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.     

A quantitative model of honey bee colony population dynamics

Since 2006 the rate of honey bee colony failure has increased significantly. As an aid to testing hypotheses for the causes of colony failure we have developed a compartment model of honey bee colony population dynamics to explore the impact of different death rates of forager bees on colony growth and development. The model predicts a critical threshold forager death rate beneath which colonies regulate a stable population size. If death rates are sustained higher than this threshold rapid population decline is predicted and colony failure is inevitable. The model also predicts that high forager death rates draw hive bees into the foraging population at much younger ages than normal, which acts to accelerate colony failure. The model suggests that colony failure can be understood in terms of observed principles of honey bee population dynamics, and provides a theoretical framework for experimental investigation of the problem.     

High Concentrations of the Alarm Pheromone Component,Isopentyl Acetate,Reduces Foraging and Dancing in <Emphasis Type="Italic">Apis mellifera</Emphasis> Ligustica and <Emphasis Type="Italic">Apis cerana</Emphasis> Cerana

A honeybee colony is a superorganism that has evolved precise communication systems, which allow the colony to gather information from numerous individuals and coordinate its behavior. Alarm pheromones, such as isopentyl acetate (IPA), the main component of sting alarm pheromone, play a critical role in the coordination of individual behaviors as well as colony communication in honeybee colonies. In this study, honeybees (Apis mellifera ligustica and Apis cerana cerana) were exposed to relatively high levels of IPA at a foraging site (6–8 bee equivalents) and inside their colony (28–58 bee equivalents) to investigate the influence of alarm pheromones on foraging activity and hive flight activity. IPA reduced the number of bees that flew out the hive, foraged, and waggle danced. Under both contexts in the hive and at the food source, IPA can therefore inhibit honey bee foraging and foraging communication.     

Sticking to their choice – honey bee subfamilies abandon declining food sources at a slow but uniform rate

Abstract. 1. The allocation of honey bee foragers among food patches is a result of decisions made by individual bees that are based on internal and external cues.
2. Decision-making processes are often based on internal thresholds. For example, if the quality of the food source is assessed by a forager as exceeding its internal threshold, the bee will continue foraging on that food source.
3. It is often assumed that all individuals have the same threshold and therefore use the same thresholds in decision-making, but because the honey bee queen mates with 12–30 males, the workers within a colony are genetically heterogeneous. Thus, the thresholds used by individual bees may be genetically variable within a colony.
4. Models of colony-level foraging behaviour of honey bees suggest that the rate of abandoning food sources is a critical parameter affecting foraging success. Moreover, these models show that variance among subfamilies in their abandonment rates may increase the colony's foraging efficiency.
5. Experimental data showing the relationship between the probability of abandoning a food source and its profitability are lacking, as is information on any variation in abandonment rates among subfamilies.
6. Abandonment rates were determined experimentally for four honey bee families for seven different sucrose concentrations. The results showed that abandonment rates appear to be invariant among (sub)families. The importance of forager fidelity to declining food sources is discussed with respect to foraging efficiency in a changing environment.     

Reception and learning of electric fields in bees

Honeybees, like other insects, accumulate electric charge in flight, and when their body parts are moved or rubbed together. We report that bees emit constant and modulated electric fields when flying, landing, walking and during the waggle dance. The electric fields emitted by dancing bees consist of low- and high-frequency components. Both components induce passive antennal movements in stationary bees according to Coulomb''s law. Bees learn both the constant and the modulated electric field components in the context of appetitive proboscis extension response conditioning. Using this paradigm, we identify mechanoreceptors in both joints of the antennae as sensors. Other mechanoreceptors on the bee body are potentially involved but are less sensitive. Using laser vibrometry, we show that the electrically charged flagellum is moved by constant and modulated electric fields and more strongly so if sound and electric fields interact. Recordings from axons of the Johnston organ document its sensitivity to electric field stimuli. Our analyses identify electric fields emanating from the surface charge of bees as stimuli for mechanoreceptors, and as biologically relevant stimuli, which may play a role in social communication.     

Does the Earth's Magnetic Field Serve as a Reference for Alignment of the Honeybee Waggle Dance?

The honeybee (Apis mellifera) waggle dance, which is performed inside the hive by forager bees, informs hive mates about a potent food source, and recruits them to its location. It consists of a repeated figure-8 pattern: two oppositely directed turns interspersed by a short straight segment, the “waggle run”. The waggle run consists of a single stride emphasized by lateral waggling motions of the abdomen. Directional information pointing to a food source relative to the sun''s azimuth is encoded in the angle between the waggle run line and a reference line, which is generally thought to be established by gravity. Yet, there is tantalizing evidence that the local (ambient) geomagnetic field (LGMF) could play a role. We tested the effect of the LGMF on the recruitment success of forager bees by placing observation hives inside large Helmholtz coils, and then either reducing the LGMF to 2% or shifting its apparent declination. Neither of these treatments reduced the number of nest mates that waggle dancing forager bees recruited to a feeding station located 200 m north of the hive. These results indicate that the LGMF does not act as the reference for the alignment of waggle-dancing bees.     

Bumble bee olfactory information flow and contact-based foraging activation

Nestmate foraging activation and interspecific variation in foraging activation is poorly understood in bumble bees, as compared to honey bees and stingless bees. We therefore investigated olfactory information flow and foraging activation in the New World bumble bee species, Bombus impatiens. We (1) tested the ability of foragers to associate forager-deposited odor marks with rewarding food, (2) determined whether potential foragers will seek out the food odor brought back by a successful forager, and (3) examined the role of intranidal tactile contacts in foraging activation. Bees learned to associate forager-deposited odor marks with rewarding food. They were significantly more attracted to an empty previously rewarding feeder presented at a random position within an array of eight previously non-rewarding feeders. However, foragers did not exhibit overall odor specificity for short-term, daily floral shifts. For two out of three tested scents, activated foragers did not significantly prefer the feeder providing the same scent as that brought back by a successful forager. Finally, bees contacted by the successful forager inside the nest were significantly more likely to leave the nest to forage (38.6% increase in attempts to feed from empty feeders) than were non-contacted bees. This is the first demonstration that tactile contact, a hypothesized evolutionary basal communication mechanism in the social corbiculate bees, is involved in bumble bee foraging activation. Received 4 September 2007; revised 30 May 2008; accepted 15 July 2008.     

A Mathematical Model of Forager Loss in Honeybee Colonies Infested with <Emphasis Type="Italic">Varroa destructor</Emphasis> and the Acute Bee Paralysis Virus

We incorporate a mathematical model of Varroa destructor and the Acute Bee Paralysis Virus with an existing model for a honeybee colony, in which the bee population is divided into hive bees and forager bees based on tasks performed in the colony. The model is a system of five ordinary differential equations with dependent variables: uninfected hive bees, uninfected forager bees, infected hive bees, virus-free mites and virus-carrying mites. The interplay between forager loss and disease infestation is studied. We study the stability of the disease-free equilibrium of the bee-mite-virus model and observe that the disease cannot be fought off in the absence of varroacide treatment. However, the disease-free equilibrium can be stable if the treatment is strong enough and also if the virus-carrying mites become virus-free at a rate faster than the mite birth rate. The critical forager loss due to homing failure, above which the colony fails, is calculated using simulation experiments for disease-free, treated and untreated mite-infested, and treated virus-infested colonies. A virus-infested colony without varroacide treatment fails regardless of the forager mortality rate.     

Experience-dependent plasticity in the mushroom bodies of the solitary bee Osmia lignaria (Megachilidae)

All members of the solitary bee species Osmia lignaria (the orchard bee) forage upon emergence from their natal nest cell. Conversely, in the honey bee, days-to-weeks of socially regulated behavioral development precede the onset of foraging. The social honey bee's behavioral transition to foraging is accompanied by neuroanatomical changes in the mushroom bodies, a region of the insect brain implicated in learning. If these changes were general adaptations to foraging, they should also occur in the solitary orchard bee. Using unbiased stereological methods, we estimated the volume of the major compartments of the mushroom bodies, the neuropil and Kenyon cell body region, in adult orchard bees. We compared the mushroom bodies of recently emerged bees with mature bees that had extensive foraging experience. To separate effects of general maturation from field foraging, some orchard bees were confined to a cage indoors. The mushroom body neuropil of experienced field foragers was significantly greater than that of both recently emerged and mature caged orchard bees, suggesting that, like the honey bee, this increase is driven by outdoor foraging experience. Unlike the honey bee, where increases in the ratio of neuropil to Kenyon cell region occur in the worker after emerging from the hive cell, the orchard bee emerged from the natal nest cell with a ratio that did not change with maturation and was comparable to honey-bee foragers. These results suggest that a common developmental endpoint may be reached via different development paths in social and solitary species of foraging bees.     

Intra-Colonial Variability in the Dance Communication in Honeybees (Apis mellifera)

Honeybees have evolved numerous mechanisms for increasing colony-level foraging efficiency, mainly the combined system of scout-recruit division of labour and recruitment communication. A successful forager performs waggle dances on the surface of the comb where it interacts with nectar receivers and dance followers. A forager uses tremble dance when it experiences difficulty finding a receiver bee to unload food upon return to the hive. A bee colony containing numerous subfamilies may increase its efficiency in dance communication if dances are realized by particular groups of specialized individuals or subfamilies rather than by undifferentiated workers. In this study, we determined the subfamily frequencies of waggle and tremble dancers in a colony headed by a naturally mated queen, where the 17 subfamilies can be identified by microsatellite genetic markers. Our results demonstrate that a genetic component is associated with the dance communication in honeybees. More than half of the waggle dances and the tremble dances were performed by workers from only four subfamilies in each case.     

Viral Infection Affects Sucrose Responsiveness and Homing Ability of Forager Honey Bees,Apis mellifera L.

Honey bee health is mainly affected by Varroa destructor, viruses, Nosema spp., pesticide residues and poor nutrition. Interactions between these proposed factors may be responsible for the colony losses reported worldwide in recent years. In the present study, the effects of a honey bee virus, Israeli acute paralysis virus (IAPV), on the foraging behaviors and homing ability of European honey bees (Apis mellifera L.) were investigated based on proboscis extension response (PER) assays and radio frequency identification (RFID) systems. The pollen forager honey bees originated from colonies that had no detectable level of honey bee viruses and were manually inoculated with IAPV to induce the viral infection. The results showed that IAPV-inoculated honey bees were more responsive to low sucrose solutions compared to that of non-infected foragers. After two days of infection, around 10⁷ copies of IAPV were detected in the heads of these honey bees. The homing ability of IAPV-infected foragers was depressed significantly in comparison to the homing ability of uninfected foragers. The data provided evidence that IAPV infection in the heads may enable the virus to disorder foraging roles of honey bees and to interfere with brain functions that are responsible for learning, navigation, and orientation in the honey bees, thus, making honey bees have a lower response threshold to sucrose and lose their way back to the hive.     

The scent of the waggle dance

The waggle dance of honey bee (Apis mellifera L.) foragers communicates to nest mates the location of a profitable food source. We used solid-phase microextraction and gas chromatography coupled with mass spectrometry to show that waggle-dancing bees produce and release two alkanes, tricosane and pentacosane, and two alkenes, Z-(9)-tricosene and Z-(9)-pentacosene, onto their abdomens and into the air. Nondancing foragers returning from the same food source produce these substances in only minute quantities. Injection of the scent significantly affects worker behavior by increasing the number of bees that exit the hive. The results of this study suggest that these compounds are semiochemicals involved in worker recruitment. By showing that honey bee waggle dancers produce and release behaviorally active chemicals, this study reveals a new dimension in the organization of honey bee foraging.     

Persistence to Unrewarding Feeding Locations by Honeybee Foragers (Apis mellifera): the Effects of Experience,Resource Profitability and Season

Honeybee foragers that find a profitable food source quickly establish spatiotemporal memories, which allow them to return to this foraging site on subsequent days. The aim of this study was to investigate how the previous experience of honeybee foragers at a feeding location affects their persistence at that location once food is no longer available. We hypothesised that persistence would be greater to locations that were more rewarding (closer to the hive, higher concentration of sucrose solution), for which a bee had greater prior experience (0.5‐h vs. 2‐h training access), and at times of the year of lower nectar availability in the environment. We studied individually marked worker bees from four colonies trained to sucrose‐solution feeders. Our results support most of these predictions. Persistence, measured both in duration and number of visits, was greater to locations that previously offered sucrose solution of higher concentration (2 m vs. 1 m ) or were closer to the hive (20 m vs. 450 m). Persistence was also greater in bees that had longer access at the feeder before the syrup was terminated (2 h vs. 0.5 h). However, contrary to our prediction, persistence was not higher in the season of the lowest nectar availability in the environment in the study year. In summary, honeybees show considerable persistence at foraging sites that ceased providing rewards. The decision to abandon a foraging site depends on the profitability the forager experienced when the foraging site was still rewarding.     

Thorax vibrations of a stingless bee (<Emphasis Type="Italic">Melipona seminigra</Emphasis>). I. No influence of visual flow

An important question in stingless bee communication is whether the thorax vibrations produced by foragers of the genus Melipona upon their return to the nest contain spatial information about food sources or not. As previously shown M. seminigra is able to use visual flow to estimate flight distances. The present study investigated whether foraging bees encode the visually measured distance in their thorax vibrations. Bees were trained to collect food in flight tunnels lined with a black-and-white pattern on their side walls and floor, which substantially influenced the image motion they experienced. When the bees had collected inside the tunnels the temporal pattern of their vibrations differed significantly from the pattern after collecting in a natural environment. These changes, however, were not associated with the visual flow experienced inside the tunnel. Bees collecting in tunnels offering little visual flow (stripes parallel to flight direction) modified their vibrations similarly to bees collecting in tunnels with high image motion (cross stripes). A higher energy expenditure due to drastically reduced flight velocities inside the tunnel is suggested to be responsible for changes in the thorax vibrations. The bees' vibrations would thus reflect the overall energetic budget of a foraging trip.     

Effects of experience and juvenile hormone on the organization of the mushroom bodies of honey bees

There is an age-related division of labor in the honey bee colony that is regulated by juvenile hormone. After completing metamorphosis, young workers have low titers of juvenile hormone and spend the first several weeks of their adult lives performing tasks within the hive. Older workers, approximately 3 weeks of age, have high titers of juvenile hormone and forage outside the hive for nectar and pollen. We have previously reported that changes in the volume of the mushroom bodies of the honey bee brain are temporally associated with the performance of foraging. The neuropil of the mushroom bodies is increased in volume, whereas the volume occupied by the somata of the Kenyon cells is significantly decreased in foragers relative to younger workers. To study the effect of flight experience and juvenile hormone on these changes within the mushroom bodies, young worker bees were treated with the juvenile hormone analog methoprene but a subset was prevented from foraging (big back bees). Stereological volume estimates revealed that, regardless of foraging experience, bees treated with methoprene had a significantly larger volume of neuropil in the mushroom bodies and a significantly smaller Kenyon cell somal region volume than did 1-day-old bees. The bees treated with methoprene did not differ on these volume estimates from untreated foragers (presumed to have high endogenous levels of juvenile hormone) of the same age sampled from the same colony. Bees prevented from flying and foraging nonetheless received visual stimulation as they gathered at the hive entrance. These results, coupled with a subregional analysis of the neuropil, suggest a potentially important role of visual stimulation, possibly interacting with juvenile hormone, as an organizer of the mushroom bodies. In an independent study, the brains of worker bees in which the transition to foraging was delayed (overaged nurse bees) were also studied. The mushroom bodies of overaged nurse bees had a Kenyon cell somal region volume typical of normal aged nurse bees. However, they displayed a significantly expanded neuropil relative to normal aged nurse bees. Analysis of the big back bees demonstrates that certain aspects of adult brain plasticity associated with foraging can be displayed by worker bees treated with methoprene independent of foraging experience. Analysis of the over-aged nurse bees suggests that the post-metamorphic expansion of the neuropil of the mushroom bodies of worker honey bees is not a result of foraging experience. © 1995 John Wiley & Sons, Inc.     

Optic flow informs distance but not profitability for honeybees

How do flying insects monitor foraging efficiency? Honeybees (Apis mellifera) use optic flow information as an odometer to estimate distance travelled, but here we tested whether optic flow informs estimation of foraging costs also. Bees were trained to feeders in flight tunnels such that bees experienced the greatest optic flow en route to the feeder closest to the hive. Analyses of dance communication showed that, as expected, bees indicated the close feeder as being further, but they also indicated this feeder as the more profitable, and preferentially visited this feeder when given a choice. We show that honeybee estimates of foraging cost are not reliant on optic flow information. Rather, bees can assess distance and profitability independently and signal these aspects as separate elements of their dances. The optic flow signal is sensitive to the nature of the environment travelled by the bee, and is therefore not a good index of flight energetic costs, but it provides a good indication of distance travelled for purpose of navigation and communication, as long as the dancer and recruit travel similar routes. This study suggests an adaptive dual processing system in honeybees for communicating and navigating distance flown and for evaluating its energetic costs.     

Measurement of Electric Charges Carried by Bees: Evidence of Biological Variations

Various insects, especially social insects, possess electric charges. Erickson (1982, 1983) shows their involvement in the odor receptor efficiency of honey bee antenna. Also, the author suggests the importance of charges in the transfer of pollen grains from flowers to pollinator insects. To measure directly electric charges, we fit a sensor used to determine the charges of raindrops. Strongly clustered wintering bees and foraging bees were measured. The individual values range between ?400pC to +600pC (m = 153 +/105pC) during winter time. The foraging bees possess variable charges, generally smaller than wintering bees (m = 29 +/? 40pC). 7.0% of measured bees whole are charged negatively and less than 1% of these have no charges. The presence of electric charges throughout bees yearly cycle is significant for the insect society. Moreover electric forces contribute to explain some aspects of bee-parasite relationships.     

Individual recruitment in honeybees, <Emphasis Type="Italic">Apis mellifera</Emphasis> L.

The recruitment of honeybee foragers individually exploiting a low-flow rate-feeder that presented different temporal reward programs was experimentally analyzed. By capturing hive bees that landed at the feeder in a 2-h period, the arrival rate of incoming bees could be obtained. With this procedure we quantitatively analyzed the maximum number of hive bees that can be brought to the feeding station by single foragers. Test bees collected sucrose solution during 12 visits to a rate-feeder located 160 m from the hive. The constant programs offered 0.6, 1.2, or 2.4 M sugar for all 12 visits, while the variable programs delivered either 0.6, 1.2, or 0.6 M or 0.6, 2.4, or 0.6 M, with four visits for each molarity. Results showed that the sucrose concentration exploited by single foragers increased the arrival rate. Moreover, there was a linear relationship within this range of sucrose concentrations that presented a slope of 1.58. Since the sugar solutions were provided at the same flow rate (5 μl/min) in all the programs, the arrival rate expressed in terms of sucrose flow rate (milligrams of sucrose/minute) shows that one additional incoming bee per hour arrived when the single forager assessed an increase in the sucrose flow rate of 0.75 mg sucrose/min at the rate-feeder. The absence of differences in the frequency of visits of the single foragers during the constant programs suggests that the differences observed in the arrival rate can mainly be explained by a more intensive display of the recruitment mechanisms performed per foraging trip instead of by their iterativeness throughout different foraging cycles. Variable reward programs showed that arrival rate is rapidly adjusted according to the reward change and is independent of its magnitude. Received in revised form: 17 August 2001 Electronic Publication     

The hive bee to forager transition in honeybee colonies: the double repressor hypothesis

In summer, the honeybee (Apis mellifera) worker population consists of two temporal castes, a hive bee group performing a multitude of tasks including nursing inside the nest, and a forager group specialized on collecting nectar, pollen, water and propolis. Elucidation of the regulatory mechanisms responsible for the hive bee to forager transition holds a prominent position within present day sociobiology. Here we suggest a new explanation dubbed the "double repressor hypothesis" aimed to account for the substantial amount of empirical data in this field. This is the first time where both the regular transition and starvation-induced precocious transition are explained within the same regulatory framework. We suggest that the transition is under regulatory control by an internal and an external repressor of the allatoregulatory central nervous system, where these two repressors modulate a positive regulatory feedback loop involving juvenile hormone (JH) and the lipoprotein vitellogenin. The concepts of age-neutrality, fixed and variable response thresholds and reinforcement are integral parts of our explanation, and in addition they are given explicit physiological content. The hypothesis is represented by a differential equations model at the level of the individual bee, and by a discrete individual-based colony model. The two models generate predictions in accordance with empirical data concerning the cumulative probability of becoming a forager, mean age at onset of foraging, reversal of foragers, time window of reversal, relationship between JH titre and onset of foraging, relative representations of genotypic groups, and effects of forager depletion and confinement.     

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.