell, or mites per adult bee, but did affect adult bee population for two sampling months. Varroa levels were similar in all colonies throughout the study. We found no evidence that small cell foundation was beneficial with regard to varroa control under the tested conditions in Florida.     

Brood pheromone regulates foraging activity of honey bees (Hymenoptera: Apidae)

Brood pheromone modulated the foraging behavior of commercial honey bee, Apis mellifera L., colonies pollinating a 10-ha market garden of cucumber, Cucurbita pepo L., and zucchini, Cucumis saticus L., in Texas in late autumn. Six colonies were randomly selected to receive 2000 larval equivalents of brood pheromone and six received a blank control. The ratio of pollen to nonpollen foragers entering colonies was significantly greater in pheromone-treated colonies 1 h after treatment. Pheromone-treated foragers returned with pollen load weights that were significantly heavier than controls. Pollen returned by pheromone-treated foragers was 43% more likely to originate from the target crop. Number of pollen grains washed from the bodies of nonpollen foragers from pheromone-treated colonies was significantly greater than controls and the pollen was 54% more likely to originate from the target crop. Increasing the foraging stimulus environment with brood pheromone increased colony-level foraging and individual forager efforts. Brood pheromone is a promising technology for increasing the pollination activity and efficiency of commercial honey bee colonies.     

Factors influencing seasonal absconding in colonies of the African honey bee,Apis mellifera scutellata

Summary This study investigated the effects of colony growth and development, food storage, foraging activity and weather on the migration behavior of African honey bees in the Okavango River Delta, Botswana. Four observation colonies were studied during the honey bee migration season (November–May), at which time the availability of blooming species was reduced. Two of the colonies (colonies 1 & 2) migrated during the study period, while the remaining two (colonies 3 & 4) did not. During the 4–6 weeks preceding the onset of migration preparations, colonies 1 & 2 exhibited increasing population sizes, high levels of brood production with low brood mortality, relatively large stores of food, and increasing mass. In contrast, the populations of colonies 3 & 4 did not increase, brood-rearing activity was erratic and lower, brood mortality was higher, food stores became depleted and colony mass declined. Both colonies 3 & 4 ceased rearing brood, and colony 3 died of starvation. Colony foraging activity was examined by monitoring waggle-dance activity 2–3 days each week. For 4–6 weeks before the onset of migration in colonies 1 & 2, daily foraging areas and mean daily foraging distances became increasingly large and variable. Colonies 3 & 4 exhibited foraging patterns similar to those observed for colonies 1 & 2 preceding migration. There was no clear association between 7 weather parameters examined and migration behavior. These data suggest that migration is influenced by an interaction of intra-colony demographics, food reserves and foraging patterns. Migration may be feasible only for those colonies that possess (1) a population of appropriate size and age structure to compensate for the natural attrition of older workers during the emigration process, and (2) sufficient food reserves for long-distance travel and the establishment of a new nest. Changing foraging patterns may reflect a deteriorating foraging environment, which may trigger the onset of migration preparations, provided that colony demographics and food reserves are conducive. Colonies that show decreased brood production, higher brood mortality and reduced food stores may be incapable of migrating, even when experiencing deteriorating foraging conditions. Rather, such colonies may have a greater chance of survival if they attempt to persist in a given area.