Waggle Research Articles

Intra-dance variation among waggle runs and the design of efficient protocols for honey bee dance decoding

SummaryNoise is universal in information transfer. In animal communication, this presents a challenge not only for intended signal receivers, but also to biologists studying the system. In honey bees, a forager communicates to nestmates the location of an important resource via the waggle dance. This vibrational signal is composed of repeating units (waggle runs) that are then averaged by nestmates to derive a single vector. Manual dance decoding is a powerful tool for studying bee foraging ecology, although the process is time-consuming: a forager may repeat the waggle run 1- >100 times within a dance. It is impractical to decode all of these to obtain the vector; however, intra-dance waggle runs vary, so it is important to decode enough to obtain a good average. Here we examine the variation among waggle runs made by foraging bees to devise a method of dance decoding. The first and last waggle runs within a dance are significantly more variable than the middle run. There was no trend in variation for the middle waggle runs. We recommend that any four consecutive waggle runs, not including the first and last runs, may be decoded, and we show that this methodology is suitable by demonstrating the goodness-of-fit between the decoded vectors from our subsamples with the vectors from the entire dances.

How dancing honey bees keep track of changes: the role of inspector bees

How do honey bees track changes in their foraging environment? Previously, 2 complementary mechanisms have been identified by which bees can effectively switch between food sources when their relative quality changes. First, an increase in profitability of a food source elicits an increase in waggle dances (the bees’ recruitment mechanism) for that source. Second, bees that have retired from foraging at a food source make occasional inspection visits to that food source and resume foraging if its quality improves. Here, we investigate, using both field experiments and a mathematical model, the relative importance of these 2 mechanisms. By manipulating dance information available to the bees, we find that when food sources change quality frequently, inspector bees provide a rapid response to changes, whereas the waggle dance contributes to a response over a longer time period. The bees’ ability to switch feeders without dance language information was found to be robust with respect to the spatial configuration of the feeders. Our results show that individual memory, in the form of inspector bees, and collective communication can interact to allow an insect colony to adapt to changes on both short and long timescales. Key words: Apis mellifera, collective memory, dynamic environment, foraging, honey bee, mathematical modeling. [Behav Ecol]

The dance legacy of Karl von Frisch

Karl von Frisch published “Die Tanze der Bienen” in 1946, which demonstrated that successful honey bee foragers perform a stereotyped dance to communicate the location of valuable resources to her nestmates. This discovery proved to be the starting point of many areas of investigation. Here I review some recent advancement in our understanding of the waggle dance.

Energetically optimal foraging strategy is emergent property of time-keeping behavior in honey bees

Forager honey bees exhibit a robust time memory, based on an endogenous circadian clock, enabling them to schedule their flights to coincide with the nectar presentation of known food sources. They retain this time memory for several consecutive days even in the absence of nectar rewards. Recent work has identified 2 classes of forager: ‘‘persistent’’ foragers that reconnoiter a known food source to ascertain its status and ‘‘reticent’’ foragers that apparently wait in the hive for a waggle dance confirming source availability. Surprisingly, a foraging group contains 40‐90% persistent foragers, depending on experience at the source. What is the benefit in sending so many foragers to investigate a source when only a few foragers are required to reactivate the entire group? We used an agent-based software model to test the energetics underlying several different ratios of persistent and reticent individuals in the foraging group while varying 6 ecological factors: forager group size, source distance, source sucrose concentration, source availability in hours, number of days the source is known to the colony, and the rate at which new unemployed foragers appear on the dance floor. Our model demonstrates 2 primary explanations. First, a large number of persistent foragers are needed to ensure that at least some foragers will reconnoiter their source early in its availability, thus enabling the group to effectively exploit the source. Second, the cost of a reconnaissance flight is negligible compared with even a single successful foraging trip. Key words: agent-based model, circadian rhythms, food-anticipatory activity, foraging, honey bees, time memory. [Behav Ecol]

How habitat affects the benefits of communication in collectively foraging honey bees.

Honey bees (Apis mellifera) use the dance language to symbolically convey information about the location of floral resources from within the nest. To figure out why this unique ability evolved, we need to understand the benefits it offers to the colony. Previous studies have shown that, in fact, the location information in the dance is not always beneficial. We ask, in which ecological habitats do honey bee colonies actually benefit from the dance language, and what is it about those habitats that makes communication useful? In this study, we examine the effects of floral distribution patterns on the benefits of dance communication across five different habitats. In each habitat, we manipulated colonies' ability to communicate and measured their foraging success, while simultaneously characterizing the naturally occurring floral distribution. We find that communication is most beneficial when floral species richness is high and patches contain many flowers. These are ecological features that could have helped shape the evolution of the honey bee dance language.

Morphological properties of neurons in the honeybee auditory system

Morphological properties of neurons in the honeybee auditory system

ミツバチの尻振りダンスと採餌行動における効果

ミツバチの尻振りダンスと採餌行動における効果

The recruiter's excitement – features of thoracic vibrations during the honey bee's waggle dance related to food source profitability

The honey bee's waggle dance constitutes a remarkable example of an efficient code allowing social exploitation of available feeding sites. In addition to indicating the position (distance, direction) of a food patch, both the occurrence and frequency of the dances depend on the profitability of the exploited resource (sugar concentration, solution flow rate). During the waggle dance, successful foragers generate pulsed thoracic vibrations that putatively serve as a source of different kinds of information for hive bees, who cannot visually decode dances in the darkness of the hive. In the present study, we asked whether these vibrations are a reliable estimator of the excitement of the dancer when food profitability changes in terms of both sugar concentration and solution flow rate. The probability of producing thoracic vibrations as well as several features related to their intensity during the waggle phase (pulse duration, velocity amplitude, duty cycle) increased with both these profitability variables. The number of vibratory pulses, however, was independent of sugar concentration and reward rate exploited. Thus, pulse number could indeed be used by dance followers as reliable information about food source distance, as suggested in previous studies. The variability of the dancer's thoracic vibrations in relation to changes in food profitability suggests their role as an indicator of the recruiter's motivational state. Hence, the vibrations could make an important contribution to forager reactivation and, consequently, to the organisation of collective foraging processes in honey bees.

Honey bees use social information in waggle dances more fully when foraging errors are more costly

Social animals can obtain valuable information from group members, but sometimes experience conflicts between this social information and personal information obtained through their own experience. Experienced honey bee foragers (Apis mellifera) have personal information about familiar food sources, and can also obtain social information by following waggle dances. However, it is unclear whether temporarily unemployed foragers whose visits to a food source have been interrupted make full use of social information from dancers or rely primarily on their own personal information to determine whether their familiar food source is active again. We hypothesized that experienced foragers should pay more attention to the social information in waggle dances when foraging errors that can arise from ignoring social information are more costly. We manipulated the cost of mistakenly flying to a familiar but unprofitable food source by training bees to visit feeders that were either close (100 m) or far (1000 m) from the hive and found that temporarily unemployed foragers who had been trained to forage at more distant feeders were more likely to pay attention to social information about food source location. Our findings demonstrate that experienced forager bees can flexibly alter the extent to which they rely on social, as opposed to personal, information and are more likely to fully utilize social information from dancers when foraging errors are more costly. Key words: Apis mellifera, communication, dance language, reactivation, social information, waggle dance. [Behav Ecol]

Hydrocarbons emitted by waggle-dancing honey bees stimulate colony foraging activity by causing experienced foragers to exploit known food sources

Two hypotheses concerning the function of the hydrocarbons emitted by waggle-dancing bees are investigated in this study. First, we test the hypothesis that the waggle-dance compounds stimulate foraging behavior. In support of this hypothesis, the number of bee departures from a hive increased as much as 46% and the number of forager visits to a feeder station increased as much as 106% when the dance compounds were introduced into the hive. Second, we test the hypothesis that the waggle-dance compounds stimulate foraging by causing experienced foragers to depart the hive to exploit known food sources. In support of this hypothesis, individually marked foragers visited an empty feeder station both more often and in greater numbers following exposure to the waggle-dance compounds than following exposure to a control substance. The results of these experiments suggest that the waggle-dance compounds function as a foraging semiochemical, operating in synergy with the waggle dance itself.

Analysis of the Waggle Dance Motion of Honeybees for the Design of a Biomimetic Honeybee Robot

The honeybee dance “language” is one of the most popular examples of information transfer in the animal world. Today, more than 60 years after its discovery it still remains unknown how follower bees decode the information contained in the dance. In order to build a robotic honeybee that allows a deeper investigation of the communication process we have recorded hundreds of videos of waggle dances. In this paper we analyze the statistics of visually captured high-precision dance trajectories of European honeybees (Apis mellifera carnica). The trajectories were produced using a novel automatic tracking system and represent the most detailed honeybee dance motion information available. Although honeybee dances seem very variable, some properties turned out to be invariant. We use these properties as a minimal set of parameters that enables us to model the honeybee dance motion. We provide a detailed statistical description of various dance properties that have not been characterized before and discuss the role of particular dance components in the commmunication process.

Neural representation for distance and direction of resource for honeybees

Many insects manage their foraging behaviors or prey detection based on resource information. Their brain system should encode the resource location efficiently. Honeybees remember the nectar source location and communicate with their colleagues using their own dance language [1]. Desert ants demonstrate elegant homing navigation with path integration [2] and they can estimate the homing vector, distance and direction. We presume they may have common neural structure and representation for the resource vector or homing vector. For the resource vector, we can build a neural network consisting of two layers of neurons, which has a polar form representation. Each neuron is one of directionally selective neurons and also includes the information of the distance. For the distance information, the activation in direction-cell neurons has the exponential form of inhibition to the distance neuron as gate neurons, which resembles multiplicative neurons [3]. A population of the neurons efficiently encodes the resource location, that is, the distance and direction of the resource. The resource vector representation can be applied to honeybees or other insects. It is known that two types of dances in honeybees’ dance communication, waggle dances and sickle dances, has the information of resource vector. It has been pointed out that waggle dance has several cues, vibration, odor, air flow and tactile information. From the sickle dance, the colleagues on following the dancer bee can continuously records the duration and direction of its temporal path, and accumulate the information, which finally provides the net distance and direction of the resource from the comb. We suggest the mechanism is similar to the path integration system, although the accumulated distance is replaced by the accumulated duration in the preferred direction in the dance translation. The distance to the resource is involved with duration of the waggle run and duration of the return run [4]. In that point, the neural network can represent the resource information well.

A new approach for the simultaneous tracking of multiple honeybees for analysis of hive behavior

Social activities are among the most striking of animal behaviors, and the clarification of their mechanisms is a major subject in ethology. Honeybees are a good model for revealing these mechanisms because they display various social behaviors, such as division of labor, in their colonies. Image processing is a precise and convenient tool for obtaining animal behavior data, but even recent methods are inadequate for the identification or description of honeybee behavior. This is because of the difficulty distinguishing between the large number of individuals in a small hive and their multiple movements. The present study developed a new computer-aided system, using a vector quantization method, for the identification and behavioral tracking of individual honeybees. The vector quantization method enabled separation of honeybee bodies in photographs recorded as a movie. This system succeeded in analyzing a huge number of frames quickly and can thus save both time and labor. Moreover, the system identified more than 72% of the bees in a hive and found and determined the active areas in the hive by extracting the trajectories of walking bees. In addition, useful behavioral data on the honeybee waggle dance were obtained using the present system.

Consistent personality differences in house-hunting behavior but not decision speed in swarms of honey bees (Apis mellifera)

Speed-accuracy tradeoffs are a common feature of decision-making processes, both in individual animals and in groups of animals working together to reach a single collective decision. Individual organisms display consistent differences in their “impulsivity,” and vary in their tendency to make rapid, impulsive choices as opposed to slower, more accurate decisions. However, we do not yet know whether groups of animals consistently differ in their tendency to prioritize decision speed over accuracy. We challenged 17 swarms of honey bees (Apis mellifera) to simultaneously choose a new nest site in each of three locations, and measured their decision speeds in each trial. We found that swarms displayed consistent personality differences in the number of waggle dances and shaking signals they performed and in how actively they scouted for new nest sites. However, swarms did not consistently differ in how long they took to choose a nest site. We suggest that house-hunting A. mellifera swarms may place an especially high emphasis on decision accuracy when choosing a nest site, and that chance events—such as the time when each swarm discovers a sufficiently high-quality nest site—may consequently play a greater role in determining a swarm’s decision speed than intrinsic characteristics such as a swarm’s “impulsivity.”

How do honeybees attract nestmates using waggle dances in dark and noisy hives?

It is well known that honeybees share information related to food sources with nestmates using a dance language that is representative of symbolic communication among non-primates. Some honeybee species engage in visually apparent behavior, walking in a figure-eight pattern inside their dark hives. It has been suggested that sounds play an important role in this dance language, even though a variety of wing vibration sounds are produced by honeybee behaviors in hives. It has been shown that dances emit sounds primarily at about 250–300 Hz, which is in the same frequency range as honeybees' flight sounds. Thus the exact mechanism whereby honeybees attract nestmates using waggle dances in such a dark and noisy hive is as yet unclear. In this study, we used a flight simulator in which honeybees were attached to a torque meter in order to analyze the component of bees' orienting response caused only by sounds, and not by odor or by vibrations sensed by their legs. We showed using single sound localization that honeybees preferred sounds around 265 Hz. Furthermore, according to sound discrimination tests using sounds of the same frequency, honeybees preferred rhythmic sounds. Our results demonstrate that frequency and rhythmic components play a complementary role in localizing dance sounds. Dance sounds were presumably developed to share information in a dark and noisy environment.

Dance Type and Flight Parameters Are Associated with Different Mushroom Body Neural Activities in Worker Honeybee Brains

BackgroundHoneybee foragers can transmit the information concerning the location of food sources to their nestmates using dance communication. We previously used a novel immediate early gene, termed kakusei, to demonstrate that the neural activity of a specific mushroom body (MB) neuron subtype is preferentially enhanced in the forager brain. The sensory information related to this MB neuron activity, however, remained unclear.Methodology/Principal FindingsHere, we used kakusei to analyze the relationship between MB neuron activity and types of foraging behavior. The number of kakusei-positive MB neurons was higher in the round dancers that had flown a short distance than in the waggle dancers that had flown a long distance. Furthermore, the amount of kakusei transcript in the MBs inversely related to the waggle-phase duration of the waggle dance, which correlates with the flight distance. Using a narrow tunnel whose inside was vertically or axially lined, we manipulated the pattern of visual input, which is received by the foragers during flight, and analysed kakusei expression. The amount of kakusei transcript in the MBs was related to the foraging frequency but not to the tunnel pattern. In contrast, the number of kakusei-positive MB neurons was affected by the tunnel patterns, but not related to foraging frequency.Conclusions/SignificanceThese results suggest that the MB neuron activity depends on the foraging frequency, whereas the number of active MB neurons is related to the pattern of visual input received during foraging flight. Our results suggest that the foraging frequency and visual experience during foraging are associated with different MB neural activities.

A Common Frame of Reference for Learned and Communicated Vectors in Honeybee Navigation

Humans draw maps when communicating about places or verbally describe routes between locations. Honeybees communicate places by encoding distance and direction in their waggle dances. Controversy exists not only about the structure of spatial memory but also about the efficiency of dance communication. Some of these uncertainties were resolved by studies in which recruits' flights were monitored using harmonic radar. We asked whether the two sources of vector information--the previously learned flight vector to a food source and the communicated vector--are represented in a common frame of spatial reference. We found that recruits redirect their outbound flights and perform novel shortcut flights between the communicated and learned locations in both directions. Guidance by beacons at the respective locations or by the panorama of the horizon was excluded. These findings indicate a spatial reference based on either large-scale vector integration or a common geocentric map-like spatial memory. Both models predict a memory structure that stores the spatial layout in such a way that decisions are made according to estimated distances and directions. The models differ with respect to the role of landmarks and the time of learning of spatial relations.

Bee colony intelligence in zone constrained two-sided assembly line balancing problem

Bees Algorithm is a relatively new member of swarm intelligence based meta-heuristics which tries to model natural behavior of real honey bees in food foraging. Honey bees use several mechanisms like waggle dance to optimally locate food sources and to search new ones. This makes them a good candidate for developing new search algorithms for solving optimization problems in operational research. On the other hand, two-sided assembly lines are generally occurred in assembly of large-sized products such as buses and trucks. In a two-sided assembly line, different assembly tasks are carried out on the same product in parallel to both left and right sides of the line. In this study Bees Algorithm is adopted to solve two-sided assembly line balancing problem with zoning constraint so as to minimize the number of stations for a given cycle time. An extensive computational study is carried out and the results are compared with the results of several algorithms from the literature with the results of exact solution approaches and several algorithms from the literature such as ant colony optimization, tabu search.

Honeybee foragers increase the use of waggle dance information when private information becomes unrewarding

Social insect foragers often have access to both social and private information about the locations of food sources. In honeybees, Apis mellifera, foragers can follow waggle dances (social information) to obtain vector information about the location of profitable food sources or they can use route memories (private information) acquired during previous foraging trips. The relative use of social information versus private information is poorly understood and currently debated. It is hypothesized that social information should be prioritized when the use of private information has a low benefit. We tested this hypothesis by training foragers to a high-quality 2 M sucrose feeder, which subsequently became unrewarding. As foragers continued to experience zero reward from their private route information they increased the time spent following waggle dances advertising an alternative food source with the same odour. A significant proportion of foragers successfully switched to the food source indicated by dances. Overall, trained foragers showed a strong attachment to the known but currently unrewarding feeder, even after repeatedly following dances advertising a profitable alternative. Successful recruits to the novel food source advertised by the waggle dances had more social information about this source in that they had followed dances for longer. Our results suggest that honeybee foragers follow a strategy that is conservative in terms of switching from one food patch to another.

Honey bee forager thoracic temperature inside the nest is tuned to broad-scale differences in recruitment motivation

Insects that regulate flight muscle temperatures serve as crucial pollinators in a broad range of ecosystems, in part because they forage over a wide span of temperatures. Honey bees are a classic example and maintain their thoracic muscles at temperatures (T(th)) tuned to the caloric benefits of floral resources. Using infrared thermography, we tested the hypothesis that forager motivation to recruit nestmates for a food source is positively correlated with T(th). We trained bees to a sucrose feeder located 5-100 m from the nest. Recruiting foragers had a significantly higher average T(th) (2.7°C higher) when returning from 2.5 mol l(-1) sucrose (65% w/w) than when returning from 1.0 mol l(-1) sucrose (31% w/w). Foragers exhibited significantly larger thermal fluctuations the longer they spent inside the nest between foraging trips. The difference between maximum and minimum temperatures during a nest visit (T(range)) increased with total duration of the nest visit (0.7°C increase per additional min spent inside the nest). Bees that recruited nestmates (waggle or round danced) were significantly warmer, with a 1.4-1.5 times higher ΔT(th) (difference between T(th) and nest ambient air temperature) than bees who tremble danced or simply walked on the nest floor without recruiting between foraging bouts. However, recruiter T(th) was not correlated with finer-scale measures of motivation: the number of waggle dance circuits or waggle dance return phase duration. These results support the hypothesis that forager T(th) within the nest is correlated to broad-scale differences in foraging motivation.