Hearing in honeybees: localization of the auditory sense organ

Airborne sound signals emitted by dancing honeybees (Apis mellifera) contain information about the locations of food sources. Honeybees can perceive these near field sounds and rely on them to decode the messages of the dance language. The dance sound is characterized by rhythmical air particle movement of high velocity amplitudes. The aim of the present study was to identify the sensory structures used to detect near field sound signals. In an operant conditioning experiment, bees were trained to respond to sound. Ablation experiments with these trained bees revealed that neither mechanosensory hairs on the antennae or head nor bristle fields at the joints of the antenna, but Johnston's organ, a chordotonal organ in the pedicel of the antenna, is used to detect near field sound in honeybees.     

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.     

Hearing in the Asian honeybeesApis dorsata andApis florea

Summary In the dance language of the western honeybee,Apis mellifera, airborne near field sound signals and a sense of hearing are used to communicate the locations of food sources. In the Asian honeybeeApis dorsata similar acoustical signals have been found recently, whereasApis florea does not emit dance sounds to transfer information about the location of food sources. The aim of the present study was to investigate the sense of hearing in these two species. Operant conditioning experiments reveal that both species are able to detect such near field sounds. The results support the hypothesis of acoustical communication inApis dorsata. The auditory sense ofApis florea, which does not use acoustical signals in the dance language, is discussed as a preadaptation for the evolution of an acoustical dance communication in ancestral honeybees.     

基于COⅠ基因序列的蜜蜂属系统发育分析及其舞蹈和筑巢行为进化分析

【目的】分析蜜蜂属Apis的系统发育关系,并在此基础上探讨蜜蜂属舞蹈方向、舞蹈声音、营巢环境、巢脾结构的祖先状态和演变过程。【方法】PCR扩增并测定中国分布的蜜蜂属内东方蜜蜂A. cerana、西方蜜蜂A. mellifera、大蜜蜂A. dorsata、黑大蜜蜂A. laboriosa、小蜜蜂A. florea和黑小蜜蜂A. andreniformis的线粒体COⅠ基因序列,并从NCBI数据库中下载分布于其他国家或地区的上述6种蜜蜂以及绿努蜂A. nulunsis、苏拉威西蜂A. nigrocinta、沙巴蜂A. koschevnikovi、炳式大蜜蜂A. dorsata binghami的COⅠ同源序列。分别利用最大简约法(MP)、最大似然法(ML)和贝叶斯分析(BI)依据这些序列数据构建蜜蜂属系统发育关系。对蜜蜂属上述种的舞蹈语言和筑巢行为进行编码并作为性状特征标记到系统发育树中,利用简约法对祖先状态进行追溯。【结果】系统发育分析结果表明,蜜蜂属可划分为3大类群,即穴居蜜蜂类群(东方蜜蜂、西方蜜蜂、苏拉威西蜂、绿努蜂、沙巴蜂)、大蜜蜂类群(大蜜蜂、黑大蜜蜂)和小蜜蜂类群(小蜜蜂、黑小蜜蜂);小蜜蜂类群更加接近于祖型,大蜜蜂类群和穴居蜜蜂类群是两支单系;炳式大蜜蜂是独立于大蜜蜂和黑大蜜蜂的蜂种,且与黑大蜜蜂的亲缘关系更近。祖先状态重建结果显示：蜜蜂属祖先在露天环境下筑造垂直的单脾,且在传播食物或巢址信息时跳水平方向的无声摆尾舞,有嗡嗡声的舞蹈及筑造复脾是后来形成的。【结论】COⅠ基因可作为分子标记用于分析蜜蜂属的舞蹈和筑巢行为的祖先状态及进化过程;蜜蜂筑造复脾、跳有嗡嗡声的舞蹈是后期的适应性进化行为。     

A comparison of the dance language in<Emphasis Type="Italic"> Apis mellifera carnica</Emphasis> and<Emphasis Type="Italic"> Apis florea</Emphasis> reveals striking similarities

Honeybees have a dance language by which successful foragers inform nestmates about attractive food patches. The classical concept of dialects in the dance language of honeybees points to two differences in the dances by different species and races, firstly in the flight distance at which the dancers start performing waggle dances instead of round dances, and secondly in the circuit duration of the waggle dance performed for a given flight distance. However, recent findings have indicated that the dance language is influenced and affected by a number of parameters, both genetic and environmental. The current study was carried out to see whether the distance at which dancers change from round dances to waggle dances is statistically different in two different species, Apis mellifera carnica and A. florea and to develop a set of definitions for such comparative studies. Results show that the two species do not differ in the relative proportion of waggle dances and round dances performed at a given distance. Thus, this study points to the need of addressing the dialect question again.     

Hearing in honeybees: the mechanical response of the bee's antenna to near field sound

In the dance language, honeybees use airborne near field sound signals to inform their nestmates of the location of food sources. In behavioral experiments it has recently been shown that Johnston's organ, a chordotonal organ located in the pedicel of the antenna, is used to perceive these sound signals. In the present study the mechanical response of the antennal flagellum to stimulation with near field sound signals was investigated using laser vibrometry. The absolute amplitudes of antennal deflection with acoustical stimulation, the response to sounds of different displacement and velocity amplitudes, the shape of movement of the flagellum, the mechanical frequency response and the mechanical directional sensitivity of the auditory sense organ of the honeybee are described. Using pulsed stimuli simulating the dance sounds it is shown that the temporal pattern of the dance sound is resolved on the level of antennal vibrations.     

Honeybees (Apis mellifera) modulate dance communication in response to pollution by imidacloprid

Imidacloprid, one of the most commonly used insecticides, is highly toxic to honeybees and other beneficial insects. Imidacloprid is a chloronicotinyl insecticide, which has a highly specific affinity to the nicotinic acetylcholine receptors (nAChRs) in the honeybee’s nervous system. So it may interfere with dance behavior and memory formation. We found the waggle dances were modulated in honeybees fed sucrose water containing imidacloprid (pesticide group) compared to those fed normal sucrose water (control group). In our data, dancers of the pesticide group significantly increased the variance of divergence angle and the return phases in waggle dances than the control group. And the dance followers in pesticide group significantly increased the variance of crop content than the control group. Furthermore, four learning and memory related genes were significantly regulated at the gene expression levels between pesticide and control group. Our data revealed that the sub-lethal dose of imidacloprid impaired the honeybees’ learning and memory and resulted in cognitive disorder. The dancers may adjust their recruitment behavior leading to the observed reduced number of followers. We conclude that modulation of in-hive communication serves to protect the colony from foraging toxic food.     

Responses to light under varying magnetic conditions in the honeybee,Apis mellifica

Summary In the dance of honeybees the indication of direction to a food source can be influenced by magnetic and photic stimuli. We have tested the behaviour of dancing honeybees illuminated with white light under varying magnetic conditions. The bees respond to the light stimulus with a maximum deviation from the correct dancing direction when they dance parallel to the inclination of the earth's magnetic field (EMF). The response to light drops to zero with increasing deviation from this zero-point direction (see also Martin and Lindauer 1977). The time of total indifference to light varies with the magnetic conditions. In the natural EMF the reaction to light becomes zero 20.3° (i.e. 1 h) after the bees have passed the zeropoint. In the compensated EMF this effect is delayed by 10°. The bees show nearly no reaction to light when the EMF is amplified to 2 Gauss.The relative spectral sensitivity of dancing honey-bees was tested in the compensated EMF. It is 1:1.63:2.64 for green-, blue-, and UV-light, respectively.Abbreviation EMF earth's magnetic field     

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.     

Waggle dances in absconding colonies of the red dwarf honeybee, Apis florea

The directional information encoded in the waggle dances of absconding colonies of Apis florea shows how different sites are advertised during decision-making. Colonies of A. florea were observed from the inception of absconding until the swarm settled at a new nest site. The number of waggle dancers at the beginning of the absconding sequence was low, gradually increased and then declined shortly before liftoff. During the last 2 to 0.5?h before liftoff, the dances still indicated different directions. This significantly decreased in the last 0.5?h until only one or two dance directions were being advertised. All colonies reached a near consensus in the last 20 dances before liftoff. The swarm flight path is meandering so the actual distance flown is about twice that indicated by the dances. During the last 3?min the waggle dance in most colonies showed nest target angles that were closely clustered indicating that the final directions advertised were close to the chosen target site. In all absconding/migratory species of honeybees thus far studied, there is a special dance associated with absconding that appears not to select specific destinations but rather a particular direction in search of a new nesting area.     

Mechanisms of dance orientation in the Asian honey beeApis florea L.

Summary Early studies of dance communication inApis florea had shown that waggle dances are not performed on a vertical plane and oriented to gravity, as in the other species ofApis, but instead take place on the flattened top of the exposed comb and are oriented to celestial cues directly. More recent experiments showed thatA. florea can dance in the absence of a view of the sun or blue sky, but did not establish what mechanism permitted this orientation. I now report that dances can be oriented directly to landmarks visible from the nest, the first evidence of an environmental feature other than celestial cues or gravity being involved in dance orientation. Landmarks near the nest are probably used to refer to celestial cues, in a fashion analogous to the use of broad features of the landscape by honeybees in order to learn the sun's course, which permits them to determine their flight angle on overcast days or at night, and to compensate accurately for solar movement.Apis florea may therefore be able to learn the sun's course with respect to two sets of landmarks.In other experiments I have examined the influence of slope onA. florea's dance orientation to visual references. In the first extensive observations of its dances on a vertical plane, I have amply confirmed that this species cannot transpose light and gravity in setting its dance angle, as the other species ofApis can. Nor do dancers orient so as to match visual information seen during the dance with that remembered from the flight. Patterns in the data when the same patch of sky was presented from different angles suggest instead thatA. florea continues to orient to projections of celestial cues onto the horizontal plane even when dancing on a steep slope. This compensation for slope may involve an ability to detect gravity and factor it out in aligning the dance to celestial cues.These insights suggest thatA. florea's dance orientation system has been adapted to requirements imposed by its nesting behavior, and has diverged sharply from the system shared by the other species ofApis.     

Mathematical analysis of the honeybee waggle dance

A honeybee informs her nestmates of the location of a flower by doing a waggle dance. The waggle dance encodes both the direction of and distance to the flower from the hive. To reveal how the waggle dance benefits the colony, we created a Markov model of bee foraging behavior and performed simulation experiments by incorporating the biological parameters that we obtained from our own observations of real bees as well as from the literature. When two feeders were each placed 400 m away from the hive in different directions, a virtual colony in which honeybees danced and correctly transferred information (a normal, real bee colony) made significantly greater numbers of successful visits to the feeders compared to a colony with inaccurate information transfer. Howerer, when five feeders were each located 400 m from the hive, the inaccurate information transfer colony performed better than the normal colony. These results suggest that dancing's ability to communicate accurate information depends on the number of feeders. Furthermore, because non-dancing colonies always made significantly fewer visits than those two colonies, we concluded that dancing behavior is beneficial for hives' ability to visit food sources.     

Pulsed mass recruitment by a stingless bee, Trigona hyalinata

Research on bee communication has focused on the ability of the highly social bees, stingless bees (Hymenoptera, Apidae, Meliponini) and honeybees (Apidae, Apini), to communicate food location to nest-mates. Honeybees can communicate food location through the famous waggle dance. Stingless bees are closely related to honeybees and communicate food location through a variety of different mechanisms, many of which are poorly understood. We show that a stingless bee, Trigona hyalinata, uses a pulsed mass-recruitment system that is highly focused in time and space. Foragers produced an ephemeral, polarized, odour trail consisting of mandibular gland secretions. Surprisingly, the odour trail extended only a short distance away from the food source, instead of providing a complete trail between the nest and the food source (as has been described for other stingless bees). This abbreviated trail may represent an intermediate strategy between full-trail marking, found in some stingless bees, and odour marking of the food alone, found in stingless bees and honeybees.     

The Significance of Odor Cues and Dance Language Information for the Food Search Behavior of Honeybees (Hymenoptera: Apidae)

Although several independent lines of evidence show that bees can make use of information provided by their dance language, there is an ongoing controversy about the significance of the dance information versus odor cues in the search behavior of recruited bees. A series of experiments was performed to assess the relative significance of dance information and odors for the site-specific search of recruit bees. In these experiments recruit bees were trapped automatically at arrays of artificial flowers at various distances from the hive. The distribution of directions in which the recruits searched for food was compared between recruitment by dancers performing well-oriented dances on the vertical side of the comb and dancers performing disoriented dances on a horizontal comb. The results show quantitatively that bees use both odor cues and the dance information. The greater the distance to the feeding site, the greater is the relative significance of the dance information.     

Increase in dance imprecision with decreasing foraging distance in the honey bee <Emphasis Type="Italic">Apis mellifera</Emphasis> L. is partly explained by physical constraints

Honey bee foragers communicate the direction and distance of both food sources and new nest sites to nest mates by means of a symbolic dance language. Interestingly, the precision by which dancers transfer directional information is negatively correlated with the distance to the advertised food source. The ‘tuned-error’ hypothesis suggests that colonies benefit from this imprecision as it spreads recruits out over a patch of constant size irrespective of the distance to the advertised site. An alternative to the tuned-error hypothesis is that dancers are physically incapable of dancing with great precision for nearby sources. Here we revisit the tuned-error hypothesis by studying the change in dance precision with increasing foraging distance over relatively short distances while controlling for environmental influences. We show that bees indeed increase their dance precision with the increase in foraging distance. However, we also show that dances performed by swarm-scouts for a nearby (30 m) nest site, where there could be no benefit to imprecision, are either without or with only limited directional information. This result suggests that imprecision in dance communication is caused primarily by physical constraints in the ability of dancers to turn around quickly enough when the advertised site is nearby.     

Rapid partner switching may facilitate increased broadcast group size in dance compared with conversation groups

Dancing is a universal human activity that involves exertive rhythmic movement to music. It is often conducted in a social environment and often involves synchronization. It has been found to cause dancers to bond socially. Like conversation, it has been suggested that dancing may be an inexpensive form of social bonding, in that both activities facilitate efficient group bonding by allowing multiple individuals to bond simultaneously. However, no previous study has systematically observed the size of naturally occurring dance groups. During unobtrusive observation of natural dance and conversation behavior, we found that the cumulative number of dance partners (cumulative group) was greater than the number of partners at any one moment (instantaneous group), whereas no such difference was found for conversation. Additionally, the length of uninterrupted engagement (bout) was negatively predicted by group size in conversation but not dance groups, and it was significantly longer in conversation groups than dance groups. Finally, instantaneous group size was significantly larger in dance than conversation groups, and also positively related to time spent synchronizing in dance groups. Together, these results suggest that dance may allow a larger number of individuals to simultaneously engage with each other than conversation does because (i) more rapid partner switching increases cumulative broadcast group; and (ii) synchrony facilitates simultaneous interaction with multiple individuals, allowing for larger instantaneous groups. We conclude that the capacity for information transfer provided by language comes at a cost in terms of social bonding, and that dance may have played an important role in bonding large hominin social groups.     

Do introduced honeybees (Apis mellifera,Hymenoptera) provide full pollination service to bird‐adapted Australian plants with small flowers? An experimental study of Brachyloma ericoides (Epacridaceae)

Abstract In many previous studies of the effects of introduced honeybees on Australian ecosystems, it has been assumed that floral morphology is a primary factor determining whether introduced honeybees will be effective in pollinating endemic plants. Although both honeybees and birds contacted stigmas and anthers of the small‐flowered Brachyloma ericoides (Epacridaceae), the exclusion of birds but not honeybees resulted in a significantly lower proportion of flowers producing capsules (12.3 ± 2 vs 21.0 ± 2%). This suggests that native birds contributed significantly to fruit set even though honeybees were much more frequent visitors to flowers (5–6 vs 0.7–2.5 times per day) and moved more frequently between plants (25 vs 12.2% of movements). Fruit set following exposure to birds and honeybees was very low compared with shrub species in general and may have been limited by the pre‐emptive removal of pollen by the 10% of honeybees that actively collected pollen.     

Impacts of hive honeybees on Tasmanian leatherwood Eucryphia lucida Labill. (Eucryphiaceae)

Despite honeybees (Apis mellifera L.) occurring as a feral and commercially managed species in many parts of Australia, the effects of honeybees on native Australian ecosystems are poorly understood. We examined the impacts of honeybee apiaries on Tasmanian Leatherwood Eucryphia lucida Labill. (Eucryphiaceae) by comparing commercial apiary sites with control sites >2 km from the nearest apiary. Feral honeybees were common at control sites (73% of honeybees feral) but were scarce at apiary sites (2%), and hive honeybees appeared to be competitively displacing feral honeybees near apiaries. Visit rates by native insects appeared to be un‐affected by the increased numbers of hive honeybees near apiaries. Standing crops of nectar sugar were significantly depressed at apiary sites. Pollen was rapidly removed from flowers at apiary sites resulting in full separation of the male and female flower‐phases (flowers completely dichogamous). In contrast, at control sites, pollen tended to remain in flowers into the female phase (flowers partially dichogamous). There was no difference in the total number of pollen grains deposited on stigmas or in percentage seed set among apiary and control sites. However, fruit set was elevated at apiary sites, possibly owing to reduced autonomous (within‐flower) selfing. Our study indicated that honeybees significantly reduce floral resources (nectar and pollen) around apiaries, although any competitive effects on native insects may have been obscured by large variation in the abundance of native insects among experimental sites.