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Differential parallel processing of olfactory information in the honeybee, Apis mellifera L.

Two distinct neuronal pathways connect the first olfactory neuropil, the antennal lobe, with higher integration areas, such as the mushroom bodies, via antennal lobe projection neurons. Intracellular recordings were used to address the question whether neuroanatomical features affect odor-coding properties. We found that neurons in the median antennocerebral tract code odors by latency differences or specific inhibitory phases in combination with excitatory phases, have a more specific activity profile for different odors and convey the information with a delay. The neurons of the lateral antennocerebral tract code odors by spike rate differences, have a broader activity profile for different odors, and convey the information quickly. Thus, rather preliminary information about the olfactory stimulus first reaches the mushroom bodies and the lateral horn via neurons of the lateral antennocerebral tract and subsequently odor information becomes more specified by activities of neurons of the median antennocerebral tract. We conclude that this neuroanatomical feature is not related to the distinction between different odors, but rather reflects a dual coding of the same odor stimuli by two different neuronal strategies focusing different properties of the same stimulus.

Action Potentials↗

Octopamine modulates responsiveness to foraging-related stimuli in honey bees (Apis mellifera).

The biogenic amine neurochemical octopamine is involved in the onset of foraging behaviour in honey bees. We tested the hypothesis that octopamine influences honey bee behavioural development by modulating responsiveness to task-related stimuli. We examined the effect of octopamine treatment on responsiveness to brood pheromone (an activator of foraging) and to the presence of older bees in the colony (an inhibitor of foraging in young bees). Octopamine treatment increased responsiveness to brood pheromone and decreased responsiveness to social inhibition. These results identify octopamine both as an important source of variation in response thresholds and as a modulator of pheromonal communication in insect societies. We speculate that octopamine plays more than one role in the organisation of behavioural development indicating a very high level of integration between the neurochemical system and the generation of complex behaviour.

Aging↗

Deciding to learn: modulation of learning flights in honeybees, Apis mellifera.

Upon discovering new sources of food, honeybees and other insects perform learning flights to memorize visual landmarks that can guide their return. Learning flights are longest following initial visits to the food and subsequently decline in duration, which suggests that the investment in learning results from an active decision modulated by a bee's accumulating experience. We document various factors that influence this decision: (1). learning flights reappear when experienced bees encounter a delay in finding food at a familiar place and the durations of such "reorientation flights" increase with the length of the delay; (2). the decay in learning flight duration over visits following such reorientation flights is more rapid than following initial discovery of the food; (3). learning flight duration increases with the visual complexity of the scene surrounding the food, and when spatial relationships among landmarks are unstable; and (4). durations of learning flights at a new feeding place are influenced by the sucrose concentration in the food. Taken together, these experiments suggest that bees can adjust their learning efforts in response to changing needs for visual information and that both sources of spatial uncertainty and the quality of the food influence the value of such information.

Animals↗

Trophallaxis in forager honeybees (Apis mellifera): resource uncertainty enhances begging contacts?

Trophallaxis among adult worker honeybees is the transfer of liquid food by mouth from one individual to another. Within the colony, nectar foragers perform offering contacts (as food-donors) to transfer the contents of their crops to recipient nest-mates and, in addition, they also perform begging contacts (as food-receivers). The biological relevance of these last interactions remains unknown. Previous evidence suggests that begging may be involved in the exchange of information on food resources that occurs naturally between employed foragers and nest-mates. This work was aimed to reveal possible connections between the information obtained while foraging and the begging behavior displayed inside the nest. Experiments were intended to (1) analyze whether chemosensory information obtained while foraging, i.e., odors and sucrose concentrations, affects begging behavior, and (2) determine whether resource uncertainty enhances begging contacts. Results showed that: (1) most begging contacts lasted less than 1 s, a duration which only allows receiving food samples from nest-mates; (2) the diversity of odors and sucrose concentrations at the feeding place enhances the occurrence of begging contacts; and (3) an increased resource uncertainty enhances the forager begging behavior. In addition, results suggest that foragers may direct their begging contacts frequently to other employed nectar foragers.

Animal Communication↗

Activity of protein kinase A and gustatory responsiveness in the honey bee ( Apis mellifera L.).

The cAMP-dependent protein kinase A is involved in the induction of long-term memory and habituation in the bee. Gustatory responsiveness correlates strongly with associative and non-associative learning in bees. We tested whether protein kinase A activity in the antennal lobes correlates with gustatory responsiveness. Thirty minutes after feeding, bees with high gustatory responsiveness had a significantly higher protein kinase A activity than bees with low responsiveness. Ninety minutues after feeding, when gustatory responsiveness had increased in initially unresponsive bees, no changes in protein kinase A activity were found. We also tested time-dependent effects of protein kinase A activator and protein kinase A inhibitor on gustatory responsiveness. Injection of the protein kinase A activator adenosine 3'5'-cyclic monophosphate 8-bromo-sodium salt or of the protein kinase A inhibitor KT 5720 did not affect gustatory responsiveness within the first 4 h after treatment. Feeding of adenosine 3'5'-cyclic monophosphate 8-bromo-sodium salt over 4 days increased gustatory responsiveness in newly emerged bees and adult foragers. These results enable us to distinguish between two different forms of gustatory responsiveness: basal and transient gustatory responsiveness. Basal gustatory responsiveness correlates with protein kinase A activity and can only be modulated in the range of several days. Transient gustatory responsiveness appears to be independent of protein kinase A activity and can be modulated in the range of minutes to hours.

Animals↗

Effect of pheromones, hormones, and handling on sucrose response thresholds of honey bees (Apis mellifera L.).

The responsiveness of bees to sucrose is an important indicator of honey bee foraging decisions. Correlated with sucrose responsiveness is forage choice behavior, age of first foraging, and conditioned learning response. Pheromones and hormones are significant components in social insect systems associated with the regulation of colony-level and individual foraging behavior. Bees were treated to different exposure regimes of queen and brood pheromones and their sucrose responsiveness measured. Bees reared with queen or brood pheromone were less responsive than controls. Our results suggest responsiveness to sucrose is a physiologically, neuronally mediated response. Orally administered octopamine significantly reduced sucrose response thresholds. Change in response to octopamine was on a time scale of minutes. The greatest separation between octopamine treated and control bees occurred 30 min after feeding. There was no significant sucrose response difference to doses ranging from 0.2 mug to 20 mug of octopamine. Topically applied methoprene significantly increased sucrose responsiveness. Handling method significantly affected sucrose responsiveness. Bees that were anesthetized by chilling or CO(2) treatment were significantly more responsive than control bees 30 min after handling. Sixty minutes after handling there were no significant treatment differences. We concluded that putative stress effects of handling were blocked by anesthetic.

Anesthesia↗

The effect of complexity on the discrimination of oriented bars by the honeybee (Apis mellifera).

Visual discrimination of black bars by honeybees was studied in a Y-choice apparatus with fixed vertical patterns at constant range. The problem is to discover how bees remember different degrees of complexity of the orientation cue. Previous conclusions with parallel gratings and single bars disagree. With broad bars versus orthogonal bars, the bees learn the orientation cue if the bars are centred at the same place, but they learn the position cue in the vertical direction when the bars are at different places on the two targets. With several bars on each target, the bees learn their orientation and positions. As fixed patterns increase in complexity, the bees follow a simple rule, to look only at the range of places where the cues were displayed. The frame of reference is disrupted when a black spot is added to the training pattern. There is abundant evidence that the bees do not re-assemble the pattern or learn shapes. The filters that detect the position and orientation cues are coarsely tuned, so that they respond in a graded way, but the memory of the range of directions of the cue, as seen from the point of choice, is more exact.

Animals↗

Pharmacology of the neuronal nicotinic acetylcholine receptor of cultured Kenyon cells of the honeybee, Apis mellifera.

We investigated the pharmacology of the nicotinic acetylcholine receptor of honeybee Kenyon cells, a subset of olfactory interneurons, which are crucial for olfactory learning and memory. Whole-cell currents were recorded using patch-clamp techniques. Pressure application of agonists induced inward currents in cultured Kenyon cells at holding potentials of -110 mV. Acetylcholine or carbamylcholine were full agonists, nicotine, epibatidine and cytisine were only partial agonists. Coapplications of these partial agonists with acetylcholine reduced the current amplitude. The most efficient antagonists were dihydroxy-beta-erythroidine (EC(50)=0.5 pmol x l(-1)) and methyllycaconitine (EC(50)=24 pmol x l(-1)). The open channel blocker mecamylamine, d-tubocurarine and hexamethonium were rather weak blockers of the honeybee nicotinic response. Bath applications of the muscarinic antagonist atropine inhibited nicotinic currents dependent on concentration (EC(50)=24.3 micromol x l(-1)). Muscarine, pilocarpine or oxotremorine (1 mmol x l(-1)) did not induce any measurable currents. The non-cholinergic drugs strychnine, bicuculline and picrotoxin partially and reversibly blocked the acetylcholine-induced currents. Our results indicate the expression of only one nicotinic acetylcholine receptor subtype in cultured Kenyon cells. Muscarinic as well as non-cholinergic antagonists also inhibit the receptor function, distinguishing the honeybee nicotinic receptor from the "typical" nicotinic receptor of vertebrates and from many described insects receptors.

Animals↗

Antennal sucrose perception in the honey bee (Apis mellifera L.): behaviour and electrophysiology.

Physiological mechanisms of antennal sucrose perception in the honey bee were analysed using behavioural and electrophysiological methods. Following sucrose stimulation of the tip of a freely moving antenna, the latency of proboscis extension was 320-340 ms, 80-100 ms after the first activity in muscle M17 controlling this response. When bees were allowed to actively touch a sucrose droplet with one antenna, contacts with the solution were frequent with durations of 10-20 ms and average intervals between contacts of approximately 40 ms. High sucrose concentrations led to short and frequent contacts. The proboscis response and M17 activity were largely independent of stimulus duration and temporal pattern. Taste hairs of the antennal tip displayed spike responses to sucrose concentrations down to at least 0.1%. The first 25 ms of the response were suitable for discrimination of sucrose concentrations. This time interval corresponds to the duration of naturally occurring gustatory stimuli. Sucrose responses between different hairs on the same antenna showed a high degree of variability, ranging from less than five to over 40 spikes per 0.5 s for a stimulus of 0.1% sucrose. This variability of receptor responses extends the dynamic range of sucrose perception over a large range of concentrations.

Action Potentials↗

Intensity and the ratios of compounds in the scent of snapdragon flowers affect scent discrimination by honeybees (Apis mellifera).

Floral scent is used by pollinators during foraging to identify and discriminate among flowers. The ability to discriminate among scents may depend on both scent intensity and the ratios of the concentrations of the volatile compounds of a complex mixture rather than on the presence of a few compounds. We used four scent-emitting cultivars of snapdragon (Antirrhinum majus) to test this hypothesis by examining the ability of honeybees to differentiate among their scents. Each cultivar produced three monoterpenes (myrcene, E-beta-ocimene, and linalool) and five phenylpropanoids (methylbenzoate, acetophenone, dimethoxytoluene, cis-methylcinnamate, and trans-methylcinnamate). Cultivars were reliably classified by their scents in a canonical discriminant analysis. Honeybees were unable to discriminate among the scents of flowers of the same cultivar in our assay. The ability of honeybees to discriminate among the scents of different cultivars was a function of the intensity of the floral scent. Discrimination was also correlated to the distance among the scents described by the discriminant analysis; the cultivars that had the greatest differences observed in the discriminant analysis were the easiest to discriminate. Our results show that honeybees are capable of using all of the floral volatiles to discriminate subtle differences in scent.

Animals↗

Recognition of a familiar place by the honeybee (Apis mellifera).

Recent work shows that at any one place bees detect a limited variety of simple cues in parallel. At each choice point, they recognize a few cues in the range of positions where the cues occurred during the learning process. There is no need to postulate that they re-assemble the surrounding panorama in memory; only that they retain memories of the coincidences of cues in the expected retinotopic directions. The cues could be stimuli that excite groups of peripheral visual neurons. All the experimentally known cues are described, including modulation of the receptors, the locations of areas of black or colour, the nearness, size, averaged edge orientation, and radial and tangential edges. Cues of each type are separately summed within large fields, the size of which varies with the cue. Local orientation cues from edges at right angles cancel each other within each field, which also suggests that the discrimination of shape and texture is limited. Resolution depends on lateral interactions and the number of ommatidia required for each cue. To identify a new place, a few sparse cues, together with their directions, are learned in orientation flights. When the bee returns, the cues in the panorama are progressively matched as they coincide with the cues in memory. The limited number of cues, though economical for memory, may restrict the foraging behaviour and lead to flower constancy. This kind of a visual system is a candidate model for other animals or machines with economical processing systems.

Animals↗

The functions of antennal mechanoreceptors and antennal joints in tactile discrimination of the honeybee (Apis mellifera L.).

Honeybees learn and discriminate excellently between different surface structures and different forms of objects, which they scan with their antennae. The sensory plate on the antennal tip plays a key role in the perception of mechanosensory and gustatory information. It is densely covered with small tactile hairs and carries a few large taste hairs. Both types of sensilla contain a mechanoreceptor, which is involved in the antennal scanning of an object. Our experiments test the roles of the mechanoreceptors on the antennal tip in tactile antennal learning and discrimination. Joints between head capsule and scapus and between scapus and pedicellus enable the bee to perform three-dimensional movements when they scan an object. The role of these joints in tactile antennal learning and discrimination is studied in separate experiments. The mechanoreceptors on the antennal tip were decisive for surface discrimination, but not for tactile acquisition or discrimination of shapes. When the scapus-pedicellus joint or the headcapsule-scapus joint was fixed on both antennae, tactile learning was still apparent but surface discrimination was abolished. Fixing both scapi to the head capsule reduced tactile acquisition.

Animals↗

How long will honey bees (Apis mellifera L.) be stimulated by scent to revisit past-profitable forage sites?

Honey bees utilise floral food sources that vary temporally in their relative and absolute quality. Via a sophisticated colony organisation, a honey bee colony allocates its foragers such that the colony focuses on the most profitable forage sites while keeping track of changes within its foraging environment. One important mechanism of the allocation of foragers is the ability of experienced foragers to revisit past-profitable forage sites after a period of temporary dearth caused by, for example, inclement weather. The scent of past-profitable forage within the colony brought back by other foragers is sufficient to reactivate these experienced foragers. Here I determine for how long bees react to the scent of a past-profitable forage site. I show that the ability of foragers to revisit the location of a past-profitable food source diminishes rapidly over a period of 10 days, until no forager reacts to the cue (scent). I discuss the implications of these findings with respect to the colony's ability to react rapidly to changing foraging conditions.

Animals↗

Increase in dance imprecision with decreasing foraging distance in the honey bee Apis mellifera 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 dance 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.

Animal Communication↗

The effects of rearing temperature on developmental stability and learning and memory in the honey bee, Apis mellifera.

Honey bee workers maintain the brood nest of their colony within a narrow temperature range of 34.5+/-1.5 degrees C, implying that there are significant fitness costs if brood is reared outside the normal range. However, the effects of abnormal incubation temperatures are subtle and not well documented. Here we show that short-term learning and memory abilities of adult workers are affected by the temperature they experienced during pupal development. In contrast, long-term learning and memory is not significantly affected by rearing temperature. Furthermore, we could detect no effects of incubation temperature on fluctuating asymmetry, as a measure of developmental stability, in workers, queens or drones. We conclude that the most important consequence of abnormal rearing temperatures are subtle neural deficiencies affecting short-term memory rather than physical abnormalities.

Animals↗

Associative visual learning, color discrimination, and chromatic adaptation in the harnessed honeybee Apis mellifera L.

We studied associative visual learning in harnessed honeybees trained with monochromatic lights associated with a reward of sucrose solution delivered to the antennae and proboscis, to elicit the proboscis extension reflex (PER). We demonstrated five properties of visual learning under these conditions. First, antennae deprivation significantly increased visual acquisition, suggesting that sensory input from the antennae interferes with visual learning. Second, covering the compound eyes with silver paste significantly decreased visual acquisition, while covering the ocelli did not. Third, there was no significant difference in the visual acquisition between nurse bees, guard bees, and foragers. Fourth, bees conditioned with a 540-nm light stimulus exhibited light-induced PER with a 618-nm, but not with a 439-nm light stimulus. Finally, bees conditioned with a 540-nm light stimulus exhibited PER immediately after the 439-nm light was turned off, suggesting that the bees reacted to an afterimage induced by prior adaptation to the 439-nm light that might be similar to the 540-nm light.

Acclimatization↗

Selective modulation of task performance by octopamine in honey bee (Apis mellifera) division of labour.

Octopamine treatment has previously been shown to increase honey bee foraging behaviour. We determined the effects of octopamine on other tasks to learn how octopamine affects division of labour in honey bee colonies. Octopamine treatment did not increase the rate of corpse removal from the hive, suggesting that elevated brain levels of octopamine do not act to increase the performance of all flight-related tasks. Octopamine treatment also did not increase attendance in the queen's retinue, suggesting that elevated brain levels of octopamine do not act to increase responsiveness to all olfactory stimuli. Consistent with these findings, octopamine treatment enhanced the foraging response to brood pheromone but not the cell capping response, a component of brood care. These results demonstrate a relatively specific form of neuromodulation by octopamine in the regulation of division of labour in honey bee colonies.

Animals↗

Locomotion and the pollen hoarding behavioral syndrome of the honeybee (Apis mellifera L.).

Honeybees selected for the colony level phenotype of storing large quantities of pollen (pollen hoarding) in the nest exhibit greater walking activity than those selected against pollen hoarding. In this study, we use a simple walking assay to demonstrate that walking activity increases with the proportion of high pollen-hoarding alleles in pure and backcrossed strains of bees (high-strain bees > offspring generated from a high backcross > offspring generated from a low backcross > low-strain bees). The trait is heritable but is not associated with markers linked to three quantitative trait loci (QTL) mapped for their effects on pollen hoarding with demonstrated pleiotropic effects on pollen and nectar foraging and learning behavior. However, locomotion in non-selected bees is correlated with responsiveness to sucrose, a trait that correlates with foraging and learning behavior. We propose that pollen-hoarding behavior involves a syndrome of behavioral traits with complex genetic and regulatory architectures that span sensory sensitivity, foraging behavior, and learning. We propose that locomotor activity is the component of this syndrome and reflects the early maturation of the bees that become pollen foragers.

Animals↗