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     

Effects of intracolony variability in behavioral development on plasticity of division of labor in honey bee colonies

There is a genetic component to plasticity in age polyethism in honey bee colonies, such that workers of some genotypes become precocious foragers more readily than do workers of other genotypes, in colonies lacking older bees. Using colonies composed of workers from two identifiable genotype groups, we determined that intracolony differences in the likelihood of becoming a precocious forager are a consequence of differences in rates of behavioral development that are also evident under conditions leading to normal development. An alternative hypothesis, that differences in the likelihood of becoming a precocious forager are due to differences in general sensitivity to altered colony conditions, was not supported. In three out of three trials, workers from the genotype group that was more likely to exhibit precocious foraging in single cohort colonies also foraged at relatively younger ages in colonies in which workers exhibited normal behavioral development. In contrast, in three out of three trials, workers from the genotype group that was more likely to exhibit precocious foraging in single-cohort colonies did not show disproportionately more overaged nursing in colonies in which workers exhibited delayed development. These results indicate that genotypic differences in plasticity in age-related division of labor are based on genotypic differences in rates of behavioral development.     

The effect of colony size and starvation on food flow in the fire ant,Solenopsis invicta (Hymenoptera: Formicidae)

Summary Food-sharing experiments were performed with laboratory colonies of Solenopsis invicta containing 1000, 10,000, or 20,000 workers and starved for 0, 3, 7, or 14 days. The effect of these variables was measured on the uptake of radioactive sugar water (1 M) by 1% of the colony's workers and on the trophallactic flow of food from these foragers to the remainder of the colony.Patterns of food distribution in small colonies differed significantly from those in larger nests. In 1000-ant nests, small workers more frequently received food than large workers, but in bigger colonies the opposite occurred.Fire ants were adept at distributing sugar water, with food from a few workers rapidly reaching the majority of the colony as foragers donate their crop contents to groups of recipients and these recipients may themselves act as donors.Foragers respond to colony starvation by individually taking up more food and sharing this fluid with a greater proportion of nestmates. Even foragers from satiated colonies can retrieve at least small amounts of liquid.The forager's state of hunger plays an important role in regulating food distribution. In sugar-satiated nests, previously starved foragers are highly successful at passing on labelled sugar whereas prviously fed foragers are not.     

Control of food influx by temporal subcastes in the fire ant,Solenopsis invicta

Summary Temporal subcastes in the fire ant, Solenopsis invicta Buren were selectively starved to determine if foragers could assess the nutritional status of their nestmates and respond accordingly. We found that starved foragers increase the honey entering the colony (Fig. 1). When nurses are starved more oil and liquid egg yolk enters the colony (Figs. 2, 3) and when both reserves and nurses are starved, more egg yolk powder is brought in by the foragers (Fig. 4). When queens are starved, more liquid egg yolk and oil enters the colony (Figs. 2, 3). Starved larvae increase the oil in the colony (Fig. 2) and when held with nurses for 24h before feeding, increase the egg yolk powder brought in and receive significantly more of it than other subcaste members (Fig. 5). We conclude that foragers can respond to the nutritional needs of their nestmates. Based on our behavioural observations, the quantity of food brought in by the foragers is regulated via discriminatory solicitation by reserves in response to the nutritional needs of the nurses.     

The communal crop: modulation of sucrose response thresholds of pre-foraging honey bees with incoming nectar quality

We examined whether the quality (concentration) of incoming sucrose solutions returned by foraging honey bees affected the response thresholds of pre-foraging members of the colony. Six pairs of colonies were given ad libitum access to sucrose solution feeders. A colony from each pair was switched from 20–50% sugar concentration feeders while the other continued to have access to 20% sucrose feeders. Proboscis extension response (PER) scores to an increasing series of sucrose concentrations were significantly higher in pre-foragers of colonies foraging on 20% sucrose throughout compared to pre-foragers in colonies where foraging was switched to 50% sucrose. Although all colonies had honey stores, the concentration of sugar solution in non-foraging bees crops were significantly lower in bees from colonies foraging on 20% sucrose compared to those from colonies foraging on 50% sucrose. Because response thresholds to sugar of young bees were modulated by the concentration of sucrose solution returned to colonies, we repeated the 2000 study of Pankiw and Page that potentially confounded baseline response thresholds with modulated scores due to experience in the colony. Here, we examined PER scores to sucrose in bees within 6 h of emergence, prior to feeding experience, and their forage choice 2 to 3 weeks later. Pollen foragers had higher PER scores as newly emerged bees compared to bees that eventually became nectar foragers. These results confirm those of the 2000 study by Pankiw and Page. Combined, these experiments demonstrate that variation in pre-forager sucrose response thresholds are established prior to emerging as adults but may be modulated by incoming resources later on. Whether this modulation has long-term effects on foraging behavior is unknown but modulation has short-term effects and the potential to act as a means of communication among all bees in the colony.Communicated by M. Giurfa     

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.     

Honey bee foragers as sensory units of their colonies

Forager honey bees function not only as gatherers of food for their colonies, but also as sensory units shaped by natural selection to gather information regarding the location and profitability of forage sites. They transmit this information to colony members by means of waggle dances. To investigate the way bees transduce the stimulus of nectar-source profitability into the response of number of waggle runs, I performed experiments in which bees were stimulated with a sucrose solution feeder of known profitability and their dance responses were videorecorded. The results suggest that several attributes of this transduction process are adaptations to enhance a bee's effectiveness in reporting on a forage site. (1) Bees register the profitability of a nectar source not by sensing the energy gain per foraging trip or the rate of energy gain per trip, but evidently by sensing the energetic efficiency of their foraging. Perhaps this criterion of nectar-source profitability has been favored by natural selection because the foraging gains of honey bees are typically limited by energy expenditure rather than time availability. (2) There is a linear relationship between the stimulus of energetic efficiency of foraging and the response of number of waggle runs per dance. Such a simple stimulus-response function appears adequate because the range of suprathreshold stimuli (max/min ratio of about 10) is far smaller than the range of responses (max/min ratio of about 100). Although all bees show a linear stimulus-response function, there are large differences among individuals in both the response threshold and the slope of the stimulus-response function. This variation gives the colony a broader dynamic range in responding to food sources than if all bees had identical thresholds of dance response. (3) There is little or no adaptation in the dance response to a strong stimulus (tonic response). Thus each dancing bee reports on the current level of profitability of her forage site rather than the changes in its profitability. This seems appropriate since presumably it is the current profitability of a forage site, not the change in its profitability, which determines a site's attractiveness to other bees. (4) The level of forage-site quality that is the threshold for dancing is tuned by the bees in relation to forage availability. Bees operate with a lower dance threshold when forage is sparse than when it is abundant. Thus a colony utilizes input about a wide range of forage sites when food is scarce, but filters out input about low-reward sites when food is plentiful. (5) A dancing bee does not present her information in one spot within the hive but instead distributes it over much of the dance floor. Consequently, the dances for different forage sites are mixed together on the dance floor. This helps each bee following the dances to take a random sample of the dance information, which is appropriate for the foraging strategy of a honey bee colony since it is evidently designed to allocate foragers among forage sites in proportion to their profitability.     

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
     

Colony energy requirements affect the foraging currency of bumble bees

Summary This study examines whether the foraging behavior of worker bumble bees (Bombus: Apidae) collecting nectar on inflorescences of seablush (Plectritis congesta: Valerianaceae) is affected by colony energetic requirements, which were experimentally manipulated either by adding sucrose solution to honey pots or by removing virtually all available nectar from the pots. The competing hypotheses tested were: (1) no change; energetic requirements do not affect behavior, since there is a single best way to collect food in a given environment; (2) energetic currency; the energetic currency maximized by foragers changes according to colony energetic condition, with nectar-depletion causing a shift from maximizing long-term productivity to maximizing immediate energetic gain, thereby de-emphasizing energetic costs; and (3) predation; foragers devalue risk of predation as risk of starvation increaes, with colony nectar-depletion causing foragers to be less predation riskaverse in order to increase immediate energetic gain. Relative to when their colony energy reserves were enhanced, foragers from nectar-depleted colonies selected smaller inflorescences, visited fewer flowers per inflorescence, probed flowers at a higher rate while on each inflorescence, and walked between inflorescences less often, thereby spending a greater proportion of their foraging trip in flight. These behaviors increased a bee's energetic costs while foraging, and should also have increased its immediate energetic gains, allowing rejection of the no change hypothesis. Predictions of the predation hypothesis were generally not supported, and our results best support the energetic currency hypothesis. Foraging currency of bumble bees therefore appears to be a function of colony energetic state. Offprint requests to: R.V. Cartar     

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     

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.     

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     

The regulation of pollen foraging by honey bees: how foragers assess the colony's need for pollen

Summary The honey bee colony presents a challenging paradox. Like an organism, it functions as a coherent unit, carefully regulating its internal milieu. But the colony consists of thousands of loosely assembled individuals each functioning rather autonomously. How, then, does the colony acquire the necessary information to organize its work force? And how do individuals acquire information about specific colony needs, and thus know what tasks need be performed? I address these questions through experiments that analyze how honey bees acquire information about the colony's need for pollen and how they regulate its collection. The results demonstrate features of the colony's system for regulating pollen foraging: (1) Pollen foragers quickly acquire new information about the colony's need for pollen. (2) When colony pollen stores are supplemented, many pollen foragers respond by switching to nectar foraging or by remaining in the hive and ceasing to forage at all. (3) Pollen foragers do not need direct contact with pollen to sense the colony's change of state, nor do they use the odor of pollen as a cue to assess the colony's need for pollen. (4) Pollen foragers appear to obtain their information about colony pollen need indirectly from other bees in the hive. (5) The information takes the form of an inhibitory cue. The proposed mechanism for the regulation of pollen foraging involves a hierarchical system of information acquisition and a negative feedback loop. By taking advantage of the vast processing capacity of large numbers of individuals working in parallel, such a system of information acquisition and dissemination may be ideally suited to promote efficient regulation of labor within the colony. Although each individual relies on only limited, local information, the colony as a whole achieves a finely-tuned response to the changing conditions it experiences.     

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.     

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.     

Collective decision-making in honey bees: how colonies choose among nectar sources

Summary A honey bee colony can skillfully choose among nectar sources. It will selectively exploit the most profitable source in an array and will rapidly shift its foraging efforts following changes in the array. How does this colony-level ability emerge from the behavior of individual bees? The answer lies in understanding how bees modulate their colony's rates of recruitment and abandonment for nectar sources in accordance with the profitability of each source. A forager modulates its behavior in relation to nectar source profitability: as profitability increases, the tempo of foraging increases, the intensity of dancing increases, and the probability of abandoning the source decreases. How does a forager assess the profitability of its nectar source? Bees accomplish this without making comparisons among nectar sources. Neither do the foragers compare different nectar sources to determine the relative profitability of any one source, nor do the food storers compare different nectar loads and indicate the relative profitability of each load to the foragers. Instead, each forager knows only about its particular nectar source and independently calculates the absolute profitability of its source. Even though each of a colony's foragers operates with extremely limited information about the colony's food sources, together they will generate a coherent colonylevel response to different food sources in which better ones are heavily exploited and poorer ones are abandoned. This is shown by a computer simulation of nectar-source selection by a colony in which foragers behave as described above. Nectar-source selection by honey bee colonies is a process of natural selection among alternative nectar sources as foragers from more profitable sources survive (continue visiting their source) longer and reproduce (recruit other foragers) better than do foragers from less profitable sources. Hence this colonial decision-making is based on decentralized control. We suggest that honey bee colonies possess decentralized decision-making because it combines effectiveness with simplicity of communication and computation within a colony. Offprint requests to: T.D. Seeley     

Honeybees modify gustatory responsiveness after receiving nectar from foragers within the hive

Food quality is a relevant characteristic to be transferred within eusocial insect colonies because its evaluation improves the collective foraging efficiency. In honeybees, colony mates could directly acquire this resource characteristic during trophallactic encounters with nectar foragers. In the present study, we focused on the gustatory responsiveness of bees that have unloaded food from incoming foragers. The sugar sensitivity of receiver bees was assessed in the laboratory by using the proboscis extension response paradigm. After unloading, hive bees were captured either from a colony that foraged freely in the environmental surroundings or from a colony that foraged at an artificial feeder with a known sucrose solution. In the first situation, the sugar sensitivity of the hive bees negatively correlated with the sugar concentration of the nectar crops brought back by forager mates. Similarly, in the controlled situation, the highest sucrose concentration the receivers accepted during trophallaxis corresponded to the highest thresholds to sucrose. The results indicate that first-order receivers modify their sugar sensitivity according to the quality of the food previously transferred through trophallaxis by the incoming foragers. In addition, trophallaxis is a mechanism capable of transferring gustatory information in honeybees. Its implications at a social scale might involve changes in the social information as well as in nectar distribution within the colony.     

Social foraging by honeybees: how colonies allocate foragers among patches of flowers

Summary To understand how a colony of honeybees keeps its forager force focussed on rich sources of food, and analysis was made of how the individual foragers within a colony decide to abandon or continue working (and perhaps even recruit to) patches of flowers. A nectar forager grades her behavior toward a patch in response to both the nectar intake rate of her colony and the quality of her patch. This results in the threshold in patch quality for acceptance of a patch being higher when the colonial intake rate of nectar is high than when it is low. Thus colonies can adjust their patch selectivity so that they focus on rich sources when forage is abundant, but spread their workers among a wider range of sources when forage is scarce. Foragers assess their colony's rate of nectar intake while in the nest, unloading nectar to receiver bees. The ease of unloading varies inversely with the colonial intake rate of nectar. Foragers assess patch quality while in the field, collecting nectar. By grading their behavior steeply in relation to such patch variables as distance from the nest and nectar sweetness, foragers give their colony high sensitivity to differences in profitability among patches. When a patch's quality declines, its foragers reduce their rate of visits to the patch. This diminishes the flow of nectar from the poor patch which in turn stimulates recruitment to rich patches. Thus a colony can swiftly redistribute its forager force following changes in the spatial distribution of rich food sources. The fundamental currency of nectar patch quality is not net rate of energy intake, (Gain-Cost)/Time, but may be net energy efficiency, (Gain-Cost)/Cost.     

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     

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.