Social foraging in honey bees: how nectar foragers assess their colony's nutritional status

Summary A honey bee colony operates as a tightly integrated unit of behavioral action. One manifestation of this in the context of foraging is a colony's ability to adjust its selectivity among nectar sources in relation to its nutritional status. When a colony's food situation is good, it exploits only highly profitable patches of flowers, but when its situation is poor, a colony's foragers will exploit both highly profitable and less profitable flower patches. The nectar foragers in a colony acquire information about their colony's nutritional status by noting the difficulty of finding food storer bees to receive their nectar, rather than by evaluating directly the variables determining their colony's food situation: rate of nectar intake and amount of empty storage comb. (The food storer bees in a colony are the bees that collect nectar from returning foragers and store it in the honey combs. They are the age group (generally 12–18 day old bees) that is older than the nurse bees but younger than the foragers. Food storers make up approximately 20% of a colony members.) The mathematical theory for the behavior of queues indicates that the waiting time experienced by nectar foragers before unloading to food storers (queue length) is a reliable and sensitive indicator of a colony's nutritional status. Queue length is automatically determined by the ratio of two rates which are directly related to a colony's nutritional condition: the rate of arrival of loaded nectar foragers at the hive (arrival rate) and the rate of arrival of empty food storers at the nectar delivery area (service rate). These two rates are a function of the colony's nectar intake rate and its empty comb area, respectively. Although waiting time conveys crucial information about the colony's nutritional status, it has not been molded by natural selection to serve this purpose. Unlike signals, which are evolved specifically to convey information, this cue conveys information as an automatic by-product. Such cues may prove more important than signals in colony integration.     

Odour transfer in stingless bee marmelada (Frieseomelitta varia) demonstrates that entrance guards use an “undesirable–absent” recognition system

In group-level recognition, discriminators use sensory information to distinguish group members and non-members. For example, entrance guards in eusocial insect colonies discriminate nestmates from intruders by comparing their odour with a template of the colony odour. Despite being a species-rich group of eusocial bees closely related to the honey bees, stingless bee nestmate recognition is a relatively little-studied area. We studied Frieseomelitta varia, a common Brazilian species of stingless bee known as marmelada. By measuring the rejection rates of nestmate and non-nestmate worker bees by guards, we were able to show that guards became significantly less accepting (from 91 to 46%) of nestmates that had acquired odour cues from non-nestmate workers; however, guards did not become significantly more accepting (from 31 to 42%) of non-nestmates that had acquired equivalent amounts of odour cues from the guard’s nestmates. These data strongly suggest that guards use an “undesirable–absent” system in recognition, whereby incoming conspecific workers are only accepted if undesirable cues are absent, despite the presence of desirable cues. We suggest that an undesirable–absent system is adaptive because robbing by conspecifics may be an important selective factor in F. varia, which would lead to selection for a non-permissive acceptance strategy by guards.     

Honeybee foragers adjust crop contents before leaving the hive

Upon leaving the hive, foragers carry a small amount of honey, which they subsequently consume to generate energy for flight. We investigated the relationship between waggle-phase duration and crop volume in foragers (both dancers and dance followers) leaving the hive. Our findings indicate that these variables were positively correlated in the two types of bee, suggesting that they were able to adjust the amount of food that they carry depending on the distance to a food source. We also found that dance followers left the hive with a larger amount of honey than dancers. We suggest two possible explanations: (1) dance followers have less information about the location of the food source than dancers, who have a better knowledge of the surrounding area; or (2) honeybees lack a precise calibration method for estimating energy needs from waggle-run duration. The effect of foraging experience was confirmed: bees decreased their honey load at departure with repeated trips to a sugar-syrup feeder. Honeybees showed a different pattern of change when the feeder provided soybean flour as a pollen substitute, possibly because honeybees use honey not only as an energy source but also as “glue” to form “balls” of pollen on their hind legs. Based on our observations that followers of sugar-syrup foragers carry a different amount of honey in their crop than followers of soybean-followers, we suggest that waggle dancers also convey information concerning food type.     

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

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

Food-exchange by foragers in the hive – a means of communication among honey bees?

Dancing and trophallactic behaviour of forager honey bees, Apis mellifera ligustica >Spinola, that returned from an automatic feeder with a regulated flow rate of 50% weight-to-weight sucrose solution (range: 0.76–7.65 μl/min) were studied in an observation hive. Behavioural parameters of dancing, such as probability, duration and dance tempo, increased with the nectar flow rate, though with very different response curves among bees. For trophallaxis (i.e. mouth-to-mouth exchange of food), the frequency of giving-contacts and the transfer rate of the nectar increased with the nectar flow rate. After unloading, foragers often approached other nest mates and begged for food before returning to the food source. This behaviour was less frequent at higher nectar flow rates. These results show that the profitability of a food source in terms of nectar flow rate had a quantitative representation in the hive through quantitative changes in trophallactic and dancing behaviour. The role of trophallaxis as a communication channel during recruitment is discussed. Received: 14 January 1995/Accepted after revision: 14 August 1995     

Stingless bee response to spider webs is dependent on the context of encounter

In the course of their foraging bouts, bees frequently encounter spider webs among the vegetation. The ability to see and avoid these webs is vital for the success of the individual bee’s foraging bout. In this study, we report on the response of stingless bees (Trigona carbonaria) towards the webs of the St. Andrew’s Cross spider (Argiope keyserlingi). We studied the ability of bees to avoid webs in different contexts: when bees were on their foraging path or when they were returning to the hive as well as when they were flying North or South. We show that the probability of a bee being able to avoid a web depends on the context of the bee’s flight rather than the visual appearance of the web. Furthermore, the presence of the spider seems to alert the bee to the web, resulting in bees being more able to avoid capture. We show, specifically, that the probability of being captured is higher when the bee is returning to the hive compared with when the bee is foraging. The likelihood of avoiding a web is also influenced by the compass direction of the flight, although to a lesser extent. Our results indicate that the context of the predator–prey encounter has a significant influence on a bee’s ability to escape interception by a spider web.     

Timekeeping in the honey bee colony: integration of circadian rhythms and division of labor

The daily patterns of task performance in honey bee colonies during behavioral development were studied to determine the role of circadian rhythmicity in age-related division of labor. Although it is well known that foragers exhibit robust circadian patterns of activity in both field and laboratory settings, we report that many in-hive tasks are not allocated according to a daily rhythm but rather are performed 24 h per day. Around-the-clock activity at the colony level is accomplished through the performance of some tasks by individual workers randomly with respect to time of day. Bees are initially arrhythmic with respect to task performance but develop diel rhythmicity, by increasing the occurrence of inactivity at night, prior to becoming foragers. There are genotypic differences for age at onset of rhythmicity and our results suggest that these differences are correlated with genotypic variation in rate of behavioral development: genotypes of bees that progressed through the age polyethism schedule faster also acquired behavioral rhythmicity at an earlier age. The ontogeny of circadian rhythmicity in honey bee workers ensures that essential in-hive behaviors are performed around the clock but also allows the circadian clock to be engaged before the onset of foraging. Received: 6 October 1997 / Accepted after revision: 28 March 1998     

Division of labor during honey bee colony defense

Summary Some worker honey bees respond to major disturbances of the colony by flying around the assailant and possibly stinging; they are a subset of the bees involved in colony defense. These defenders have an open-ended age distribution similar to that of foragers, but defensive behavior is initiated at a younger age than foraging is. Behavioral and genetic evidence shows that defenders and foragers are distinct groups of older workers. Behaviorally, defenders have less worn wings than foragers, suggesting less flight activity. Genetically, defenders differ in allozyme frequencies, demonstrating different subfamily composition from foragers in the same colony. They also differ in allozyme frequencies from guards in the same colony, providing further evidence for division of labor associated with colony defense. We use this information to develop a model for honey bee colony defense involving at least two distinct groups of workers and we propose that the non-guard defenders be called soldiers, due to their important role in colony defense.Offprint requests to: M.D. Breed     

Reward rate and forager activation in honeybees: recruiting mechanisms and temporal distribution of arrivals

We analyzed the foraging and recruitment activity of single foragers ( Apis mellifera), exploiting low reward rates of sucrose solution. Single employed foragers (test bees) were allowed to collect 2.0 m sucrose solution delivered by a rate-feeder located at 160 m from the hive for 2 h. Flow rates varied between 1.4 and 5.5 µl/min. The individual behavior of the test bees was registered both at the hive and the food source, and the social output was calculated as the number of incoming bees arriving at the feeder per hour (henceforth: arrival rate). Incoming bees were captured once they landed at the feeder and assigned to one of three categories according to their foraging experience and hive interactions with the test bee: inspector, reactivated, or inexperienced bees. Both the waggle-runs performed per hour of foraging by test bees and the social output attained, increased with the reward rate. Also the number of hive-stays and the trophallactic-offering contacts performed by test bees were positively correlated with the arrival rate. For the highest reward rates, the duration of Nasonov-gland exposure at the feeding place was higher, and the arrival of most of the incoming bees occurred shortly after the test bee landed at the feeding platform. Thus, in addition to hive-interactions, landing of incoming bees at the food source is promoted by olfactory and/or visual information provided by the test bees. The proportions of inspector, reactivated, and inexperienced bees changed depending on the reward rate offered. Therefore, not only the occurrence and intensity of the recruitment-related behaviors performed by the test bees, but also the stimulation required by each category of incoming bees, determined the social output observed.     

The role of wax and resin in the nestmate recognition system of a stingless bee, Tetragonisca angustula

Recent research has shown that entrance guards of the stingless bee Tetragonisca angustula make less errors in distinguishing nestmates from non-nestmates than all other bee species studied to date, but how they achieve this is unknown. We performed four experiments to investigate nestmate recognition by entrance guards in T. angustula. We first investigated the effect of colony odours on acceptance. Nestmates that acquired odour from non-nestmate workers were 63% more likely to be rejected while the acceptance rate of non-nestmates treated with nestmate odour increased by only 7%. We further hypothesised that guards standing on the wax entrance tube might use the tube as an odour referent. However, our findings showed that there was no difference in the acceptance of non-nestmates by guards standing on their own colony’s entrance tube versus the non-nestmate’s entrance tube. Moreover, treatment of bees with nestmate and non-nestmate resin or wax had a negative effect on acceptance rates of up to 65%, regardless of the origin of the wax or resin. The role of resin as a source of recognition cues was further investigated by unidirectionally transferring resin stores between colonies. Acceptance rates of nestmates declined by 37% for hives that donated resin, contrasting with resin donor hives where acceptance of non-nestmates increased by 21%. Overall, our results confirm the accuracy of nestmate recognition in T. angustula and reject the hypothesis that this high level of accuracy is due to the use of the wax entrance tubes as a referent for colony odour. Our findings also suggest that odours directly acquired from resin serve no primary function as nestmate recognition cues. The lack of consistency among colonies plus the complex results of the third and fourth experiments highlight the need for further research on the role of nest materials and cuticular profiles in understanding nestmate recognition in T. angustula.     

The honey bee shaking signal: function and design of a modulatory communication signal

This study explores the meaning and functional design of a modulatory communication signal, the honey bee shaking signal, by addressing five questions: (I) who shakes, (II) when do they shake, (III) where do they shake, (IV) how do receivers respond to shaking, and (V) what conditions trigger shaking. Several results confirm the work of Schneider (1987) and Schneider et al. (1986a): (I) most shakers were foragers (at least 83%); (II) shaking exhibited a consistent temporal pattern with bees producing the most signals in the morning (0810–1150 hours) just prior to a peak in waggle dancing activity; and (IV) bees moved faster (by 75%) after receiving a shaking signal. However, this study differs from previous work by providing a long-term, temporal, spatial, and vector analysis of individual shaker behavior. (III) Bees producing shaking signals walked and delivered signals in all areas of the hive, but produced the most shaking signals directly above the waggle dance floor. (IV) Bees responded to the signal by changing their direction of movement. Prior to receiving a signal, bees selected from the waggle dance floor moved, on average, towards the hive exit. After receiving a signal, some bees continued moving towards the exit but others moved directly away from the exit. During equivalent observation periods, non-shaken bees exhibited a strong tendency to move towards the hive exit. (V) Renewed foraging activity after food dearth triggered shaking signals, and, the level of shaking is positively correlated with the duration of food dearth. However, shaking signal levels also increased in the morning before foraging had begun and in the late afternoon after foraging had ceased. This spontaneous afternoon peak has not previously been reported. The shaking signal consequently appears to convey the general message “reallocate labor to different activities” with receiver context specifying a more precise meaning. In the context of foraging, the shaking signal appears to activate (and perhaps deactivate) colony foraging preparations. The generally weak response elicited by modulatory signals such as the shaking signal may result from a high receiver response threshold which allows the receiver to integrate multiple sources of information and which thereby increases the probability that receiver actions will be appropriate to colony needs. Received: 21 March 1997 / Accepted after revision: 30 August 1997     

农药暴露的机制模型：蜜蜂毒理学的重要缺失

杀虫剂在最近的蜜蜂数量减少中所扮演的角色是有争议的，部分原因是实地研究常常无法检测到实验室研究所预测的效果。这种不一致性突出了蜜蜂毒理学研究领域的一个关键空白：对蜜蜂在它们的环境中杀虫剂暴露的模式和过程知之甚少。本文作者提出蜜蜂暴露杀虫剂的2个关键过程：1)工蜂采集花蜜的过程中收集农药；2)工蜂带回的农药在蜂巢中的再分配。工蜂收集农药的过程必须被理解为环境污染和蜜蜂觅食活动之间的时空交集。这意味着农药暴露是分配的，而不是离散的，觅食工蜂的一个子集可能会获得有害剂量的农药，而群体暴露将会显得安全。蜂箱中农药的分布是一个复杂的过程，主要是由群体成员之间食物转移的相互作用而产生，而这一过程中花粉和花蜜之间有重要的区别。因此应该优先将关于蜜蜂生物学的大量文献用于发展更严谨的蜂蜜农药暴露机制模型。与效应机制模型结合，暴露机制模型具有整合蜜蜂毒理学领域的潜力，以促进风险评估和基础研究。
精选自Sponsler, D. B. and Johnson, R. M. (2017), Mechanistic modeling of pesticide exposure: The missing keystone of honey bee toxicology. Environmental Toxicology and Chemistry, 36: 871–881. doi: 10.1002/etc.3661
详情请见http://onlinelibrary.wiley.com/doi/10.1002/etc.3661/full
     

Swarm cognition in honey bees

We synthesize findings from neuroscience, psychology, and behavioral biology to show that some key features of cognition in the neuron-based brains of vertebrates are also present in the insect-based swarm of honey bees. We present our ideas in the context of the cognitive task of nest-site selection by honey bee swarms. After reviewing the mechanisms of distributed evidence gathering and processing that are the basis of decision making in bee swarms, we point out numerous similarities in the functional organization of vertebrate brains and honey bee swarms. These include the existence of interconnected subunits, parallel processing of information, a spatially distributed memory, layered processing of information, lateral inhibition, and mechanisms of focusing attention on critical stimuli. We also review the performance of simulated swarms in standard psychological tests of decision making: tests of discrimination ability and assessments of distractor effects.     

The stop signal of honey bees: reconsidering its message

Summary The stop signal of honey bees has long been regarded as a vibrational begging signal produced by dance followers to elicit food from waggle dancers (Esch 1964). On the basis of playback experiments and behavioral analysis, this study presents the following evidence for a different signal function. Stop signals (1) can be produced by tremble dancers, dance followers, and waggle dancers; (2) rarely elicit trophallaxis; and (3) evidently cause waggle dancers to leave the dance floor. Subsequent work by Kirchner (submitted) using vibrational playback experiments confirms the latter observation. When the colony's food storers are temporarily overwhelmed by a large nectar influx, returning foragers will search for prolonged periods before unloading food and consequently begin to tremble dance (Seeley 1992). In this study, tremble dancers were the major producer of stop signals on the dance floor. The stop signal may thus retard recruitment until balance is restored.     

In-hive patterns of temporal polyethism in strains of honey bees (Apis mellifera) with distinct genetic backgrounds

Honey bee workers exhibit an age-based division of labor (temporal polyethism, DOL). Younger bees transition through sets of tasks within the nest; older bees forage outside. Components of temporal polyethism remain unrevealed. Here, we investigate the timing and pattern of pre-foraging behavior in distinct strains of bees to (1) determine if a general pattern of temporal DOL exists in honey bees, (2) to demonstrate a direct genetic impact on temporal pacing, and (3) to further elucidate the mechanisms controlling foraging initiation. Honey bees selected for differences in stored pollen demonstrate consistent differences in foraging initiation age. Those selected for increased pollen storage (high pollen hoarding strain, HSBs) initiate foraging earlier in life than those selected for decreased pollen storage (low pollen hoarding strain, LSBs). We found that HSBs both initiate and terminate individual pre-foraging tasks earlier than LSBs when housed in a common hive environment. Unselected commercial bees (wild type) generally demonstrated intermediate behavioral timing. There were few differences between genotypes for the proportion of pre-foraging effort dedicated to individual tasks, though total pre-foraging effort differences differed dramatically. This demonstrates that behavioral pacing can be accelerated or slowed, but the pattern of behavior is not fundamentally altered, suggesting a general pattern of temporal behavior in honey bees. This also demonstrates direct genetic control of temporal pacing. Finally, our results suggest that earlier HSB protein (pollen) consumption termination compared to LSBs may contribute to an earlier decline in hemolymph vitellogenin protein titers, which would explain their earlier onset of foraging.     

Worker allocation in insect societies: coordination of nectar foragers and nectar receivers in honey bee (Apis mellifera) colonies

Nectar collection in the honey-bee is partitioned. Foragers collect nectar and take it to the nest, where they transfer it to receiver bees who then store it in cells. Because nectar is a fluctuating and unpredictable resource, changes in worker allocation are required to balance the work capacities of foragers and receivers so that the resource is exploited efficiently. Honey bee colonies use a complex system of signals and other feedback mechanisms to coordinate the relative and total work capacities of the two groups of workers involved. We present a functional evaluation of each of the component mechanisms used by honey bees – waggle dance, tremble dance, stop signal, shaking signal and abandonment – and analyse how their interplay leads to group-level regulation. We contrast the actual regulatory system of the honey bee with theory. The tremble dance conforms to predicted best use of information, where the group in excess applies negative feedback to itself and positive feedback to the group in shortage, but this is not true of the waggle dance. Reasons for this and other discrepancies are discussed. We also suggest reasons why honey bees use a combination of recruitment plus abandonment and not switching between subtasks, which is another mechanism for balancing the work capacities of foragers and receivers. We propose that the waggle and tremble dances are the primary regulation mechanisms, and that the stop and shaking signals are secondary mechanisms, which fine-tune the system. Fine-tuning is needed because of the inherent unreliability of the cues, queueing delays, which foragers use to make recruitment decisions. Received: 15 December 1998 / Received in revised form: 6 March 1999 / Accepted: 12 March 1999     

Displaced honey bees perform optimal scale-free search flights

Honey bees (Apis mellifera) are regularly faced with the task of navigating back to their hives from remote food sources. They have evolved several methods to do this, including compass-directed "vector" flights and the use of landmarks. If these hive-centered mechanisms are disrupted, bees revert to searching for the hive, but the nature and efficiency of their searching strategy have hitherto been unknown. We used harmonic radar to record the flight paths of honey bees that were searching for their hives. Our subsequent analysis of these paths revealed that they can be represented by a series of straight line segments that have a scale-free, Lévy distribution with an inverse-square-law tail. We show that these results, combined with the "no preferred direction" characteristic of the segments, demonstrate that the bees were flying an optimal search pattern. Lévy movements have already been identified in a number of other animals. Our results are the best reported example where the movements are mostly attributable to the adoption of an optimal, scale-free searching strategy.     

Retinue attraction and ovary activation: responses of wild type and anarchistic honey bees (Apis mellifera) to queen and brood pheromones

In most social insect colonies, workers do not attempt to lay eggs in the presence of a queen. However, in the honey bee (Apis mellifera), a rare phenotype occurs in which workers activate their ovaries and lay large numbers of male eggs despite the presence of a fecund queen. We examined the proximate mechanisms by which this ‘anarchistic’ behaviour is expressed. We tested the effects of brood and queen pheromones on retinue attraction and worker ovary activation using caged worker bees. We found no difference between the anarchistic and wild type queen pheromones in the retinue response elicited in either wild type or anarchistic workers. Further, we found that anarchistic queens produce a pheromone blend that is as effective at inhibiting ovary activation as the wild type queen pheromone. However, anarchistic workers are less inhibited by queen pheromones than their wild type counterparts, in a dose-dependent manner. These results show that the anarchistic phenomenon is not due to changes in the production of queen pheromones, but rather is due in part to a shift in the worker response to these queen-produced signals. In addition, we demonstrate the dose-dependent nature of the effect of queen pheromones on honey bee worker ovary activation.     

The occurrence and context of tremble dancing in free-foraging honey bees (<Emphasis Type="Italic">Apis mellifera</Emphasis>)

Nectar foraging in honey bees is regulated by several communication signals that are performed mainly by foragers. One of these signals is the tremble dance, which is consistently performed by foragers from a rich food source which, upon return to the hive, experience a long delay before unloading their nectar to a nectar receiver. Although tremble dancing has been studied extensively using artificial nectar sources, its occurrence and context in a more natural setting remain unknown. Therefore, this study tests the sufficiency of the current explanations for tremble dancing by free-foraging honey bees. The main finding is that only about half of the observations of tremble dancing, referred to as delay-type tremble dancing, are a result of difficulty in finding a nectar receiver. In the remaining observations, tremble dancing was initiated immediately upon entering the hive, referred to as non-delay-type tremble dancing. Non-delay tremble dancing was associated with first foraging successes, both in a forager's career and in a single day. More than 75% of tremble dancing was associated with good foraging conditions, as indicated by the dancer continuing to forage after dancing. However, at least some of the other cases were associated with deteriorated foraging conditions, such as the end of the day, after which foraging was discontinued. No common context could be identified that explains all cases of tremble dancing or the subset of non-delay-type tremble dancing. This study shows that the current explanations for the cause of the tremble dance are insufficient to explain all tremble dancing in honey bees that forage at natural food sources.     

The tremble dance of the honey bee: message and meanings

Summary The nectar foragers of a honey bee colony, upon return to the hive, sometimes perform a mysterious behavior called the tremble dance. In performing this dance, a forager shakes her body back and forth, at the same time rotating her body axis by about 50° every second or so, all the while walking slowly across the comb. During the course of a dance, which on average lasts 30 min, the bee travels about the broodnest portion of the hive. It is shown experimentally that a forager will reliably perform this dance if she visits a highly profitable nectar source but upon return to the hive experiences great difficulty finding a food-storer bee to take her nectar. This suggests that the message of the tremble dance is I have visited a rich nectar source worthy of greater exploitation, but already we have more nectar coming into the hive than we can handle. It is also shown experimentally that the performance of tremble dances is followed quickly by a rise in a colony's nectar processing capacity and (see Nieh, in press and Kirchner, submitted) by a drop in a colony's recruitment of additional bees to nectar sources. These findings suggest that the tremble dance has multiple meanings. For bees working inside the hive, its meaning is apparently I should switch to the task of processing nectar, while for bees working outside the hive (gathering nectar), its meaning is apparently I should refrain from recruiting additional foragers to my nectar source. Hence it appears that the tremble dance functions as a mechanism for keeping a colony's nectar processing rate matched with its nectar intake rate at times of greatly increased nectar influx. Evidently the tremble dance restores this match in part by stimulating a rise in the processing rate, and in part by inhibiting any further rise in the intake rate. Correspondence to: T. Seeley