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.     

Hearing in honeybees: operant conditioning and spontaneous reactions to airborne sound

Summary Airborne sound signals emitted by dancing bees (Apis mellifera) play an essential role in the bees' dance communication. It has been shown earlier that bees can learn to respond to airborne sounds in an aversive conditioning paradigm. Here we present a new training paradigm. A Y-choice situation was used to determine the frequency range and amplitude thresholds of hearing in bees. In addition, spontaneous reactions of bees to airborne sound were observed and used to determine thresholds of hearing. Both methods revealed that bees are able to detect sound frequencies up to about 500 Hz. The hearing threshold is 100–300 mm/s peak-to-peak velocity and is roughly constant over the range of detectable frequencies. The amplitude of the signals emitted in the dance language is 5 to 10 times higher, so we can conclude that bees can easily detect the dance sounds.     

Discrimination of nestmate workers and drones in honeybees

Summary Discrimination of nestmates from non-nestmates has mainly been investigated in female social insects. Little is known about discrimination of males. Here we show that under natural conditions at the nest entrance, honeybee workers can discriminate nestmate drones from non-nestmate drones as effectively as they can discriminate nestmate workers from non-nestmate workers.     

Pattern recognition in honeybees: chromatic properties of orientation analysis

The spectral properties of the discrimination of pattern orientation in freely flying honeybees (Apis mellifera) were examined. Bees were trained to discriminate between two random black/white gratings oriented perpendicularly to each other, one of which was associated with a reward. Subsequently the bees were tested on two-colour gratings or gratings consisting of grey and coloured stripes, providing a range of different chromatic contrasts, luminance contrasts and specific channel contrasts. The results of these experiments indicate that orientation analysis in the honeybee is mediated almost exclusively by the green receptor channel, although the bee's visual system as a whole is endowed with excellent trichromatic colour vision.     

Pattern recognition in honeybees: eidetic imagery and orientation discrimination

The roles of eidetic imagery and orientational cues, respectively, in the discrimination of visual patterns by honeybees (Apis mellifera) were evaluated by training the bees to discriminate between patterns consisting of periodic, black and white square wave gratings. Training and tests with a number of different pairs of patterns revealed that bees use orientational cues almost exclusively, if such are present, and make use of eidetic images only when orientational cues are not available. On the other hand, if a pattern carries strong orientational cues, bees learn the orientation even if it is irrelevant to the discrimination task on which they are trained.     

Pore canals in the cornea of a functionally specialized area of the honey bee's compound eye

Summary The fine structure of the cornea in an anatomically and functionally specialized part of the honey bee's compound eye (dorsal rim area) was examined by light microscopy, transmission electron and scanning electron microscopy. Under incident illumination the cornea appears grey and cloudy, leaving only the centers of the corneal lenses clear. This is due to numerous pore canals that penetrate the cornea from the inside, ending a few m below the outer surface. They consist of (1) a small cylindrical cellular evagination of a pigment cell (proximal), and (2) a rugged-walled, pinetree-shaped extracellular part (distal). The functional significance of these pore canals is discussed. It is concluded that their light scattering properties cause the wide visual fields of the photoreceptor cells measured electrophysiologically in the dorsal rim area, and that this is related to the way this eye region detects polarization in skylight.     

Detection of coloured stimuli by honeybees: minimum visual angles and receptor specific contrasts

Honeybees Apis mellifera were trained to distinguish between the presence and the absence of a rewarded coloured spot, presented on a vertical, achromatic plane in a Y-maze. They were subsequently tested with different subtended visual angles of that spot, generated by different disk diameters and different distances from the decision point in the device. Bees were trained easily to detect bee-chromatic colours, but not an achromatic one. Chromatic contrast was not the only parameter allowing learning and, therefore, detection: _min, the subtended visual angle at which the bees detect a given stimulus with a probability P ₀ = 0.6, was 5° for stimuli presenting both chromatic contrast and contrast for the green photoreceptors [i.e. excitation difference in the green photoreceptors, between target and background (green contrast)], and 15° for stimuli presenting chromatic but no green contrast. Our results suggest that green contrast can be utilized for target detection if target recognition has been established by means of the colour vision system. The green-contrast signal would be used as a far-distance signal for flower detection. This signal would always be detected before chromatic contrast during an approach flight and would be learned in compound with chromatic contrast, in a facilitation-like process.     

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.     

Thermal behavior of round and wagtail dancing honeybees

The thermal behavior of round and wagtail dancing honeybees (Apis mellifera carnica) gathering sucrose solutions of concentrations between 0.5 and 2 mol·l^-1 was investigated under field conditions by infrared thermography (30–506 m flight distance). During the stay inside the hive thoracic surface temperature ranged from 31.4 to 43.9 °C. In both round and wagtail dancing honeybees the concentration of sucrose in the food influenced dancing temperature in a non-linear way. Average dancing temperature was 37.9 °C in foragers gathering a 0.5 mol·l^-1 sucrose solution, 40.1°C with a 1 mol·l^-1, 40.6°C with a 1.5 mol·l^-1 and 40.7°C with a 2 mol·l^-1 solution. The variability of thoracic temperature was highest with the 0.5 mol·l^-1 and lowest with the 1.5 and 2 mol·l^-1 concentrations. Thoracic temperatures during trophallactic contact with hive bees were similar to dancing temperature at 1.5 mol·l^-1 but lower at the other concentrations. During periods of distribution of food to hive bees (trophallactic contact >2.5s) the dancers' thorax cooled down by more than 0.5°C considerably more frequently with the 0.5 mol·l^-1 solution (65% of cases) than with the 1.5 mol·l^-1 solution (26%). By contrast, heating the thorax up by more than 0.5°C was infrequent with the 0.5 mol·l^-1 solution (2%) but occurred at a maximum rate of 26% with the 1.5 mol·l^-1 solution. Bees gathering the 1 or 2 mol·l^-1 solutions showed intermediate behavior. Linear model analysis showed that at higher concentrations the dancers compensated better for variations of hive air temperature: per 1 °C increase of hive temperature dancing temperature increased by 0.34, 0.22, 0.12, and 0.13 °C with 0.5, 1, 1.5, and 2 mol·l^-1 sucrose solutions, respectively. The results furnish evidence that dancing honeybees follow a strategy of selective heterothermy by tuning their thermal behavior to the needs of the behavior performed at the moment. Thoracic temperature is regulated to a high level and more accurately when fast exploitation of profitable food sources is recommended. Thoracic temperature is lowered when the ratio of gain to costs of foraging becomes more unfavorable.Abbreviations SD standard deviation - SD _reg SD around regression line - H _rel relative humidity at feeding station - T _a air temperature at feeding station - T _i air temperature near the dancers - T _d Thoracic surface temperatures - T _d dancing - T _tr trophallactic contact (distribution of food) - T _w walking - T _stay mean temperature of total stay in the hive     

Estimating the genetic variance of group characters: social behaviour of honeybees (Apis mellifera L.)

Summary A new approach is presented to estimate the genetic variance of social behaviour of groups. Honeybees (Apis mellifera L.) are used as an example for highly social organisms. Most characters of economic importance strongly rely on collective group characters of honeybee colonies. The average relatedness between small groups of workers of one honeybee colony can be estimated using a discrete multinomial distribution. The genetic variance of a social behaviour (alarm behaviour) of groups of honeybee workers is estimated with the intraclass correlation between groups within a colony. In two populations tested, the coefficient of genetic determination was high (0.96–0.98) indicating that the metabolic bio-assay used was only weakly affected by environmental effects.     

Age and rearing environment interact in the retention of early olfactory memories in honeybees

Due to the changing behavioral contexts at which social insects are exposed during the adult lifespan, they are ideal models to analyze the effect of particular sensory stimuli during young adulthood on later behavior. Specifically, our goal is to understand early influences on later foraging behavior. For that, olfactory memories were established by worker honeybees to different pre-foraging ages using either (1) classical conditioning in the proboscis extension response (PER) paradigm or (2) the offering of scented-sugar solution under different rearing conditions. By testing long-term memories (LTM) through a single PER test in workers of foraging ages (17-25 days), we found that retention of the early olfactory memories in honey bees is age-dependent and not time-dependent. Independently of the environmental conditions in which they were reared (laboratory cages or hives), bees were able to retain food-odor association from 5 days after emergence, but rarely before. In most experiments we observed a bi-modal pattern of response: bees exposed to scented-food at 5-8 and 13-16 days showed better retention than those exposed at 9-12 days. These differences disappeared for bees reared in hives. Retrieval of LTMs depending on the timing and the continuous inputs of appropriate sensory stimuli are discussed.     

Pollination disruption by European honeybees in the Australian bird-pollinated shrubGrevillea barklyana (Proteaceae)

European honeybees (Apis mellifera) were less efficient pollinators ofGrevillea barklyana than nectar-feeding birds. Nectar-collecting honeybees did not contact reproductive parts of flowers. Pollen-collecting honeybees preferentially visited malestage flowers but rarely visited female-stage flowers. Fruit set on caged inflorescences that allowed access to honeybees but excluded birds was reduced by more than 50% compared to inflorescences that were visited by both types of visitors. Further, fruit set on caged inflorescences was less than on bagged inflorescences that excluded both birds and honeybees, indicating that pollen removal by bees decreased opportunities for delayed autonomous selfing in the absence of birds. Although fruit set was not pollen-limited at the study site, pollen removal by honeybees would decrease fruit set in small populations where birds are scarce. In addition, pollen removal by honeybees would reduce opportunities for outcrossing and reproductive success through male function. Although honeybees have been in Australia for insufficient time to have exerted selection on floral traits, evolutionary shifts in response to these animals are likely to occur in the future.     

Descriptive study of antennation during trophallactic unloading contacts in honeybees <Emphasis Type="Italic">Apis mellifera carnica</Emphasis>

Summary  Trophallaxis, the mouth-to-mouth transfer of food, is a widespread behavior occurring between individuals of eusocial insect societies. Antennal movements during food transfer are, in honeybees, too rapid to be characterized using standard video recordings. Using a high-speed camera (200 frames/s), we recorded nectar unloading performed by forager honeybees (Apis mellifera carnica Spinola) within the hive once they returned from collecting sugar solution at a feeder that delivered nectar at a variable rate. Frequency patterns attained a mean value of 13 Hz. Antennation intensity showed a tendency to increase with the reward rate recently exploited by the food donor. This raises the question whether or not antennation intensity is a reliable parameter providing modulatory information related to food-source profitability.Received 12 September 2002; revised 21 March 2002; accepted 24 April 2003.     

Odor preference in honeybees as a function of amount of reward: Tests of two explanations

How does a foraging honeybee come to prefer a color or odor paired with the large of two amounts of sucrose solution to a color or odor paired with the smaller amount? One hypothesis is that the attractiveness of a color or odor is based on the strength of its association with the taste of sucrose, which increases with the duration of concurrent color-taste or odor-taste stimulation. Another hypothesis is that the attractiveness of a color or odor is based on association with the afferent consequences of feeding, which are different for the two amounts. Both hypotheses were tested in experiments on proboscis-extension conditioning, a technique that provides better control of stimulation than is possible in work with free-flying foragers. In Experiments 1–3, which were designed to test the first hypothesis, an odor that accompanied the ingestion of sucrose on training trials was found to elicit extension of the proboscis when subsequently it was presented alone, but the duration of concurrent stimulation had no significant effect on the probability or persistence of the response. In Experiments 4 and 5, which were designed to test the second hypothesis, an odor that immediately followed the ingestion of sucrose on training trials failed to elicit extension of the proboscis when subsequently it was presented alone. The results support neither hypothesis.     

Variation in worker response to honey bee (Apis mellifera L.) queen mandibular pheromone (Hymenoptera: Apidae)

Genetic and environmental influences on the worker honey bee retinue response to queen mandibular gland pheromone (QMP) were investigated. Worker progeny were reared from queens originating from four sources: Australia, New Zealand, and two locations in British Columbia, Canada (Simon Fraser University and Vancouver Island). Progeny from New Zealand queens responded significantly higher (P < 0.05) than progeny from Australia in a QMP retinue bioassay. Retinue response was not related to queen production of pheromone or colony environment, and the strain-dependent differences in retinue bioassay responses were maintained over a wide range of dosages. Selected high- and low-responding colonies were bioassayed over the course of 1 year. High-responding colonies contacted QMP lures more frequently than low-responding colonies (P < 0.05) throughout the year except in late summer. We conclude that there is a strong genetic component to QMP response by worker honey bees, as well as a seasonal effect on response.